Receptor Properties and Features of Cytokinin Signaling
Identifieur interne : 000D83 ( Pmc/Corpus ); précédent : 000D82; suivant : 000D84Receptor Properties and Features of Cytokinin Signaling
Auteurs : S. N. Lomin ; D. M. Krivosheev ; M. Yu. Steklov ; D. I. Osolodkin ; G. A. RomanovSource :
- Acta Naturae [ 2075-8251 ] ; 2012.
Abstract
Cytokinins belong to one of the most important and well-known classes of plant hormones. Discovered over half a century ago, cytokinins have retained the attention of researchers due to the variety of the effects they have on the growth and development of vegetable organisms, their participation in a plant adaptation to external conditions, and the potential to be used in biotechnology, agriculture, medicine and even cosmetics. The molecular mechanism by which cytokinins function remained unknown for a long time. Things started to change only in the 21stcentury, after the discovery of the receptors for these phytohormones. It appeared that plants found ways to adapt a two-component signal transduction system borrowed from prokaryotic organisms for cytokinin signalling. This review covers the recent advances in research of the molecular basis for the perception and transduction of the cytokinin signal. Emphasis is placed on cytokinin receptors, their domain and three-dimensional structures, subcellular localization, signalling activity, effect of mutations, ligand-binding properties, and phylogeny.
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PubMed: 23150802
PubMed Central: 3491891
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Receptor Properties and Features of Cytokinin
Signaling</title><author><name sortKey="Lomin, S N" sort="Lomin, S N" uniqKey="Lomin S" first="S. N." last="Lomin">S. N. Lomin</name><affiliation><nlm:aff id="AF1">Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya Str., 35, Moscow, Russia,127276</nlm:aff></affiliation></author><author><name sortKey="Krivosheev, D M" sort="Krivosheev, D M" uniqKey="Krivosheev D" first="D. M." last="Krivosheev">D. M. Krivosheev</name><affiliation><nlm:aff id="AF1">Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya Str., 35, Moscow, Russia,127276</nlm:aff></affiliation></author><author><name sortKey="Steklov, M Yu" sort="Steklov, M Yu" uniqKey="Steklov M" first="M. Yu." last="Steklov">M. Yu. Steklov</name><affiliation><nlm:aff id="AF1">Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya Str., 35, Moscow, Russia,127276</nlm:aff></affiliation></author><author><name sortKey="Osolodkin, D I" sort="Osolodkin, D I" uniqKey="Osolodkin D" first="D. I." last="Osolodkin">D. I. Osolodkin</name><affiliation><nlm:aff id="AF2">Department of Chemistry, Lomonosov Moscow State University, Leninskie Gory, 1/3, Moscow, Russia, 119991</nlm:aff></affiliation></author><author><name sortKey="Romanov, G A" sort="Romanov, G A" uniqKey="Romanov G" first="G. A." last="Romanov">G. A. Romanov</name><affiliation><nlm:aff id="AF1">Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya Str., 35, Moscow, Russia,127276</nlm:aff></affiliation><affiliation><nlm:aff id="AF3">Belozersky Institute of Physicochemical Biology, Lomonosov Moscow State University, Leninskie Gory, 1/40, Moscow, Russia, 119992</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">23150802</idno><idno type="pmc">3491891</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3491891</idno><idno type="RBID">PMC:3491891</idno><date when="2012">2012</date><idno type="wicri:Area/Pmc/Corpus">000D83</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Receptor Properties and Features of Cytokinin
Signaling</title><author><name sortKey="Lomin, S N" sort="Lomin, S N" uniqKey="Lomin S" first="S. N." last="Lomin">S. N. Lomin</name><affiliation><nlm:aff id="AF1">Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya Str., 35, Moscow, Russia,127276</nlm:aff></affiliation></author><author><name sortKey="Krivosheev, D M" sort="Krivosheev, D M" uniqKey="Krivosheev D" first="D. M." last="Krivosheev">D. M. Krivosheev</name><affiliation><nlm:aff id="AF1">Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya Str., 35, Moscow, Russia,127276</nlm:aff></affiliation></author><author><name sortKey="Steklov, M Yu" sort="Steklov, M Yu" uniqKey="Steklov M" first="M. Yu." last="Steklov">M. Yu. Steklov</name><affiliation><nlm:aff id="AF1">Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya Str., 35, Moscow, Russia,127276</nlm:aff></affiliation></author><author><name sortKey="Osolodkin, D I" sort="Osolodkin, D I" uniqKey="Osolodkin D" first="D. I." last="Osolodkin">D. I. Osolodkin</name><affiliation><nlm:aff id="AF2">Department of Chemistry, Lomonosov Moscow State University, Leninskie Gory, 1/3, Moscow, Russia, 119991</nlm:aff></affiliation></author><author><name sortKey="Romanov, G A" sort="Romanov, G A" uniqKey="Romanov G" first="G. A." last="Romanov">G. A. Romanov</name><affiliation><nlm:aff id="AF1">Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya Str., 35, Moscow, Russia,127276</nlm:aff></affiliation><affiliation><nlm:aff id="AF3">Belozersky Institute of Physicochemical Biology, Lomonosov Moscow State University, Leninskie Gory, 1/40, Moscow, Russia, 119992</nlm:aff></affiliation></author></analytic><series><title level="j">Acta Naturae</title><idno type="ISSN">2075-8251</idno><imprint><date when="2012">2012</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Cytokinins belong to one of the most important and well-known classes of plant
hormones. Discovered over half a century ago, cytokinins have retained the
attention of researchers due to the variety of the effects they have on the
growth and development of vegetable organisms, their participation in a plant
adaptation to external conditions, and the potential to be used in
biotechnology, agriculture, medicine and even cosmetics. The molecular mechanism
by which cytokinins function remained unknown for a long time. Things started to
change only in the 21<sup>st</sup>century, after the discovery of the receptors
for these phytohormones. It appeared that plants found ways to adapt a
two-component signal transduction system borrowed from prokaryotic organisms for
cytokinin signalling. This review covers the recent advances in research of the
molecular basis for the perception and transduction of the cytokinin signal.
Emphasis is placed on cytokinin receptors, their domain and three-dimensional
structures, subcellular localization, signalling activity, effect of mutations,
ligand-binding properties, and phylogeny.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Miller, C O" uniqKey="Miller C">C.O. Miller</name></author><author><name sortKey="Skoog, F" uniqKey="Skoog F">F. Skoog</name></author><author><name sortKey="Von Saltza, N M" uniqKey="Von Saltza N">N.M. von Saltza</name></author><author><name sortKey="Strong, F M" uniqKey="Strong F">F.M. Strong</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Mok, M C" uniqKey="Mok M">M.C. Mok</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Taiz, L" uniqKey="Taiz L">L. Taiz</name></author><author><name sortKey="Zeiger, E" uniqKey="Zeiger E">E. Zeiger</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Romanov, G A" uniqKey="Romanov G">G.A. Romanov</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Romanov, G A" uniqKey="Romanov G">G.A. Romanov</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Choi, J" uniqKey="Choi J">J. Choi</name></author><author><name sortKey="Choi, D" uniqKey="Choi D">D. Choi</name></author><author><name sortKey="Lee, S" uniqKey="Lee S">S. Lee</name></author><author><name sortKey="Ryu, C M" uniqKey="Ryu C">C.-M. Ryu</name></author><author><name sortKey="Hwang, I" uniqKey="Hwang I">I. Hwang</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Zalabak, D" uniqKey="Zalabak D">D. Zalabák</name></author><author><name sortKey="Pospisilova, H" uniqKey="Pospisilova H">H. Pospíšilová</name></author><author><name sortKey="Smehilova, M" uniqKey="Smehilova M">M. Smehilová</name></author><author><name sortKey="Mrizova, K" uniqKey="Mrizova K">K. Mrízová</name></author><author><name sortKey="Frebort, I" uniqKey="Frebort I">I. Frébort</name></author><author><name sortKey="Galuszka, P" uniqKey="Galuszka P">P. Galuszka</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Ha, S" uniqKey="Ha S">S. Ha</name></author><author><name sortKey="Vankova, R" uniqKey="Vankova R">R. Vankova</name></author><author><name sortKey="Yamaguchi Shinozaki, K" uniqKey="Yamaguchi Shinozaki K">K. Yamaguchi-Shinozaki</name></author><author><name sortKey="Shinozaki, K" uniqKey="Shinozaki K">K. Shinozaki</name></author><author><name sortKey="Tran, L S" uniqKey="Tran L">L.S. Tran</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Gold Von Simson, G" uniqKey="Gold Von Simson G">G. Gold-von Simson</name></author><author><name sortKey="Goldberg, J D" uniqKey="Goldberg J">J.D. Goldberg</name></author><author><name sortKey="Rolnitzky, L M" uniqKey="Rolnitzky L">L.M. Rolnitzky</name></author><author><name sortKey="Mull, J" uniqKey="Mull J">J. Mull</name></author><author><name sortKey="Leyne, M" uniqKey="Leyne M">M. Leyne</name></author><author><name sortKey="Voustianiouk, A" uniqKey="Voustianiouk A">A. Voustianiouk</name></author><author><name sortKey="Slaugenhaupt, S A" uniqKey="Slaugenhaupt S">S.A. Slaugenhaupt</name></author><author><name sortKey="Axelrod, F B" uniqKey="Axelrod F">F.B. Axelrod</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Kolyachkina, S V" uniqKey="Kolyachkina S">S.V. Kolyachkina</name></author><author><name sortKey="Tararov, V I" uniqKey="Tararov V">V.I. Tararov</name></author><author><name sortKey="Alexeev, C S" uniqKey="Alexeev C">C.S. Alexeev</name></author><author><name sortKey="Krivosheev, D M" uniqKey="Krivosheev D">D.M. Krivosheev</name></author><author><name sortKey="Romanov, G A" uniqKey="Romanov G">G.A. Romanov</name></author><author><name sortKey="Stepanova, E V" uniqKey="Stepanova E">E.V. Stepanova</name></author><author><name sortKey="Solomko, E S" uniqKey="Solomko E">E.S. Solomko</name></author><author><name sortKey="Inshakov, A N" uniqKey="Inshakov A">A.N. Inshakov</name></author><author><name sortKey="Mikhailov, S N" uniqKey="Mikhailov S">S.N. Mikhailov</name></author></analytic></biblStruct><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Inoue, T" uniqKey="Inoue T">T. Inoue</name></author><author><name sortKey="Higuchi, M" uniqKey="Higuchi M">M. Higuchi</name></author><author><name sortKey="Hashimoto, Y" uniqKey="Hashimoto Y">Y. Hashimoto</name></author><author><name sortKey="Seki, M" uniqKey="Seki M">M. Seki</name></author><author><name sortKey="Kobayashi, M" uniqKey="Kobayashi M">M. Kobayashi</name></author><author><name sortKey="Kato, T" uniqKey="Kato T">T. Kato</name></author><author><name sortKey="Tabata, S" uniqKey="Tabata S">S. Tabata</name></author><author><name sortKey="Shinozaki, K" uniqKey="Shinozaki K">K. Shinozaki</name></author><author><name sortKey="Kakimoto, T" uniqKey="Kakimoto T">T. Kakimoto</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Suzuki, T" uniqKey="Suzuki T">T. Suzuki</name></author><author><name sortKey="Miwa, K" uniqKey="Miwa K">K. Miwa</name></author><author><name sortKey="Ishikawa, K" uniqKey="Ishikawa K">K. Ishikawa</name></author><author><name sortKey="Yamada, H" uniqKey="Yamada H">H. Yamada</name></author><author><name sortKey="Aiba, H" uniqKey="Aiba H">H. Aiba</name></author><author><name sortKey="Mizuno, T" uniqKey="Mizuno T">T. Mizuno</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Ueguchi, C" uniqKey="Ueguchi C">C. Ueguchi</name></author><author><name sortKey="Sato, S" uniqKey="Sato S">S. Sato</name></author><author><name sortKey="Kato, T" uniqKey="Kato T">T. Kato</name></author><author><name sortKey="Tabata, S" uniqKey="Tabata S">S. Tabata</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Yamada, H" uniqKey="Yamada H">H. Yamada</name></author><author><name sortKey="Suzuki, T" uniqKey="Suzuki T">T. Suzuki</name></author><author><name sortKey="Terada, K" uniqKey="Terada K">K. Terada</name></author><author><name sortKey="Takei, K" uniqKey="Takei K">K. Takei</name></author><author><name sortKey="Ishikawa, K" uniqKey="Ishikawa K">K. Ishikawa</name></author><author><name sortKey="Miwa, K" uniqKey="Miwa K">K. Miwa</name></author><author><name sortKey="Yamashino, T" uniqKey="Yamashino T">T. Yamashino</name></author><author><name sortKey="Mizuno, T" uniqKey="Mizuno T">T. Mizuno</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="M Honen, A P" uniqKey="M Honen A">A.P. Mähönen</name></author><author><name sortKey="Bonke, M" uniqKey="Bonke M">M. Bonke</name></author><author><name sortKey="Kauppinen, L" uniqKey="Kauppinen L">L. Kauppinen</name></author><author><name sortKey="Riikonen, M" uniqKey="Riikonen M">M. Riikonen</name></author><author><name sortKey="Benfey, P N" uniqKey="Benfey P">P.N. Benfey</name></author><author><name sortKey="Helariutta, Y" uniqKey="Helariutta Y">Y. Helariutta</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Ueguchi, C" uniqKey="Ueguchi C">C. Ueguchi</name></author><author><name sortKey="Koizumi, H" uniqKey="Koizumi H">H. Koizumi</name></author><author><name sortKey="Suzuki, T" uniqKey="Suzuki T">T. Suzuki</name></author><author><name sortKey="Mizuno, T" uniqKey="Mizuno T">T. Mizuno</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Anantharaman, V" uniqKey="Anantharaman V">V. Anantharaman</name></author><author><name sortKey="Aravind, L" uniqKey="Aravind L">L. Aravind</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Mougel, C" uniqKey="Mougel C">C. Mougel</name></author><author><name sortKey="Zhulin, I B" uniqKey="Zhulin I">I.B. Zhulin</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Wolanin, P M" uniqKey="Wolanin P">P.M. Wolanin</name></author><author><name sortKey="Thomason, P A" uniqKey="Thomason P">P.A. Thomason</name></author><author><name sortKey="Stock, J B" uniqKey="Stock J">J.B. Stock</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Heyl, A" uniqKey="Heyl A">A. Heyl</name></author><author><name sortKey="Schmulling, T" uniqKey="Schmulling T">T. Schmülling</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Maxwell, B B" uniqKey="Maxwell B">B.B. Maxwell</name></author><author><name sortKey="Kieber, J J" uniqKey="Kieber J">J.J. Kieber</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Schaller, G E" uniqKey="Schaller G">G.E. Schaller</name></author><author><name sortKey="Kieber, J J" uniqKey="Kieber J">J.J. Kieber</name></author><author><name sortKey="Shiu, S H" uniqKey="Shiu S">S.-H. Shiu</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Schaller, G E" uniqKey="Schaller G">G.E. Schaller</name></author><author><name sortKey="Shiu, S H" uniqKey="Shiu S">S.-H. Shiu</name></author><author><name sortKey="Armitage, J P" uniqKey="Armitage J">J.P. Armitage</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="West, A H" uniqKey="West A">A.H. West</name></author><author><name sortKey="Stock, A M" uniqKey="Stock A">A.M. Stock</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Punwani, J A" uniqKey="Punwani J">J.A. Punwani</name></author><author><name sortKey="Hutchison, C E" uniqKey="Hutchison C">C.E. Hutchison</name></author><author><name sortKey="Schaller, G E" uniqKey="Schaller G">G.E. Schaller</name></author><author><name sortKey="Kieber, J J" uniqKey="Kieber J">J.J. Kieber</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Brandstatter, I" uniqKey="Brandstatter I">I. Brandstatter</name></author><author><name sortKey="Kieber, J J" uniqKey="Kieber J">J.J. Kieber</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Rashotte, A M" uniqKey="Rashotte A">A.M. Rashotte</name></author><author><name sortKey="Carson, S D B" uniqKey="Carson S">S.D.B. Carson</name></author><author><name sortKey="To, J P C" uniqKey="To J">J.P.C. To</name></author><author><name sortKey="Kieber, J J" uniqKey="Kieber J">J.J. Kieber</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Brenner, W G" uniqKey="Brenner W">W.G. Brenner</name></author><author><name sortKey="Romanov, G A" uniqKey="Romanov G">G.A. Romanov</name></author><author><name sortKey="Kollmer, I" uniqKey="Kollmer I">I. Köllmer</name></author><author><name sortKey="Burkle, L" uniqKey="Burkle L">L. Bürkle</name></author><author><name sortKey="Schmulling, T" uniqKey="Schmulling T">T. Schmülling</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Spichal, L" uniqKey="Spichal L">L. Spíchal</name></author><author><name sortKey="Rakova, N Y" uniqKey="Rakova N">N.Y. Rakova</name></author><author><name sortKey="Riefler, M" uniqKey="Riefler M">M. Riefler</name></author><author><name sortKey="Mizuno, T" uniqKey="Mizuno T">T. Mizuno</name></author><author><name sortKey="Romanov, G A" uniqKey="Romanov G">G.A. Romanov</name></author><author><name sortKey="Strnad, M" uniqKey="Strnad M">M. Strnad</name></author><author><name sortKey="Schmulling, T" uniqKey="Schmulling T">T. Schmülling</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Miwa, K" uniqKey="Miwa K">K. Miwa</name></author><author><name sortKey="Ishikawa, K" uniqKey="Ishikawa K">K. Ishikawa</name></author><author><name sortKey="Terada, K" uniqKey="Terada K">K. Terada</name></author><author><name sortKey="Yamada, H" uniqKey="Yamada H">H. Yamada</name></author><author><name sortKey="Suzuki, T" uniqKey="Suzuki T">T. Suzuki</name></author><author><name sortKey="Yamashino, T" uniqKey="Yamashino T">T. Yamashino</name></author><author><name sortKey="Mizuno, T" uniqKey="Mizuno T">T. Mizuno</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Higuchi, M" uniqKey="Higuchi M">M. Higuchi</name></author><author><name sortKey="Pischke, M S" uniqKey="Pischke M">M.S. Pischke</name></author><author><name sortKey="M Honen, A P" uniqKey="M Honen A">A.P. Mähönen</name></author><author><name sortKey="Miyawaki, K" uniqKey="Miyawaki K">K. Miyawaki</name></author><author><name sortKey="Hashimoto, Y" uniqKey="Hashimoto Y">Y. Hashimoto</name></author><author><name sortKey="Seki, M" uniqKey="Seki M">M. Seki</name></author><author><name sortKey="Kobayashi, M" uniqKey="Kobayashi M">M. Kobayashi</name></author><author><name sortKey="Shinozaki, K" uniqKey="Shinozaki K">K. Shinozaki</name></author><author><name sortKey="Kato, T" uniqKey="Kato T">T. Kato</name></author><author><name sortKey="Tabata, S" uniqKey="Tabata S">S. Tabata</name></author><author><name sortKey="Helariutta, Y" uniqKey="Helariutta Y">Y. Helariutta</name></author><author><name sortKey="Sussman, M R" uniqKey="Sussman M">M.R. Sussman</name></author><author><name sortKey="Kakimoto, T" uniqKey="Kakimoto T">T. Kakimoto</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Nishimura, C" uniqKey="Nishimura C">C. Nishimura</name></author><author><name sortKey="Ohashi, Y" uniqKey="Ohashi Y">Y. Ohashi</name></author><author><name sortKey="Sato, S" uniqKey="Sato S">S. Sato</name></author><author><name sortKey="Kato, T" uniqKey="Kato T">T. Kato</name></author><author><name sortKey="Tabata, S" uniqKey="Tabata S">S. Tabata</name></author><author><name sortKey="Ueguchi, C" uniqKey="Ueguchi C">C. Ueguchi</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Riefler, M" uniqKey="Riefler M">M. Riefler</name></author><author><name sortKey="Novak, O" uniqKey="Novak O">O. Novak</name></author><author><name sortKey="Strnad, M" uniqKey="Strnad M">M. Strnad</name></author><author><name sortKey="Schmulling, T" uniqKey="Schmulling T">T. Schmülling</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Shi, X" uniqKey="Shi X">X. Shi</name></author><author><name sortKey="Rashotte, A M" uniqKey="Rashotte A">A.M. Rashotte</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Tanaka, Y" uniqKey="Tanaka Y">Y. Tanaka</name></author><author><name sortKey="Suzuki, T" uniqKey="Suzuki T">T. Suzuki</name></author><author><name sortKey="Yamashino, T" uniqKey="Yamashino T">T. Yamashino</name></author><author><name sortKey="Mizuno, T" uniqKey="Mizuno T">T. Mizuno</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hutchison, C E" uniqKey="Hutchison C">C.E. Hutchison</name></author><author><name sortKey="Li, J" uniqKey="Li J">J. Li</name></author><author><name sortKey="Argueso, C" uniqKey="Argueso C">C. Argueso</name></author><author><name sortKey="Gonzalez, M" uniqKey="Gonzalez M">M. Gonzalez</name></author><author><name sortKey="Lee, E" uniqKey="Lee E">E. Lee</name></author><author><name sortKey="Lewis, M W" uniqKey="Lewis M">M.W. Lewis</name></author><author><name sortKey="Maxwell, B B" uniqKey="Maxwell B">B.B. Maxwell</name></author><author><name sortKey="Perdue, T D" uniqKey="Perdue T">T.D. Perdue</name></author><author><name sortKey="Schaller, G E" uniqKey="Schaller G">G.E. Schaller</name></author><author><name sortKey="Alonso, J M" uniqKey="Alonso J">J.M. Alonso</name></author><author><name sortKey="Ecker, J R" uniqKey="Ecker J">J.R. Ecker</name></author><author><name sortKey="Kieber, J J" uniqKey="Kieber J">J.J. Kieber</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Dortay, H" uniqKey="Dortay H">H. Dortay</name></author><author><name sortKey="Mehnert, N" uniqKey="Mehnert N">N. Mehnert</name></author><author><name sortKey="Burkle, L" uniqKey="Burkle L">L. Bürkle</name></author><author><name sortKey="Schmulling, T" uniqKey="Schmulling T">T. Schmülling</name></author><author><name sortKey="Heyl, A" uniqKey="Heyl A">A. Heyl</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Deng, Y" uniqKey="Deng Y">Y. Deng</name></author><author><name sortKey="Dong, H" uniqKey="Dong H">H. Dong</name></author><author><name sortKey="Mu, J" uniqKey="Mu J">J. Mu</name></author><author><name sortKey="Zheng, B" uniqKey="Zheng B">B. Zheng</name></author><author><name sortKey="Ji, Z" uniqKey="Ji Z">Z. Ji</name></author><author><name sortKey="Yang, W C" uniqKey="Yang W">W.-C. Yang</name></author><author><name sortKey="Liang, Y" uniqKey="Liang Y">Y. Liang</name></author><author><name sortKey="Zuo, J" uniqKey="Zuo J">J. Zuo</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Lu, J M" uniqKey="Lu J">J.M. Lu</name></author><author><name sortKey="Deschenes, R J" uniqKey="Deschenes R">R.J. Deschenes</name></author><author><name sortKey="Fassler, J S" uniqKey="Fassler J">J.S. Fassler</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="M Honen, A P" uniqKey="M Honen A">A.P. Mähönen</name></author><author><name sortKey="Bishopp, A" uniqKey="Bishopp A">A. Bishopp</name></author><author><name sortKey="Higuchi, M" uniqKey="Higuchi M">M. Higuchi</name></author><author><name sortKey="Nieminen, K M" uniqKey="Nieminen K">K.M. Nieminen</name></author><author><name sortKey="Kinoshita, K" uniqKey="Kinoshita K">K. Kinoshita</name></author><author><name sortKey="Torm Kangas, K" uniqKey="Torm Kangas K">K. Törmäkangas</name></author><author><name sortKey="Ikeda, Y" uniqKey="Ikeda Y">Y. Ikeda</name></author><author><name sortKey="Oka, A" uniqKey="Oka A">A. Oka</name></author><author><name sortKey="Kakimoto, T" uniqKey="Kakimoto T">T. Kakimoto</name></author><author><name sortKey="Helariutta, Y" uniqKey="Helariutta Y">Y. Helariutta</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Gupta, S" uniqKey="Gupta S">S. Gupta</name></author><author><name sortKey="Rashotte, A M" uniqKey="Rashotte A">A.M. Rashotte</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Lohrmann, J" uniqKey="Lohrmann J">J. Lohrmann</name></author><author><name sortKey="Sweere, U" uniqKey="Sweere U">U. Sweere</name></author><author><name sortKey="Zabaleta, E" uniqKey="Zabaleta E">E. Zabaleta</name></author><author><name sortKey="B Urle, I" uniqKey="B Urle I">I. Bäurle</name></author><author><name sortKey="Keitel, C" uniqKey="Keitel C">C. Keitel</name></author><author><name sortKey="Kozma Bognar, L" uniqKey="Kozma Bognar L">L. Kozma-Bognar</name></author><author><name sortKey="Brennicke, A" uniqKey="Brennicke A">A. Brennicke</name></author><author><name sortKey="Sch Fer, E" uniqKey="Sch Fer E">E. Schäfer</name></author><author><name sortKey="Kudla, J" uniqKey="Kudla J">J. Kudla</name></author><author><name sortKey="Harter, K" uniqKey="Harter K">K. Harter</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Sakai, H" uniqKey="Sakai H">H. Sakai</name></author><author><name sortKey="Aoyama, T" uniqKey="Aoyama T">T. Aoyama</name></author><author><name sortKey="Bono, H" uniqKey="Bono H">H. Bono</name></author><author><name sortKey="Oka, A" uniqKey="Oka A">A. Oka</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Sakai, H" uniqKey="Sakai H">H. Sakai</name></author><author><name sortKey="Aoyama, T" uniqKey="Aoyama T">T. Aoyama</name></author><author><name sortKey="Oka, A" uniqKey="Oka A">A. Oka</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hosoda, K" uniqKey="Hosoda K">K. Hosoda</name></author><author><name sortKey="Imamura, A" uniqKey="Imamura A">A. Imamura</name></author><author><name sortKey="Katoh, E" uniqKey="Katoh E">E. Katoh</name></author><author><name sortKey="Hatta, T" uniqKey="Hatta T">T. Hatta</name></author><author><name sortKey="Tachiki, M" uniqKey="Tachiki M">M. Tachiki</name></author><author><name sortKey="Yamada, H" uniqKey="Yamada H">H. Yamada</name></author><author><name sortKey="Mizuno, T" uniqKey="Mizuno T">T. Mizuno</name></author><author><name sortKey="Yamazaki, T" uniqKey="Yamazaki T">T. Yamazaki</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Mason, M G" uniqKey="Mason M">M.G. Mason</name></author><author><name sortKey="Mathews, D E" uniqKey="Mathews D">D.E. Mathews</name></author><author><name sortKey="Argyros, D A" uniqKey="Argyros D">D.A. Argyros</name></author><author><name sortKey="Maxwell, B B" uniqKey="Maxwell B">B.B. Maxwell</name></author><author><name sortKey="Kieber, J J" uniqKey="Kieber J">J.J. Kieber</name></author><author><name sortKey="Alonso, J M" uniqKey="Alonso J">J.M. Alonso</name></author><author><name sortKey="Ecker, J R" uniqKey="Ecker J">J.R. Ecker</name></author><author><name sortKey="Schaller, G E" uniqKey="Schaller G">G.E. Schaller</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Ishida, K" uniqKey="Ishida K">K. Ishida</name></author><author><name sortKey="Yamashino, T" uniqKey="Yamashino T">T. Yamashino</name></author><author><name sortKey="Yokoyama, A" uniqKey="Yokoyama A">A. Yokoyama</name></author><author><name sortKey="Mizuno, T" uniqKey="Mizuno T">T. Mizuno</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Argyros, R D" uniqKey="Argyros R">R.D. Argyros</name></author><author><name sortKey="Mathews, D E" uniqKey="Mathews D">D.E. Mathews</name></author><author><name sortKey="Chiang, Y H" uniqKey="Chiang Y">Y.-H. Chiang</name></author><author><name sortKey="Palmer, C M" uniqKey="Palmer C">C.M. Palmer</name></author><author><name sortKey="Thibault, D M" uniqKey="Thibault D">D.M. Thibault</name></author><author><name sortKey="Etheridge, N" uniqKey="Etheridge N">N. Etheridge</name></author><author><name sortKey="Argyros, D A" uniqKey="Argyros D">D.A. Argyros</name></author><author><name sortKey="Mason, M G" uniqKey="Mason M">M.G. Mason</name></author><author><name sortKey="Kieber, J J" uniqKey="Kieber J">J.J. Kieber</name></author><author><name sortKey="Schaller, G E" uniqKey="Schaller G">G.E. Schaller</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Imamura, A" uniqKey="Imamura A">A. Imamura</name></author><author><name sortKey="Hanaki, N" uniqKey="Hanaki N">N. Hanaki</name></author><author><name sortKey="Nakamura, A" uniqKey="Nakamura A">A. Nakamura</name></author><author><name sortKey="Suzuki, T" uniqKey="Suzuki T">T. Suzuki</name></author><author><name sortKey="Taniguchi, M" uniqKey="Taniguchi M">M. Taniguchi</name></author><author><name sortKey="Kiba, T" uniqKey="Kiba T">T. Kiba</name></author><author><name sortKey="Ueguchi, C" uniqKey="Ueguchi C">C. Ueguchi</name></author><author><name sortKey="Sugiyama, T" uniqKey="Sugiyama T">T. Sugiyama</name></author><author><name sortKey="Mizuno, T" uniqKey="Mizuno T">T. Mizuno</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Che, P" uniqKey="Che P">P. Che</name></author><author><name sortKey="Gingerich, D J" uniqKey="Gingerich D">D.J. Gingerich</name></author><author><name sortKey="Lall, S" uniqKey="Lall S">S. Lall</name></author><author><name sortKey="Howell, S H" uniqKey="Howell S">S.H. Howell</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Kieber, Jj" uniqKey="Kieber J">JJ. Kieber</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hwang, I" uniqKey="Hwang I">I. Hwang</name></author><author><name sortKey="Sheen, J" uniqKey="Sheen J">J. Sheen</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="To, J P" uniqKey="To J">J.P. To</name></author><author><name sortKey="Haberer, G" uniqKey="Haberer G">G. Haberer</name></author><author><name sortKey="Ferreira, F J" uniqKey="Ferreira F">F.J. Ferreira</name></author><author><name sortKey="Deruere, J" uniqKey="Deruere J">J. Deruère</name></author><author><name sortKey="Mason, M G" uniqKey="Mason M">M.G. Mason</name></author><author><name sortKey="Schaller, G E" uniqKey="Schaller G">G.E. Schaller</name></author><author><name sortKey="Alonso, J M" uniqKey="Alonso J">J.M. Alonso</name></author><author><name sortKey="Ecker, J R" uniqKey="Ecker J">J.R. Ecker</name></author><author><name sortKey="Kieber, J J" uniqKey="Kieber J">J.J. Kieber</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Lee, D J" uniqKey="Lee D">D.J. Lee</name></author><author><name sortKey="Park, J Y" uniqKey="Park J">J.Y. Park</name></author><author><name sortKey="Ku, S J" uniqKey="Ku S">S.J. Ku</name></author><author><name sortKey="Ha, Y M" uniqKey="Ha Y">Y.M. Ha</name></author><author><name sortKey="Kim, S" uniqKey="Kim S">S. Kim</name></author><author><name sortKey="Kim, M D" uniqKey="Kim M">M.D. Kim</name></author><author><name sortKey="Oh, M H" uniqKey="Oh M">M.H. Oh</name></author><author><name sortKey="Kim, J" uniqKey="Kim J">J. Kim</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Muller, B" uniqKey="Muller B">B. Müller</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="M Honen, A P" uniqKey="M Honen A">A.P. Mähönen</name></author><author><name sortKey="Higuchi, M" uniqKey="Higuchi M">M. Higuchi</name></author><author><name sortKey="Torm Kangas, K" uniqKey="Torm Kangas K">K. Törmäkangas</name></author><author><name sortKey="Miyawaki, K" uniqKey="Miyawaki K">K. Miyawaki</name></author><author><name sortKey="Pischke, M S" uniqKey="Pischke M">M.S. Pischke</name></author><author><name sortKey="Sussman, M R" uniqKey="Sussman M">M.R. Sussman</name></author><author><name sortKey="Helariutta, Y" uniqKey="Helariutta Y">Y. Helariutta</name></author><author><name sortKey="Kakimoto, T" uniqKey="Kakimoto T">T. Kakimoto</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Kim, H J" uniqKey="Kim H">H.J. Kim</name></author><author><name sortKey="Ryu, H" uniqKey="Ryu H">H. Ryu</name></author><author><name sortKey="Hong, S H" uniqKey="Hong S">S.H. Hong</name></author><author><name sortKey="Woo, H R" uniqKey="Woo H">H.R. Woo</name></author><author><name sortKey="Lim, P O" uniqKey="Lim P">P.O. Lim</name></author><author><name sortKey="Lee, I C" uniqKey="Lee I">I.C. Lee</name></author><author><name sortKey="Sheen, J" uniqKey="Sheen J">J. Sheen</name></author><author><name sortKey="Nam, H G" uniqKey="Nam H">H.G. Nam</name></author><author><name sortKey="Hwang, I" uniqKey="Hwang I">I. Hwang</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Romanov, G A" uniqKey="Romanov G">G.A. Romanov</name></author><author><name sortKey="Lomin, S N" uniqKey="Lomin S">S.N. Lomin</name></author><author><name sortKey="Schmulling, T" uniqKey="Schmulling T">T. Schmülling</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Lomin, S N" uniqKey="Lomin S">S.N. Lomin</name></author><author><name sortKey="Yonekura Sakakibara, K" uniqKey="Yonekura Sakakibara K">K. Yonekura-Sakakibara</name></author><author><name sortKey="Romanov, G A" uniqKey="Romanov G">G.A. Romanov</name></author><author><name sortKey="Sakakibara, H" uniqKey="Sakakibara H">H. Sakakibara</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Wulfetange, K" uniqKey="Wulfetange K">K. Wulfetange</name></author><author><name sortKey="Lomin, S N" uniqKey="Lomin S">S.N. Lomin</name></author><author><name sortKey="Romanov, G A" uniqKey="Romanov G">G.A. Romanov</name></author><author><name sortKey="Stolz, A" uniqKey="Stolz A">A. Stolz</name></author><author><name sortKey="Heyl, A" uniqKey="Heyl A">A. Heyl</name></author><author><name sortKey="Schmulling, T" uniqKey="Schmulling T">T. Schmülling</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Caesar, K" uniqKey="Caesar K">K. Caesar</name></author><author><name sortKey="Thamm, A M" uniqKey="Thamm A">A.M. Thamm</name></author><author><name sortKey="Witthoft, J" uniqKey="Witthoft J">J. Witthöft</name></author><author><name sortKey="Elgass, K" uniqKey="Elgass K">K. Elgass</name></author><author><name sortKey="Huppenberger, P" uniqKey="Huppenberger P">P. Huppenberger</name></author><author><name sortKey="Grefen, C" uniqKey="Grefen C">C. Grefen</name></author><author><name sortKey="Horak, J" uniqKey="Horak J">J. Horak</name></author><author><name sortKey="Harter, K" uniqKey="Harter K">K. Harter</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Chen, Y F" uniqKey="Chen Y">Y.-F. Chen</name></author><author><name sortKey="Randlett, M D" uniqKey="Randlett M">M.D. Randlett</name></author><author><name sortKey="Findell, J L" uniqKey="Findell J">J.L. Findell</name></author><author><name sortKey="Schaller, G E" uniqKey="Schaller G">G.E. Schaller</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Grefen, C" uniqKey="Grefen C">C. Grefen</name></author><author><name sortKey="St Dele, K" uniqKey="St Dele K">K. Städele</name></author><author><name sortKey="Ruzicka, K" uniqKey="Ruzicka K">K. Růzicka</name></author><author><name sortKey="Obrdlik, P" uniqKey="Obrdlik P">P. Obrdlik</name></author><author><name sortKey="Harter, K" uniqKey="Harter K">K. Harter</name></author><author><name sortKey="Horak, J" uniqKey="Horak J">J. Horák</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Mok, D W S" uniqKey="Mok D">D.W.S. Mok</name></author><author><name sortKey="Mok, M C" uniqKey="Mok M">M.C. Mok</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Takei, K" uniqKey="Takei K">K. Takei</name></author><author><name sortKey="Sakakibara, H" uniqKey="Sakakibara H">H. Sakakibara</name></author><author><name sortKey="Taniguchi, M" uniqKey="Taniguchi M">M. Taniguchi</name></author><author><name sortKey="Sugiyama, T" uniqKey="Sugiyama T">T. Sugiyama</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Corbesier, L" uniqKey="Corbesier L">L. Corbesier</name></author><author><name sortKey="Prinsen, E" uniqKey="Prinsen E">E. Prinsen</name></author><author><name sortKey="Jackmard, A" uniqKey="Jackmard A">A. Jackmard</name></author><author><name sortKey="Lejeune, P" uniqKey="Lejeune P">P. Lejeune</name></author><author><name sortKey="Van Onckelen, H" uniqKey="Van Onckelen H">H. van Onckelen</name></author><author><name sortKey="Perilleux, C" uniqKey="Perilleux C">C. Perilleux</name></author><author><name sortKey="Bernier, G" uniqKey="Bernier G">G. Bernier</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hirose, N" uniqKey="Hirose N">N. Hirose</name></author><author><name sortKey="Takei, K" uniqKey="Takei K">K. Takei</name></author><author><name sortKey="Kuroha, T" uniqKey="Kuroha T">T. Kuroha</name></author><author><name sortKey="Kamada Nobusada, T" uniqKey="Kamada Nobusada T">T. Kamada-Nobusada</name></author><author><name sortKey="Hayashi, H" uniqKey="Hayashi H">H. Hayashi</name></author><author><name sortKey="Sakakibara, H" uniqKey="Sakakibara H">H. Sakakibara</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Higuchi, M" uniqKey="Higuchi M">M. Higuchi</name></author><author><name sortKey="Kakimoto, T" uniqKey="Kakimoto T">T. Kakimoto</name></author><author><name sortKey="Mizuno, T" uniqKey="Mizuno T">T. Mizuno</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Spichal, L" uniqKey="Spichal L">L. Spíchal</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Romanov, G A" uniqKey="Romanov G">G.A. Romanov</name></author><author><name sortKey="Spichal, L" uniqKey="Spichal L">L. Spíchal</name></author><author><name sortKey="Lomin, S N" uniqKey="Lomin S">S.N. Lomin</name></author><author><name sortKey="Strnad, M" uniqKey="Strnad M">M. Strnad</name></author><author><name sortKey="Schmulling, T" uniqKey="Schmulling T">T. Schmülling</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Romanov, G A" uniqKey="Romanov G">G.A. Romanov</name></author><author><name sortKey="Lomin, S N" uniqKey="Lomin S">S.N. Lomin</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Takei, K" uniqKey="Takei K">K. Takei</name></author><author><name sortKey="Ueda, N" uniqKey="Ueda N">N. Ueda</name></author><author><name sortKey="Aoki, K" uniqKey="Aoki K">K. Aoki</name></author><author><name sortKey="Kuromori, T" uniqKey="Kuromori T">T. Kuromori</name></author><author><name sortKey="Hirayama, T" uniqKey="Hirayama T">T. Hirayama</name></author><author><name sortKey="Shinozaki, K" uniqKey="Shinozaki K">K. Shinozaki</name></author><author><name sortKey="Yamaya, T" uniqKey="Yamaya T">T. Yamaya</name></author><author><name sortKey="Sakakibara, H" uniqKey="Sakakibara H">H. Sakakibara</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Lomin, S N" uniqKey="Lomin S">S.N. Lomin</name></author><author><name sortKey="Romanov, G A" uniqKey="Romanov G">G.A. Romanov</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Stolz, A" uniqKey="Stolz A">A. Stolz</name></author><author><name sortKey="Riefler, M" uniqKey="Riefler M">M. Riefler</name></author><author><name sortKey="Lomin, S N" uniqKey="Lomin S">S.N. Lomin</name></author><author><name sortKey="Achazi, K" uniqKey="Achazi K">K. Achazi</name></author><author><name sortKey="Romanov, G A" uniqKey="Romanov G">G.A. Romanov</name></author><author><name sortKey="Schmulling, T" uniqKey="Schmulling T">T. Schmülling</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Yonekura Sakakibara, K" uniqKey="Yonekura Sakakibara K">K. Yonekura-Sakakibara</name></author><author><name sortKey="Kojima, M" uniqKey="Kojima M">M. Kojima</name></author><author><name sortKey="Yamaya, T" uniqKey="Yamaya T">T. Yamaya</name></author><author><name sortKey="Sakakibara, H" uniqKey="Sakakibara H">H. Sakakibara</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Veach, Y K" uniqKey="Veach Y">Y.K. Veach</name></author><author><name sortKey="Martin, R C" uniqKey="Martin R">R.C. Martin</name></author><author><name sortKey="Mok, D W S" uniqKey="Mok D">D.W.S. Mok</name></author><author><name sortKey="Malbeck, J" uniqKey="Malbeck J">J. Malbeck</name></author><author><name sortKey="Vankova, R" uniqKey="Vankova R">R. Vankova</name></author><author><name sortKey="Mok, M C" uniqKey="Mok M">M.C. Mok</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Vyroubalova, S" uniqKey="Vyroubalova S">S. Vyroubalová</name></author><author><name sortKey="Vaclavikova, K" uniqKey="Vaclavikova K">K. Václaviková</name></author><author><name sortKey="Ture Kova, V" uniqKey="Ture Kova V">V. Turečková</name></author><author><name sortKey="Novak, O" uniqKey="Novak O">O. Novák</name></author><author><name sortKey="Smehilova, M" uniqKey="Smehilova M">M. Šmehilová</name></author><author><name sortKey="Hluska, T" uniqKey="Hluska T">T. Hluska</name></author><author><name sortKey="Ohnoutkova, L" uniqKey="Ohnoutkova L">L. Ohnoutková</name></author><author><name sortKey="Frebort, I" uniqKey="Frebort I">I. Frébort</name></author><author><name sortKey="Galuszka, P" uniqKey="Galuszka P">P. Galuszka</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Heyl, A" uniqKey="Heyl A">A. Heyl</name></author><author><name sortKey="Riefler, M" uniqKey="Riefler M">M. Riefler</name></author><author><name sortKey="Romanov, G A" uniqKey="Romanov G">G.A. Romanov</name></author><author><name sortKey="Schmulling, T" uniqKey="Schmulling T">T. Schmülling</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Scheres, B" uniqKey="Scheres B">B. Scheres</name></author><author><name sortKey="Di Laurenzio, L" uniqKey="Di Laurenzio L">L. Di Laurenzio</name></author><author><name sortKey="Willemsen, V" uniqKey="Willemsen V">V. Willemsen</name></author><author><name sortKey="Hauser, M T" uniqKey="Hauser M">M.T. Hauser</name></author><author><name sortKey="Janmaat, K" uniqKey="Janmaat K">K. Janmaat</name></author><author><name sortKey="Weisbeek, P" uniqKey="Weisbeek P">P. Weisbeek</name></author><author><name sortKey="Benfey, P N" uniqKey="Benfey P">P.N. Benfey</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="De Leon, B G" uniqKey="De Leon B">B.G. De Leon</name></author><author><name sortKey="Franco Zorrilla, J M" uniqKey="Franco Zorrilla J">J.M. Franco Zorrilla</name></author><author><name sortKey="Rubio, V" uniqKey="Rubio V">V. Rubio</name></author><author><name sortKey="Dahiya, P" uniqKey="Dahiya P">P. Dahiya</name></author><author><name sortKey="Paz Ares, J" uniqKey="Paz Ares J">J. Paz-Ares</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Kuroha, T" uniqKey="Kuroha T">T. Kuroha</name></author><author><name sortKey="Ueguchi, C" uniqKey="Ueguchi C">C. Ueguchi</name></author><author><name sortKey="Sakakibara, H" uniqKey="Sakakibara H">H. Sakakibara</name></author><author><name sortKey="Satoh, S" uniqKey="Satoh S">S. Satoh</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Stock, A M" uniqKey="Stock A">A.M. Stock</name></author><author><name sortKey="Robinson, V L" uniqKey="Robinson V">V.L. Robinson</name></author><author><name sortKey="Goudreau, P N" uniqKey="Goudreau P">P.N. Goudreau</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Heyl, A" uniqKey="Heyl A">A. Heyl</name></author><author><name sortKey="Wulfetange, K" uniqKey="Wulfetange K">K. Wulfetange</name></author><author><name sortKey="Pils, B" uniqKey="Pils B">B. Pils</name></author><author><name sortKey="Nielsen, N" uniqKey="Nielsen N">N. Nielsen</name></author><author><name sortKey="Romanov, G A" uniqKey="Romanov G">G.A. Romanov</name></author><author><name sortKey="Schmulling, T" uniqKey="Schmulling T">T. Schmülling</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Franco Zorrilla, J M" uniqKey="Franco Zorrilla J">J.M. Franco-Zorrilla</name></author><author><name sortKey="Martin, A C" uniqKey="Martin A">A.C. Martin</name></author><author><name sortKey="Solano, R" uniqKey="Solano R">R. Solano</name></author><author><name sortKey="Paz Ares, J" uniqKey="Paz Ares J">J. Paz-Ares</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Plet, J" uniqKey="Plet J">J. Plet</name></author><author><name sortKey="Wasson, A" uniqKey="Wasson A">A. Wasson</name></author><author><name sortKey="Ariel, F" uniqKey="Ariel F">F. Ariel</name></author><author><name sortKey="Le Signor, C" uniqKey="Le Signor C">C. Le Signor</name></author><author><name sortKey="Baker, D" uniqKey="Baker D">D. Baker</name></author><author><name sortKey="Mathesius, U" uniqKey="Mathesius U">U. Mathesius</name></author><author><name sortKey="Crespi, M" uniqKey="Crespi M">M. Crespi</name></author><author><name sortKey="Frugier, F" uniqKey="Frugier F">F. Frugier</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Pas, J" uniqKey="Pas J">J. Pas</name></author><author><name sortKey="Von Grotthuss, M" uniqKey="Von Grotthuss M">M. von Grotthuss</name></author><author><name sortKey="Wyrwicz, L S" uniqKey="Wyrwicz L">L.S. Wyrwicz</name></author><author><name sortKey="Rychlewski, L" uniqKey="Rychlewski L">L. Rychlewski</name></author><author><name sortKey="Barciszewski, J" uniqKey="Barciszewski J">J. Barciszewski</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Wulfetange, K" uniqKey="Wulfetange K">K. Wulfetange</name></author><author><name sortKey="Saenger, W" uniqKey="Saenger W">W. Saenger</name></author><author><name sortKey="Schmulling, T" uniqKey="Schmulling T">T. Schmülling</name></author><author><name sortKey="Heyl, A" uniqKey="Heyl A">A. Heyl</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hothorn, M" uniqKey="Hothorn M">M. Hothorn</name></author><author><name sortKey="Dabi, T" uniqKey="Dabi T">T. Dabi</name></author><author><name sortKey="Chory, J" uniqKey="Chory J">J. Chory</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Muller Dieckmann, H J" uniqKey="Muller Dieckmann H">H.J. Müller-Dieckmann</name></author><author><name sortKey="Grantz, A A" uniqKey="Grantz A">A.A. Grantz</name></author><author><name sortKey="Kim, S H" uniqKey="Kim S">S.H. Kim</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Pekarova, B" uniqKey="Pekarova B">B. Pekárová</name></author><author><name sortKey="Klumpler, T" uniqKey="Klumpler T">T. Klumpler</name></author><author><name sortKey="T Skova, O" uniqKey="T Skova O">O. Třísková</name></author><author><name sortKey="Janda, L" uniqKey="Janda L">L. Janda</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Zhang, Z" uniqKey="Zhang Z">Z. Zhang</name></author><author><name sortKey="Hendrickson, W A" uniqKey="Hendrickson W">W.A. Hendrickson</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Pils, B" uniqKey="Pils B">B. Pils</name></author><author><name sortKey="Heyl, A" uniqKey="Heyl A">A. Heyl</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Romanov, G A" uniqKey="Romanov G">G.A. Romanov</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Chow, B" uniqKey="Chow B">B. Chow</name></author><author><name sortKey="Mccourt, P" uniqKey="Mccourt P">P. McCourt</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Bishopp, A" uniqKey="Bishopp A">A. Bishopp</name></author><author><name sortKey="M Honen, A P" uniqKey="M Honen A">A.P. Mähönen</name></author><author><name sortKey="Helariutta, Y" uniqKey="Helariutta Y">Y. Helariutta</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Spartz, A K" uniqKey="Spartz A">A.K. Spartz</name></author><author><name sortKey="Gray, W M" uniqKey="Gray W">W.M. Gray</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Santner, A" uniqKey="Santner A">A. Santner</name></author><author><name sortKey="Calderon Villalobos, L I A" uniqKey="Calderon Villalobos L">L.I.A. Calderon-Villalobos</name></author><author><name sortKey="Estelle, M" uniqKey="Estelle M">M. Estelle</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Santner, A" uniqKey="Santner A">A. Santner</name></author><author><name sortKey="Estelle, M" uniqKey="Estelle M">M. Estelle</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Jaillais, Y" uniqKey="Jaillais Y">Y. Jaillais</name></author><author><name sortKey="Chory, J" uniqKey="Chory J">J. Chory</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Kumari, S" uniqKey="Kumari S">S. Kumari</name></author><author><name sortKey="Van Der Hoorn, R A L" uniqKey="Van Der Hoorn R">R.A.L. van der Hoorn</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Bleecker, A B" uniqKey="Bleecker A">A.B. Bleecker</name></author></analytic></biblStruct><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Danilenko, N G" uniqKey="Danilenko N">N.G. Danilenko</name></author><author><name sortKey="Davidenko, O G" uniqKey="Davidenko O">O.G. Davidenko</name></author></analytic></biblStruct></listBibl></div1></back></TEI><pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Acta Naturae</journal-id><journal-id journal-id-type="iso-abbrev">Acta Naturae</journal-id><journal-id journal-id-type="publisher-id">ActaNaturae</journal-id><journal-title-group><journal-title>Acta Naturae</journal-title></journal-title-group><issn pub-type="ppub">2075-8251</issn><publisher><publisher-name>A.I. Gordeyev</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">23150802</article-id><article-id pub-id-type="pmc">3491891</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject><subj-group><subject>Molecular Biology</subject></subj-group></subj-group></article-categories><title-group><article-title>Receptor Properties and Features of Cytokinin
Signaling</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Lomin</surname><given-names>S.N.</given-names></name><xref ref-type="aff" rid="AF1"></xref></contrib><contrib contrib-type="author"><name><surname>Krivosheev</surname><given-names>D.M.</given-names></name><xref ref-type="aff" rid="AF1"></xref></contrib><contrib contrib-type="author"><name><surname>Steklov</surname><given-names>M.Yu.</given-names></name><xref ref-type="aff" rid="AF1"></xref></contrib><contrib contrib-type="author"><name><surname>Osolodkin</surname><given-names>D.I.</given-names></name><xref ref-type="aff" rid="AF2"></xref></contrib><contrib contrib-type="author"><name><surname>Romanov</surname><given-names>G.A.</given-names></name><xref ref-type="aff" rid="AF1"></xref><xref ref-type="aff" rid="AF3"></xref><email>gar@ippras.ru</email></contrib></contrib-group><aff id="AF1">Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya Str., 35, Moscow, Russia,127276</aff><aff id="AF2">Department of Chemistry, Lomonosov Moscow State University, Leninskie Gory, 1/3, Moscow, Russia, 119991</aff><aff id="AF3">Belozersky Institute of Physicochemical Biology, Lomonosov Moscow State University, Leninskie Gory, 1/40, Moscow, Russia, 119992</aff><pub-date pub-type="ppub"><season>Jul-Sep</season><year>2012</year></pub-date><volume>4</volume><issue>3</issue><fpage>31</fpage><lpage>45</lpage><permissions><copyright-statement>Copyright © 2012 Park-media Ltd.</copyright-statement><copyright-year>2012</copyright-year><license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by/2.0/"><license-p>This is an open-access article distributed under the terms of the
Creative Commons Attribution License, which permits unrestricted use,
distribution, and reproduction in any medium, provided the original work is
properly cited.</license-p></license></permissions><abstract><p>Cytokinins belong to one of the most important and well-known classes of plant
hormones. Discovered over half a century ago, cytokinins have retained the
attention of researchers due to the variety of the effects they have on the
growth and development of vegetable organisms, their participation in a plant
adaptation to external conditions, and the potential to be used in
biotechnology, agriculture, medicine and even cosmetics. The molecular mechanism
by which cytokinins function remained unknown for a long time. Things started to
change only in the 21<sup>st</sup>century, after the discovery of the receptors
for these phytohormones. It appeared that plants found ways to adapt a
two-component signal transduction system borrowed from prokaryotic organisms for
cytokinin signalling. This review covers the recent advances in research of the
molecular basis for the perception and transduction of the cytokinin signal.
Emphasis is placed on cytokinin receptors, their domain and three-dimensional
structures, subcellular localization, signalling activity, effect of mutations,
ligand-binding properties, and phylogeny.</p></abstract><kwd-group kwd-group-type="author"><kwd>cytokinins</kwd><kwd>receptors</kwd><kwd>sensor histidine kinases</kwd><kwd>two-component systems</kwd><kwd>signal transduction</kwd></kwd-group></article-meta></front><body><sec><title>INTRODUCTION</title><p>Along with auxins, gibberellins, abscisic acid and ethylene, cytokinins belong to the
group of classical plant hormones. Cytokinins were discovered by F. Skoog and
co-workers in 1955 [<xref ref-type="bibr" rid="R1">1</xref>]. The hormone received
its name because of the ability to activate <italic>in vitro</italic> division
(cytokinesis) of plant cells. In terms of structure, natural cytokinins are adenine
derivatives with a small substituent at the N <sup>6 </sup> position ( <italic><xref ref-type="fig" rid="F1">Fig. 1</xref></italic> ). Most cytokinins (e.g.,
zeatin, isopentenyladenine) have the isopentenyl group at this position; however,
there can be an aromatic substituent (N <sup>6</sup> -benzyladenine, kinetin) as
well. Certain synthetic derivatives of phenylurea (e.g., thidiazuron) also exhibit
cytokinin activity. Cytokinins affect a number of physiological processes: they
stimulate cell division and expansion, plastid differentiation, they retard the
ageing process in leaves, activate metabolite inflow and shoot formation from
calluses in culture [2–<xref ref-type="bibr" rid="R5">5</xref>]. Cytokinins
are widely used in bioengineering and agricultural production to grow plant cell
cultures in bioreactors, to carry out micropropagation (cloning) of cultivated
plants, to obtain transgenic plants, to control plant sex, for cotton defoliation,
etc. [<xref ref-type="bibr" rid="R4">4</xref>, <xref ref-type="bibr" rid="R5">5</xref>]. Cytokinins participate in the inorganic nutrition of plants and in
the formation of nitrogen-fixing root nodules, affect the cereal grain size (i.e.,
the crop capacity) and the plant resistance to adverse factors [6–<xref ref-type="bibr" rid="R8">8</xref>]. Cytokinins and related compounds have
recently been finding increasing application in medicine and cosmetology; they are
used as anti-tumor agents and inhibitors of neurodegenerative processes and as an
active agent in liniments that prevent age-related changes in the skin [<xref ref-type="bibr" rid="R4">4</xref>, <xref ref-type="bibr" rid="R9">9</xref>,
<xref ref-type="bibr" rid="R10">10</xref>].</p><p>During the past 15 years there has been substantial progress in elucidating the
molecular mechanism of cytokinin action; sequencing of the genome of the model plant
<italic>Arabidopsis thaliana</italic> played a significant role [<xref ref-type="bibr" rid="R11">11</xref>]. Discovery of receptors, the key components
of hormone signal reception and transduction, was of particular significance. Four
papers devoted to the identification and characterization of cytokinin receptors in
<italic>Arabidopsis thaliana </italic> were published in 2001 [12–<xref ref-type="bibr" rid="R15">15</xref>]. A receptor named CRE1 (Cytokinin Response
1), or AHK4 (Arabidopsis Histidine Kinase 4), has been characterized. A mutation
that manifested itself in a shortening of the Arabidopsis root in the absence of
phloem ( <italic>wooden</italic><italic>leg</italic> , or <italic>wol</italic> ) was identified before that. This
mutation affects the same gene referred to as <italic>WOL</italic> [<xref ref-type="bibr" rid="R16">16</xref>]. In addition to the <italic>CRE1/AHK4/WOL
</italic> gene, two of its paralogues which became known as <italic>AHK2 </italic>and <italic>AHK3</italic> have also been identified in the Arabidopsis genome
sequence [<xref ref-type="bibr" rid="R13">13</xref>, <xref ref-type="bibr" rid="R14">14</xref>, <xref ref-type="bibr" rid="R16">16</xref>, <xref ref-type="bibr" rid="R17">17</xref>]. Thus, three cytokinin receptors have been identified in
Arabidopsis; these receptors are transmembrane proteins with a similar structure and
a molecular weight of over 100 kDa.</p><fig id="F1" orientation="portrait" position="float"><label>Fig. 1</label><caption><p> Structures of typical cytokinins. The most favoured conformations of
cytokinins are shown in the upper line; their chemical structures are shown
in the lower line.</p></caption><graphic xlink:href="AN20758251-04-031-g001"></graphic></fig><fig id="F2" orientation="portrait" position="float"><label>Fig. 2</label><caption><p>Domain structure of cytokinin receptor (exemplified by CRE1/AHK4 from
Arabidopsis). Protein domains: TM – transmembrane; LB –
ligand-binding (CHASE); HK – histidine kinase; Ac – acceptor; Ck
– cytokinins; H – conserved histidine; D – conserved
aspartate; N and C denote the N- and C-termini of the protein. The
rightwards arrows indicate the sites for phosphorylation and the transfer of
high-energy phosphates (~P).</p></caption><graphic xlink:href="AN20758251-04-031-g002"></graphic></fig><p>This review is focused upon the major questions pertaining to cytokinin recognition
and signalling, such as the domain structure of receptors, the biochemical basis of
signal perception and transduction, subcellular localization, ligand-binding
characteristics and the effect of mutations on receptor properties, the
three-dimensional structure of receptors, and the emergence and evolution of
receptors in plants.</p></sec><sec><title>THE DOMAIN STRUCTIURE OF CYTOKININ RECEPTORS</title><p>Cytokinin receptors belong to the group of catalytic receptors. They have a complex
multidomain structure ( <italic><xref ref-type="fig" rid="F2">Fig. 2</xref></italic>). The so-called CHASE domain (Cyclase/Histidine kinase Associated Sensory
Extracellular) located at the N-terminus of a receptor molecule possesses hormone
binding activity [<xref ref-type="bibr" rid="R18">18</xref>, <xref ref-type="bibr" rid="R19">19</xref>]. There are two or more transmembrane domains at the two
sides of this sensor domain. The last transmembrane domain is followed by a
catalytic domain with histidine kinase activity. The core component of this region
consists of a dimerization domain and the ATP/ADP binding phosphotransfer domain.
The dimerization domain (A-domain) consists of two antiparallel helices that are
adjacent to each other (two-stranded coiled-coils). The A-domains of two receptors
can interact thus forming a four-helix bundle. According to current concepts, each
histidine kinase subunit in the dimer is phosphorylated by the other one (
<italic>in trans </italic> reaction) [<xref ref-type="bibr" rid="R20">20</xref>]. The phosphotransfer domain contains a conserved site (H-box) of the
general structure – <bold>A</bold> TV <bold>SH</bold> E <bold>IR</bold> TP
– with the histidine residue being phosphorylated in its centre.</p><p>Four conserved motifs (N-, G1-, F-, and G2-boxes) participate in ATP binding. They
probably participate in the catalysis and transfer of the phosphate moiety as well.
The C-terminus of the receptor contains the receiver domain with the conserved
acceptor aspartate residue in the sequence denoted as DD- <bold>D-</bold> K.
Cytokinin receptors contain a pseudo-receiver domain which is structurally similar
to the receiver domain but cannot receive a phosphate from the conserved histidine
residue. The pseudo-receiver domain resides between the regions of histidine kinase
and the receiver domains [<xref ref-type="bibr" rid="R21">21</xref>, <xref ref-type="bibr" rid="R22">22</xref>]. The function of the pseudo-receiver domain
has not been elucidated.</p><p>Thus, cytokinin receptors belong to the group of membrane sensor histidine kinases in
terms of their general structure and are homologous to some other sensor proteins
from plants (ethylene receptors and phytochromes) [<xref ref-type="bibr" rid="R22">22</xref>, <xref ref-type="bibr" rid="R23">23</xref>].</p></sec><sec><title>MOLECULAR BASIS OF CYTOKININ SIGNAL TRANSDUCTION</title><p>Cytokinin receptors are structural and functional relatives of sensor histidine
kinases belonging to two-component signal transduction systems that are common among
prokaryotes, and have also been found in a number of eukaryotes except for animals
[<xref ref-type="bibr" rid="R20">20</xref>, <xref ref-type="bibr" rid="R24">24</xref>]. A classical prokaryote two-component system consists of two
proteins, namely, a sensor histidine kinase and a response regulator (usually a
transcription factor). Under the influence of external factors the histidine kinase
is activated and autophosphorylated. The high-energy phosphate then passes to the
response regulator. In two-component systems, phosphate is transferred from the
conserved histidine residue of one protein molecule (histidine kinase) to the
conserved aspartate residue of another molecule (the receiver domain of the response
regulator). This process is referred to as phosphorelay. The phosphorylation of the
response regulator results in its activation, which in turn triggers transcription
of a particular gene or gene set [<xref ref-type="bibr" rid="R25">25</xref>].</p><fig id="F3" orientation="portrait" position="float"><label>Fig. 3</label><caption><p> Scheme of cytokinin signal transduction based on the principle of multistep
His-Asp-His-Asp phosphorelay. The phosphorylation of nuclear transcription
factors (ARR-B-type response regulators) leads to their activation and
subsequent alteration of the primary response gene transcription.</p></caption><graphic xlink:href="AN20758251-04-031-g003"></graphic></fig><p>The scheme of signal transduction is more complex in the case of cytokinin
perception, since the receiver domain is part of the sensor histidine kinase (a type
of chimeric protein). The signal is transduced according to the principle of
multistep (His-Asp-His-Asp) phosphorelay ( <italic><xref ref-type="fig" rid="F3">Fig. 3</xref></italic> ). Hormone binding to the CHASE sensor domain yields
phosphorylation of the conserved histidine residue in the resulting histidine kinase
dimer. This phosphate moiety is subsequently intramolecularly transferred to the
conserved aspartate residue of the receiver domain of histidine kinase and then
transferred to the conserved histidine residue of the mobile low-molecular-weight
protein-phosphotransmitter (HP), which permanently migrates between the cytoplasm
and the cell nucleus [<xref ref-type="bibr" rid="R26">26</xref>]. When a
phosphorylated phosphotransmitter enters the nucleus, it passes its high-energy
phosphate to the conserved aspartate residue in the receiver domain of the response
regulator. This protein (which is typically a transcription factor) is activated by
phosphorylation and acquires the ability to regulate (typically, activate) the
transcription of the primary response genes [27–<xref ref-type="bibr" rid="R29">29</xref>]. The cytokinin regulation of the biosynthesis of mRNA of
the primary response genes is dependent only on a nontranscribed promoter; i.e., it
occurs at the stage of transcription initiation [<xref ref-type="bibr" rid="R4">4</xref>].</p></sec><sec><title>The features of cytokinin signaling in arabidopsis</title><p>The first cytokinin receptors were identified in Arabidopsis; their ability to
recognize the hormonal signal has been confirmed in experiments with transformed
bacteria and yeast. Expression of cytokinin receptors from plants in these
unicellular organisms resulted in the emergence of a response to low (hormonal)
cytokinin concentrations [12–<xref ref-type="bibr" rid="R14">14</xref>, <xref ref-type="bibr" rid="R30">30</xref>, <xref ref-type="bibr" rid="R31">31</xref>].
The <italic>in vivo </italic> role of these proteins as receptors has been verified
by studying the insertional mutants of Arabidopsis. In general, the mutation in a
single receptor does not result in any noticeable changes of plant phenotype.
However, mutation in two and, in particular, all three receptors has serious
effects. When all three receptors were inactivated, the triple mutant was
insensitive to cytokinins and represented a sterile dwarf plant with reduced
viability [32–<xref ref-type="bibr" rid="R34">34</xref>].</p><p>The receptors functionally complement each other, although they are not redundant in
a number of processes. The CRE1/АНК4 receptor is mainly expressed
in roots, whereas АНК3 prevails in leaves. In accordance, the
effects of cytokinin on the aerial and underground parts of a plant depend to a
larger extent on the AHK3 and CRE1/АНК4 receptors, respectively
[<xref ref-type="bibr" rid="R4">4</xref>]. Five typical phosphotransmitters
(AHP) and 22 response regulators have been identified among the elements of the
two-component system in Arabidopsis. Phosphotransmitters are small proteins up to 17
kDa [<xref ref-type="bibr" rid="R35">35</xref>]. Similarly to receptors, AHP
proteins are redundant and participate in the transduction of the cytokinin signal
additively; the mutant with respect to all five genes exhibited abruptly reduced
sensitivity to cytokinins and phenotypically resembled the receptor triple mutant
[36–<xref ref-type="bibr" rid="R39">39</xref>]. AHP 1, 2, 3 and 5 play the
key role in cytokinin signal transduction. According to current concepts, AHP
proteins permanently migrate between the nucleus and the cytoplasm; the pattern of
their localization is independent of phosphorylation [<xref ref-type="bibr" rid="R26">26</xref>, <xref ref-type="bibr" rid="R35">35</xref>, <xref ref-type="bibr" rid="R40">40</xref>].</p><p>AHP6 is another Arabidopsis protein that structurally resembles the
phosphotransmitter. However, this protein belongs to pseudo-AHPs since it does not
contain the conserved histidine residue required for the phosphorelay. The AHP6
binds to both receptors or response regulators inhibiting their interaction with
typical phosphotransmitters and thus acting as a negative regulator of cytokinin
signal transduction [<xref ref-type="bibr" rid="R41">41</xref>].</p><p>Arabidopsis response regulators can be classified into three groups (A, B, and C);
there is also a group of pseudo-regulator proteins [<xref ref-type="bibr" rid="R42">42</xref>]. The B-type response regulators which contain both the
phosphorylated N-terminal receiver domain and a special B-motif including the
DNA-binding GARP-domain and the glutamine-rich domain are the real transcription
factors [43–<xref ref-type="bibr" rid="R46">46</xref>]. Due to the nuclear
location signals (NLS) B-type response regulators are localized in the nucleus. The
total number of <italic>ARR-B</italic> genes is 11; however, B-type response
regulators are not identical in terms of cytokinin signal transduction. The
<italic>ARR1, 10</italic> and <italic>12 </italic> genes play the key role: the
triple mutant with knocked out genes is phenotypically similar to the cytokinin
receptor triple mutant [47–<xref ref-type="bibr" rid="R49">49</xref>]. The
expression of the genes of B-type response regulators is not regulated by cytokinins
[<xref ref-type="bibr" rid="R28">28</xref>, <xref ref-type="bibr" rid="R29">29</xref>, <xref ref-type="bibr" rid="R50">50</xref>, <xref ref-type="bibr" rid="R51">51</xref>]. It should be mentioned that direct evidence of the
interaction between the proteins that are components of the signal transduction
circuit and their ability to donate and accept phosphate according to the scheme
shown in <italic><xref ref-type="fig" rid="F3">Fig. 3</xref></italic> have been
obtained [<xref ref-type="bibr" rid="R13">13</xref>, <xref ref-type="bibr" rid="R36">36</xref>, <xref ref-type="bibr" rid="R38">38</xref>].</p><p>As opposed to ARR-B, the genes of A-type response regulators (ARR-A) can be promptly
activated by cytokinins and belong to the primary response genes for these hormones
[27–<xref ref-type="bibr" rid="R29">29</xref>, <xref ref-type="bibr" rid="R52">52</xref>]. ARR-A consist of the typical receiver domain and a small
C-terminal fragment. The A-type response regulators may accept phosphate from
phosphotransmitters similar to the B-type regulators; however, they cannot induce
the typical transcription response.</p><p>A body of observations allows to conclude that ARR-A act as negative regulators of
signal transduction, the conserved aspartate residue being required to implement
their inhibitory effect [53–<xref ref-type="bibr" rid="R55">55</xref>]. The
multiple mutant with respect to the genes of A-type response regulators is
characterized by increased sensitivity to cytokinin. It is assumed that the A-type
response regulators are capable of suppressing cytokinin signal transduction from
the AHP proteins by competing with the B-type regulators for the high-energy
phosphate. Thus, the participation of ARR-A in the system of cytokinin signal
transduction provides negative feedback. Although the structure of C-type response
regulators is similar to that of ARR-A, they are not induced by cytokinins and seem
not to play a significant role in cytokinin signal transduction [<xref ref-type="bibr" rid="R42">42</xref>, <xref ref-type="bibr" rid="R56">56</xref>].
In the absence of cytokinin the CRE1/AHK4 receptor acts as phosphatase and removes a
phosphate group from the AHP proteins, thus deactivating signal transduction from
the other cytokinin, receptors too [<xref ref-type="bibr" rid="R57">57</xref>]. In
general, a large number of studies carried out using Arabidopsis plants have
persuasively demonstrated that the cytokinin signal is transduced via the
two-component pathway, with hybrid histidine kinases acting as receptors.</p></sec><sec><title>SUBCELLULAR LOCALIZATION OF RECEPTORS</title><p>The cytokinin receptor is an integral transmembrane protein with the CHASE domain
located to one side of the membrane and the histidine kinase and receiver domains
located to the other side. Cytokinin receptors were believed to be localized on the
plasma membrane; it was assumed evident that the CHASE domain has to be localized
extracellularly, whereas the remaining part of the protein has to be intracellular.
This assumption was partly based on the computational prediction of subcellular
localization [<xref ref-type="bibr" rid="R12">12</xref>, <xref ref-type="bibr" rid="R14">14</xref>, <xref ref-type="bibr" rid="R16">16</xref>] and on the
analogy with a bacterial cell, where the CHASE domain of sensor proteins is
extracellular (this fact is evident from the domain name). This belief was further
bolstered when the localization of the cytokinin receptor in the plasmalemma
revealed by expression of the <italic> АНК3-GFP </italic>construct in Arabidopsis protoplasts was reported [<xref ref-type="bibr" rid="R58">58</xref>]. The localization of cytokinin receptors on the plasma membrane
assumes that the cytokinin signal enters the cell from the environment due to
extracellular cytokinins. On the other hand, it was demonstrated by determining the
pH-dependence of cytokinin binding to receptors that the binding is optimal in
neutral and alkalescent media, which are typical of the cytoplasm, and that it
decreases abruptly under acidified conditions, which are typical of the
extracellular space (the apoplast) [<xref ref-type="bibr" rid="R59">59</xref>]. This
fact attests on the contrary to the intracellular localization of the receptor.
Therefore, studies of the subcellular localization of cytokinin receptors were
continued.</p><p>Three articles claiming that the receptors (or at least their majority) are localized
inside the cell on the membranes of the endoplasmic reticulum (ER) have recently
been published [60–<xref ref-type="bibr" rid="R62">62</xref>]. Sites of
<sup>3</sup> Н- <italic>trans</italic> -zeatin high-affinity binding in
the fraction containing membranes (microsomes) but not in fractions containing
mitochondria or chloroplasts have been revealed in experiments with subcellular
organelles [<xref ref-type="bibr" rid="R60">60</xref>]. After the microsomes had
been separated in an aqueous two-phase polymer system into the plasmalemma and
endomembranes, it turned out that the high-affinity sites were mostly confined to
the endomembrane fraction both in Arabidopsis [<xref ref-type="bibr" rid="R61">61</xref>] and corn [<xref ref-type="bibr" rid="R60">60</xref>]. Taking into
account the predominance of endomembranes in the cell, it was assessed that over 90%
of the hormone binding sites are localized intracellularly.</p><p>By studying the localization of the Arabidopsis receptor-fluorescent protein fusions
expressed in tobacco leaves [<xref ref-type="bibr" rid="R61">61</xref>, <xref ref-type="bibr" rid="R62">62</xref>] and the corn receptor ZmHK1 in protoplasts
from corn leaves [<xref ref-type="bibr" rid="R60">60</xref>] it has been
demonstrated that fluorescence distribution corresponds to the endoplasmic reticulum
network. For the AHK3 receptor, the fluorescence pattern coincided with the pattern
for the ER marker but not the plasmalemma marker [<xref ref-type="bibr" rid="R61">61</xref>, <xref ref-type="bibr" rid="R62">62</xref>]. In addition, the AHK3
protein was <italic>in vivo </italic> glycosylated at the sites that are sensitive
to glycosidase endoH, which attests to localization in ER [<xref ref-type="bibr" rid="R62">62</xref>]. The same glycosylation was recorded in control experiments
for the ethylene receptor ERS1 integrated into ER [<xref ref-type="bibr" rid="R63">63</xref>, <xref ref-type="bibr" rid="R64">64</xref>], whereas the potential
endoH-sites in histidine kinase AHK1 localized in the plasmalemma were not
glycosylated [<xref ref-type="bibr" rid="R62">62</xref>].</p><p>It should be mentioned that the intracellular localization of cytokinin receptors,
which was revealed via fluorescence, was observed under various conditions of
expression of the inserted genes using promoters of different strengths. However,
the most convincing result was obtained by analysis of the localization of the
receptors expressed under natural conditions. This approach was implemented via
immunoblotting with antibodies against the corn receptor ZmHK1. The membrane
fractions obtained upon separation in a sucrose gradient in the absence or presence
of magnesium cations were analyzed [<xref ref-type="bibr" rid="R60">60</xref>]. In
the absence of magnesium, ribosomes dissociate from the ER, resulting in the shift
of the ER towards the top of the gradient. This shift is not observed if magnesium
is present in the medium. This effect referred to as the Mg-shift is typical of ER
but not the other membranes unbound to the ribosomes. It was demonstrated by the
analysis of fractions from corn cells that the ZmHK1 protein undergoes a Mg-shift
and is co-localized with the ER marker protein (BiP) [<xref ref-type="bibr" rid="R60">60</xref>].</p><p>The stable Arabidopsis transformants expressing AHK2 or AHK3 receptor genes under
their own promoters and with the Myc peptide at the C-terminus of the protein were
obtained . The expression of these constructs compensated for the phenotype of the
<italic>ahk2 ahk3</italic> double mutant of Arabidopsis, attesting to the
functionality of these modified receptors. The typical Mg-shift and correlation with
the ER marker were also revealed when analyzing the membrane fractions via
immunoblotting with anti-Myc antibodies [<xref ref-type="bibr" rid="R61">61</xref>].</p><p>All these data allow one to conclude that cytokinin receptors are mostly localized in
the endoplasmic reticulum. Along with the data pertaining to the ability of
ER-localized receptors to bind cytokinins and the pH-dependence of this binding
typical of cytoplasmic proteins, this result may attest to the fact that cytokinin
signal perception occurs mainly inside the cell and that intracellular cytokinins
play the key role in this process. However, the presence of a small number of
receptors on the plasma membrane should not be left without consideration. These
receptors can be responsible for the perception of the signal from extracellular
cytokinins. Further research is needed to assess the functional properties of each
pool of cytokinin receptors.</p></sec><sec><title>ligand-binding properties of receptors</title><p>Along with gibberellines, cytokinins are represented by a variety of isoforms in
plants ( <italic><xref ref-type="fig" rid="F1">Fig. 1</xref></italic> ); among those
<italic>trans</italic> - and <italic>cis</italic> -zeatins, isopentenyladenine,
dihydrozeatin (bases), their N <sup>9</sup> -ribosylated derivatives (ribosides) and
N <sup>9</sup> -riboside phosphate derivatives (nucleotides) are prevalent. Aromatic
cytokinins such as N <sup>6</sup> -benzyladenine and its derivatives, topolin, etc.
occur as well [<xref ref-type="bibr" rid="R4">4</xref>, <xref ref-type="bibr" rid="R5">5</xref>, <xref ref-type="bibr" rid="R65">65</xref>]. Cytokinins
migrate within a plant along transport channels: in the upward direction from the
root into the shoot via xylem and in the downward and other directions via the
phloem. Cytokinin compositions in the xylem differ from those in the phloem:
<italic>trans</italic> -zeatin-type cytokinins (mostly, <italic>trans</italic>-zeatin-riboside) are the prevailing isoforms in the xylem, whereas isopentenyl-type
cytokinins are prevalent in the phloem [66–<xref ref-type="bibr" rid="R68">68</xref>].</p><p>The physiological role of each cytokinin isoform is determined by its affinity to the
receptor; therefore, the investigation of cytokinin–receptor interaction and
ligand specificity of the receptors is of high importance. The ligand-binding
properties of cytokinin receptors have been studied mostly using heterologous model
systems upon expression of the receptor genes in transformed bacterial (
<italic>Escherichia coli</italic> ) or yeast cells. Plant receptors turned out
to be capable of functional replacement of mutant sensor histidine kinases with a
similar (hybrid) structure in these unicellular organisms [<xref ref-type="bibr" rid="R12">12</xref>, <xref ref-type="bibr" rid="R13">13</xref>, <xref ref-type="bibr" rid="R30">30</xref>].</p><p>Both functional tests [<xref ref-type="bibr" rid="R13">13</xref>, <xref ref-type="bibr" rid="R15">15</xref>, <xref ref-type="bibr" rid="R30">30</xref>,
<xref ref-type="bibr" rid="R69">69</xref>, <xref ref-type="bibr" rid="R70">70</xref>] and hormone-receptor binding assays [<xref ref-type="bibr" rid="R59">59</xref>, <xref ref-type="bibr" rid="R60">60</xref>, <xref ref-type="bibr" rid="R71">71</xref>, <xref ref-type="bibr" rid="R72">72</xref>] have been
carried out based on the aforementioned model systems. In general, as was expected,
the affinity of the hormone to the receptor positively correlated with the
hormone’s ability to induce a biological response [<xref ref-type="bibr" rid="R59">59</xref>, <xref ref-type="bibr" rid="R71">71</xref>].
<italic>trans</italic> -Zeatin is one of the most active ligands for most of the
receptors studied; <italic>К</italic><sub>d </sub> of the hormone-receptor complex varies within a range of 1–10
nM. Such values of the constants are typical of high-affinity hormone-receptor
interactions. Let us note that these values of the constants are close to the
measured concentrations of <italic>trans</italic> -zeatin in living plants [<xref ref-type="bibr" rid="R34">34</xref>, <xref ref-type="bibr" rid="R66">66</xref>,
<xref ref-type="bibr" rid="R68">68</xref>, <xref ref-type="bibr" rid="R73">73</xref>]. A Scatchard analysis has revealed the single receptor-ligand
binding site without any signs of cooperative interaction [<xref ref-type="bibr" rid="R59">59</xref>, <xref ref-type="bibr" rid="R74">74</xref>]. Meanwhile,
natural (N <sup>6</sup> -adenine derivatives) and synthetic (thidiazuron, a
phenylurea derivative) cytokinins bound to the same receptor site [<xref ref-type="bibr" rid="R59">59</xref>].</p><table-wrap id="T1" orientation="portrait" position="float"><label>Table 1</label><caption><p>Rows of cytokinin affinity for the receptors from Arabidopsis and corn</p></caption><table frame="hsides" rules="groups"><thead><tr><th rowspan="1" colspan="1">Species</th><th rowspan="1" colspan="1">Receptor**</th><th rowspan="1" colspan="1">Cytokinin affinity rows**</th></tr></thead><tbody><tr><td rowspan="1" colspan="1"><italic>Zea mays </italic></td><td rowspan="1" colspan="1">ZmHK1</td><td rowspan="1" colspan="1">iP ≥ BA >> tZ ≥ cZ >> DZ >> Ade</td></tr><tr><td rowspan="1" colspan="1"><italic>Arabidopsis thaliana </italic></td><td rowspan="1" colspan="1">CRE1/AHK4</td><td rowspan="1" colspan="1">iP ≥ tZ > BA > DZ > cZ >> Ade</td></tr><tr><td rowspan="1" colspan="1"><italic>Zea mays </italic></td><td rowspan="1" colspan="1">ZmHK2</td><td rowspan="1" colspan="1">tZ ≥ iP > DZ > BA > cZ >> Ade</td></tr><tr><td rowspan="1" colspan="1"><italic>Arabidopsis thaliana </italic></td><td rowspan="1" colspan="1">AHK3</td><td rowspan="1" colspan="1">tZ > DZ > iP > cZ > BA >> Ade</td></tr><tr><td rowspan="1" colspan="1"><italic>Zea mays </italic></td><td rowspan="1" colspan="1">ZmHK3a</td><td rowspan="1" colspan="1">iP > tZ > BA > cZ >> DZ >> Ade</td></tr><tr><td rowspan="1" colspan="1"><italic>Arabidopsis thaliana </italic></td><td rowspan="1" colspan="1">AHK2</td><td rowspan="1" colspan="1">iP > tZ > BA > cZ > DZ >> Ade</td></tr></tbody></table><table-wrap-foot><fn id="TF1-0"><p>* Orthologous receptors are grouped pairwise.</p></fn><fn id="TF1-1"><p>** Cytokinins: iP – isopentenyladenine; BA – N <sup>6</sup>-benzyladenine; tZ – <italic>trans</italic> -zeatin; cZ –
<italic>cis</italic> -zeatin; DZ – dihydrozeatin. Ade –
adenine.</p></fn></table-wrap-foot></table-wrap><p>Yet, the receptors differ in their preference of cytokinin isoforms [<xref ref-type="bibr" rid="R59">59</xref>, <xref ref-type="bibr" rid="R60">60</xref>,
<xref ref-type="bibr" rid="R75">75</xref>]. The Arabidopsis receptors CRE1/AHK4
and АНК2 have the same high affinity to <italic>trans</italic>-zeatin and isopentenyladenine and a considerably lower affinity to dihydrozeatin.
On the contrary, the AHK3 receptor is characterized by a relatively high affinity to
dihydrozeatin and a lower affinity to isopentenyladenine. All three Arabidopsis
receptors are capable of binding, though with low affinity, <italic>cis</italic>-zeatin, too. Cytokinin glucosylation at the N3 or N7 nitrogen atoms and at the
oxygen atom of the side chain blocks the hormone-receptor binding [<xref ref-type="bibr" rid="R30">30</xref>, <xref ref-type="bibr" rid="R59">59</xref>].</p><p>The ligand specificity of cytokinin receptors has also been studied for corn, a
monocotyledonous plant, three receptors of which are orthologous to those of the
dicotyledonous plant Arabidopsis: ZmHK1 orthologous to CRE1/AHK4; ZmHK2 orthologous
to АНК3; and ZmHK3 orthologous to АНК2 [<xref ref-type="bibr" rid="R76">76</xref>]. The corn receptors were partly similar to,
partly different from, their Arabidopsis counterparts [<xref ref-type="bibr" rid="R60">60</xref>, <xref ref-type="bibr" rid="R76">76</xref>]. In general, the
order of relative ligand activity turned out to be rather similar for corn and
Arabidopsis orthologues ( <italic><xref ref-type="table" rid="T1">Table
1</xref></italic> ). Whereas isopentenyladenine exhibited higher activity than
<italic>trans</italic> -zeatin with respect to ZmHK1 and ZmHK3, the opposite was
observed for ZmHK2. A stronger difference between corn receptors was observed upon
their interaction with dihydrozeatin: the affinity of ZmHK2 to this cytokinin is
more than two orders of magnitude higher compared to its affinity to ZmHK1 and
ZmHK3. A relatively high affinity to <italic>cis</italic> -zeatin is a
characteristic feature of corn receptors, ZmHK1 demonstrating almost identical
affinities to <italic>trans</italic> - and <italic>cis</italic> -zeatins. This
feature of corn receptors is in accordance with an increased concentration of
<italic>cis</italic> -zeatin in this plant species [<xref ref-type="bibr" rid="R77">77</xref>, <xref ref-type="bibr" rid="R78">78</xref>].</p><p>The regularities of the receptor preferences to certain ligands can be interpreted
with allowance for their possible role in long-range signalling in plants. The
Arabidopsis receptors AHK3 and their orthologues ZmHK2 in corn are mainly expressed
in shoots and control the metabolic processes occurring in leaves. These receptors
are “tuned” primarily to <italic>trans</italic> -zeatin-type cytokinins;
i.e., to the cytokinins transported to the shoot from the roots. In turn, the
CRE1/AHK4 and ZmHK1 receptors that are prevalent in roots actively respond to
isopentenyladenine, the major cytokinin in phloem, which is translocated from the
shoot to the roots with the phloem sap ( <italic><xref ref-type="fig" rid="F4">Fig.
4</xref></italic> ). Thus, signal exchange can occur between different parts
and organs of a plant organism, when the cytokinin signals of a remote organ turn
out to be more significant for the cell compared to the signals from the closer
located tissues [<xref ref-type="bibr" rid="R4">4</xref>, <xref ref-type="bibr" rid="R59">59</xref>, <xref ref-type="bibr" rid="R79">79</xref>].</p></sec><sec><title>effect of mutations on receptor activity</title><p>The identification of the Arabidopsis mutation named <italic>wooden leg </italic> (
<italic>wol</italic> ) resulted in the discovery of cytokinin receptors. The
mutant plants were different from the wild-type plants by a shorter length and a
disturbed development of the vascular system of the main root. The latter consisted
of protoxylem only (metaxylem and phloem have not been developed); the total number
of cells was significantly lower. Moreover, the plants had no lateral roots and
exhibited enhanced formation of adventitious roots. The phenotypic manifestation of
this mutation was first described in 1995 [<xref ref-type="bibr" rid="R80">80</xref>].</p><fig id="F4" orientation="portrait" position="float"><label>Fig. 4</label><caption><p> A model for long-distance cytokinin action. The arrow in the middle denotes
the translocation of cytokinins (Ck) of <italic>trans</italic> -zeatin type
from the root to the shoot via xylem. The lateral arrows denote the
translocation of cytokinins of the isopentenyladenine type from the shoot to
the root via phloem.</p></caption><graphic xlink:href="AN20758251-04-031-g004"></graphic></fig><p>The <italic>wol</italic> mutation was subsequently found to be localized in the gene
of sensor histidine kinase CRE1/AHK4 and to consist in the substitution of threonine
278 (threonine 301 according to the modern numeration) with isoleucine in the
hormone-binding CHASE domain [<xref ref-type="bibr" rid="R12">12</xref>, <xref ref-type="bibr" rid="R15">15</xref>, <xref ref-type="bibr" rid="R16">16</xref>].
The <italic>wol</italic> -2 and <italic>cre1-1</italic> mutations were later
obtained via chemical mutagenesis. These mutations consisted in replacing leucine
529 with isoleucine [<xref ref-type="bibr" rid="R82">82</xref>] and glycine 490 with
aspartate [<xref ref-type="bibr" rid="R12">12</xref>], respectively. All these
mutations also resulted in the typical <italic>wol</italic> phenotype caused by
underdevelopment of the vascular system due to a reduced number of meristem initial
cells because of blockage of cell division [<xref ref-type="bibr" rid="R16">16</xref>]. The defects in the vascular system impeded auxin transport to the
pericycle; as a result, lateral roots were not formed. Meanwhile, the disturbance in
the vascular system of the main root resulted in auxin accumulation in the hypocotyl
bottom region, which in turn stimulated the formation of adventitious roots. It is
of interest to note that normal development of the vascular system in adventitious
roots, as opposed to the main root, was observed in the <italic>wol-3 </italic>mutants [<xref ref-type="bibr" rid="R82">82</xref>].</p><p>The radioligand-binding technique demonstrated that the receptor loses its
cytokinin-binding capacity upon <italic>wol </italic> mutation [<xref ref-type="bibr" rid="R15">15</xref>]. However a stop codon introduced to the
mutant <italic>CRE1/AHK4 </italic> gene recovered the wild-type phenotype in
<italic>wol </italic> plants [<xref ref-type="bibr" rid="R57">57</xref>].
Therefore, it was reasonable to assume that the mutant receptor CRE1/AHK4 not only
stops participating in cytokinin signal transduction but also suppresses the
transduction of this signal from the other receptors, AHK2 and AHK3. Some bacterial
histidine kinases have been ascertained to possess phosphatase (in addition to
kinase) activity, resulting in dephosphorylation of phosphoproteins [<xref ref-type="bibr" rid="R83">83</xref>]. It has been demonstrated in <italic>in
vitro </italic> experiments and in experiments on transgenic yeasts that
CRE1/AHK4 also has a constitutive phosphatase activity, whereas its histidine kinase
activity is manifested only in the presence of cytokinins [<xref ref-type="bibr" rid="R57">57</xref>]. Thus, the <italic>wol </italic> mutation which makes
CRE1/AHK4 incapable of cytokinin binding blocks its histidine kinase activity,
whereas phosphatase activity is retained. Consequently CRE1/AHK4 harboring the
<italic>wol </italic> mutation dephosphorylates the phosphotransmitter proteins
phosphorylated with the AHK3 and AHK2 receptors, thus blocking the cytokinin signal
transduction. CRE1/AHK4 predominates in root cells [<xref ref-type="bibr" rid="R17">17</xref>, <xref ref-type="bibr" rid="R32">32</xref>]; therefore, the
<italic>wol</italic> mutant phenotype is mainly manifested in roots.</p><p>The same mutations in the CHASE domain of AHK3 and AHK2 receptors have not resulted
in the emergence of the <italic>wol</italic> -like phenotype [<xref ref-type="bibr" rid="R31">31</xref>]. This attests to the fact that the AHK2 and AHK3 receptors
do not have phosphatase activity.</p><p>Thus, a number of mutations in the CRE1/AHK4 receptors resulting in the emergence of
the typical <italic>wol</italic> -phenotype have been revealed. It has been
demonstrated that the receptor, upon all these mutations, no longer transduces
cytokinin signals despite the fact that only the <italic>wol</italic> (
<italic>wol-1</italic> ) mutation is localized in the CHASE domain. The
<italic>wol-3</italic> mutation is localized in the region between the second
transmembrane and histidine kinase domains; the <italic>wol-2</italic> and
<italic>cre1-1</italic> mutations are localized in the histidine kinase
domain.</p><p>In general, the analysis of mutations in cytokinin receptors has enabled to confirm
and refine our understanding of the roles of the defined parts of receptors. The
isolated CHASE domain with the adjacent transmembrane domains retains the ability to
high-affinity cytokinin binding, whereas the receptor without the CHASE domain lacks
such ability [<xref ref-type="bibr" rid="R84">84</xref>]. Hormone-receptor binding
was also suppressed by the other mutations in this domain [<xref ref-type="bibr" rid="R84">84</xref>]. Thus, the role of the CHASE domain as a hormone-binding
one is beyond question.</p><p>Although the mutations in the CHASE domain disturbed receptor functioning in the
absolute majority of cases, a mutation (called <italic>ore12-1</italic> ) in this
domain resulting in constitutive activity of histidine kinase was found in the AHK3
receptor [<xref ref-type="bibr" rid="R58">58</xref>]. Upon this mutation proline 243
located in the middle of the CHASE domain was replaced by serine. It was assumed
that this substitution of amino acids could result in an alteration of the CHASE
domain structure similar to that caused by cytokinin binding [<xref ref-type="bibr" rid="R58">58</xref>].</p><p>Conserved histidine and aspartate residues which undergo phosphorylation during the
signal transduction are known to play a special role in the molecules of sensor
hybrid histidine kinases. Substitution of these residues (His482Gln and Asp996Asn)
resulted in a loss of both histidine kinase activity and the ability of CRE1/AHK4 to
respond to cytokinins [<xref ref-type="bibr" rid="R12">12</xref>]. The substitution
of Asp996Asn also resulted in a total loss of phosphatase activity, whereas
substitution of histidine caused only a slight reduction in the activity [<xref ref-type="bibr" rid="R57">57</xref>]. Note that the His482Gln replacement did
not alter the cytokinin-binding capacity of the receptor [<xref ref-type="bibr" rid="R84">84</xref>].</p><p>A number of mutations in CRE1/AHK4 have been obtained using PCR: Gly435Cys,
Phe436Ser, Met447Thr in the second transmembrane domain; Val471Ala in the region
between the second transmembrane and histidine kinase domains; and Met494Leu in the
histidine kinase domain. All these mutations were localized in a short region of
approximately 60 amino acid residues between the ligand-binding domain and the
conserved histidine residue which plays a significant role in protein
autophosphorylation [<xref ref-type="bibr" rid="R31">31</xref>]. These mutations led
to the emergence of constitutive histidine kinase activity in CRE1/AHK4; i.e., this
receptor acquired the ability to send a signal whether cytokinins were present in
the media or not. Meanwhile, the mutant receptors retained their cytokinin-binding
capacity, which has been confirmed in experiments of tritium-labelled
isopentenyladenine binding by these receptors within the membranes of
<italic>Sсhizosaccharomyces pombe</italic> . It is interesting to note
that the CRE1/AHK4 receptor with the Phe436 mutations retained its constitutive
histidine kinase activity even after the <italic>wol</italic> mutation was
additionally introduced, despite losing its cytokinin-binding capacity. Thus, in the
presence of these constitutive mutations the cytokinin-binding capacity of the
receptor plays no role in signal transduction [<xref ref-type="bibr" rid="R31">31</xref>].</p><p>The introduction of mutations into the same regions of the other cytokinin receptors
may also yield the same results. For instance, substitutions of conserved
hydrophobic amino acids in the AHK2 (Ile586Ala) and AHK3 (Val449Ala) receptors,
similar to the Val471Ala substitution in the CRE1/AHK4 receptor, resulted in the
emergence of constitutive histidine kinase activity in the receptors [<xref ref-type="bibr" rid="R31">31</xref>]. The replacements of amino acids in the
second transmembrane domain and in the downstream region could result in
conformation changes in the protein molecule similar to those emerging upon
cytokinin-receptor binding, thus stimulating histidine kinase activity in the
absence of hormone.</p><p>Based on the structure of the cytokinin receptor, it is reasonable to expect that
mutations removing the receiver domain or disturbing its structure will result in
receptor inactivation. Indeed, plants <italic>A. thaliana </italic>carryingmutations in the CRE1/AHK4 receptor gene (called <italic>cre1-3</italic> and
<italic>cre1-7</italic> ) where the triplets encoding Trp1026 and Gln475,
respectively, were replaced with stop codons have been obtained [<xref ref-type="bibr" rid="R85">85</xref>]. It is evident that these mutations result
in the synthesis of a truncated receptor lacking the entire or part of the receiver
domain. In the <italic>cre1-</italic> 6 mutant, the replacement of nucleotides
resulting in Gly493Ala substitution apparently leads to splicing disturbances and to
the formation of the truncated receptor. Thr1008Ile and Ala1032Thr substitutions
occurred in the mutants <italic>cre1-4 </italic> and <italic>cre1-9</italic> ,
respectively. They resulted in the formation of full-size proteins carrying
mutations in the receiver domain [<xref ref-type="bibr" rid="R85">85</xref>]. The
response to phosphate starvation, which is suppressed by cytokinins under normal
conditions, was examined in the resulting mutant plants. As opposed to the controls,
the mutant plants almost did not respond to cytokinin in this biotest. Thus,
mutations leading to the formation of truncated CRE1/AHK4 receptors and mutations in
the receiver domain resulted in the suppression of cytokinin sensitivity of plants
in the phosphate starvation biotest [<xref ref-type="bibr" rid="R85">85</xref>].</p><p>Similar mutations in the MtCRE1 cytokinin receptor have been obtained and studied in
lucerne <italic> Medicago truncatula</italic> [<xref ref-type="bibr" rid="R86">86</xref>]. These mutations affect the histidine kinase domain of the receptor.
In the case of the <italic>mtcre1-1 </italic> mutation, the Trp573-encoding triplet
localized in the middle of the domain was substituted with a stop codon, resulting
in the formation of a truncated protein. The mutation in <italic>mtcre1-2 </italic>consisted in the replacement of Thr642Ile in the conserved G2 motif of the domain.
Upon mutation in <italic>mtcre1-3</italic> , the substitution Gly545Glu was
localized in the variable region of the domain. It has been demonstrated in the
biotest for root growth suppression that the <italic>mtcre1-1 </italic> and
<italic>mtcre1-2</italic> mutants, as opposed to the <italic>mtcre1-3 </italic>mutant, lose their sensitivity to cytokinin. Nodule formation upon exposure to
symbiotic bacteria was disturbed in the <italic>mtcre1-1 </italic> and
<italic>mtcre1-2 </italic> mutants [<xref ref-type="bibr" rid="R86">86</xref>].
All these facts underscore the significant role of each conserved domain in the
normal functioning of the receptor.</p></sec><sec><title>Three-dimensional structure of the receptor</title><p>To understand the structural and functional features of the receptor, it is important
to know the three-dimensional structure of the protein under study. X-ray
crystallography is the most common technique for studying the three-dimensional
structure; a protein monocrystal is required to carry out this type of analysis.
However, crystallization of cytokinin receptors is complicated since they are
high-molecular-weight transmembrane proteins. Therefore, thus far structural studies
have not been completed for any of these receptors.</p><p>It is more realistic to shed light on the structure of a domain of the receptor.
Research in this area has been done for the ligand-binding [79, 87–<xref ref-type="bibr" rid="R89">89</xref>] and receiver [<xref ref-type="bibr" rid="R90">90</xref>, <xref ref-type="bibr" rid="R91">91</xref>] domains. An
attempt to predict the tertiary structure of the CHASE domain of the CRE1/AHK4
receptor was made back in 2004 [<xref ref-type="bibr" rid="R87">87</xref>]. Homology
modeling of the CHASE domain based on the X-ray structures of the ligand-binding
regions of the sensor histidine kinases from bacteria <italic> E. coli</italic>(PDB ID: 1OJG) and <italic>Klebsiella pneumoniae</italic> (PDB ID: 1P0Z) was used in
this study. Molecular docking studies of the cytokinins <italic>trans</italic>-zeatin and kinetin into the putative binding site of this model were subsequently
carried out. The results showed that the CHASE domain corresponds to the so-called
PAS-type domain; the binding site covered the entire cytokinin molecule. A number of
amino acid residues responsible for protein-ligand binding have been identified
[<xref ref-type="bibr" rid="R87">87</xref>] (including Thr278, whose
substitution with Ile - the <italic>wol</italic> mutation - resulted in receptor
inactivation). However, the proposed model turned out to be generally incorrect
presumably due to the too-distant relationship between the template proteins and the
CHASE domain of CRE1/AHK4.</p><p>The investigation of the tentative structure of the hormone binding site in the CHASE
domain was continued using the evolutionary proteomics approach; i.e., the search
for the conserved amino acids of the CHASE domain required for ligand recognition
and binding [<xref ref-type="bibr" rid="R84">84</xref>]. Several amino acid residues
that may participate in the interaction with hormone have been found; five of them
were substituted with alanine in the CRE1/AHK4 receptor. Upon expression of these
mutant receptors in <italic>E. coli</italic> , two out of five substitutions
(Phe281Ala and Thr294Ala) led to complete elimination of the hormone-binding
capacity of the receptor. In two cases (Trp221Ala and Arg282Ala) binding decreased
considerably as compared to the intact CRE1/AHK4 receptor. The Lys274Ala mutation
had no effect. It has been noted that most efficient mutation sites are localized
near the predicted central β-sheet structures of the domain, which assumes that
these β-strands play a significant role in hormone binding. These results were
essentially confirmed by subsequent identification of the X-ray structure of the
CHASE domain in complex with the hormone [<xref ref-type="bibr" rid="R89">89</xref>]: the amino acid residues Thr294, Phe281, and Arg282, indeed, were in
contact with cytokinin, whereas Lys274 did not form direct contacts with the
hormone.</p><p>Decisive success in determining the three-dimensional structure of the CHASE domain
was achieved in 2011, when a research team from the Salk Institute (USA) obtained a
crystal of the CHASE domain of the CRE1/AHK4 receptor suitable for X-ray
crystallographic study [<xref ref-type="bibr" rid="R89">89</xref>]. This allowed to
determine the structure of the ligand-binding CHASE domain of the CRE1/AHK4 receptor
in complex with various cytokinins (PDB ID: 3T4J, 3T4K, 3T4L, 3T4O, 3T4Q, 3T4S,
3T4T; resolution 1.53–2.30 Å). According to the data obtained ( <italic><xref ref-type="fig" rid="F5">Fig. 5</xref></italic> ), the N-terminus of the
CHASE domain forms a long α-helix neighboring two PAS domains connected by
helical linkers. The β-strand closer to the C-terminus of the PAS domain is
covalently linked to the N-terminal α-helix via a disulfide bridge, which makes
the domain structure more rigid and compact. It is interesting to note that similar
tertiary structures of the sensor domains were previously identified in the
histidine kinases of certain bacteria ( <italic>Bacillus subtilis</italic> , PDB ID:
2FOS, 4DBJ; <italic>Sinorhizobium meliloti</italic> , PDB ID: 3E4P;
<italic>Shewanella oneidensis</italic> , PDB ID: 3LIC) despite the low
similarity between the sequences of the bacterial receptors and CRE1/AHK4 [<xref ref-type="bibr" rid="R92">92</xref>]. The sensor domains of both CRE1/AHK4 and
their bacterial homologues crystallized in the form of homodimers. It has been
ascertained that for cytokinin recognition CRE1/AHK4 uses the PAS domain located at
a significant distance from the membrane. The ligand-binding cavity of the receptor
completely embraces the ligand, as shown for a number of the best-known cytokinins:
isopentenyladenine (3T4J), N <sup>6</sup> -benzyladenine (3T4K),
<italic>trans</italic> -zeatin (3T4L), and kinetin (3T4S); differences between
the structures of the receptor CHASE domain in complex with various hormones were
negligible. The “floor” component of the cytokinin-binding site is
formed by the central β-sheet of the PAS domain and is lined by small
hydrophobic amino acid residues. Substitutions of these residues with bulkier amino
acids block the cavity for cytokinin binding, thus inactivating the receptor. That
just occurs upon the most common mutation <italic>wol,</italic> where the small
Thr278 residue is substituted with Ile having a bulkier side chain. Two short
β-strands form the hydrophobic “ceiling” of the active site. The
hydrogen bonds are formed between the adenine component of cytokinin and the Asp262
residue (these bonds play the crucial role in binding), Leu284, Tyr250, and Thr286.
The two latter hydrogen bonds are mediated by water molecules, which in turn
interact with cytokinin atoms. The remaining residues participate in hydrophobic
interactions with both the adenine- and, in particular, the tail component of
cytokinin ( <italic><xref ref-type="table" rid="T2">Table 2</xref>). </italic> The
total number of amino acids forming the ligand binding pocket is approximately 20
([<xref ref-type="bibr" rid="R89">89</xref>] and Hothorn M., personal
communication).</p><fig id="F5" orientation="portrait" position="float"><label>Fig. 5</label><caption><p>Three dimensional structure of the CHASE domain of the Arabidopsis cytokinin
receptor CRE1/AHK4. The general view (A) and structure of the binding site
with a <italic>trans</italic> -zeatin molecule (B). Cytokinin molecule is
shown in spacefill representation, cystine bridge is shown as the
ball-and-stick model. The arrow indicates the location of the bound
cytokinin.</p></caption><graphic xlink:href="AN20758251-04-031-g005"></graphic></fig><table-wrap id="T2" orientation="portrait" position="float"><label>Table 2</label><caption><p> Amino acid residues forming the cytokinin binding site of the CRE1/AHK4
receptor. </p></caption><table frame="hsides" rules="groups"><thead><tr><th rowspan="1" colspan="1">Region in contact with hormone</th><th colspan="13" rowspan="1">Amino acid residues in the CHASE domain cavity
surrounding
the bound N<sup>6</sup>-isopentenyladenine*</th></tr></thead><tbody><tr><td rowspan="2" colspan="1">Adenine
component</td><td rowspan="1" colspan="1">G200</td><td rowspan="1" colspan="1">M226</td><td rowspan="1" colspan="1">V248</td><td rowspan="1" colspan="1">Y250</td><td rowspan="1" colspan="1">L251</td><td rowspan="1" colspan="1">D262</td><td rowspan="1" colspan="1">F281</td><td rowspan="1" colspan="1">R282</td><td rowspan="1" colspan="1">L283</td><td rowspan="1" colspan="1">L284</td><td rowspan="1" colspan="1">T286</td><td rowspan="1" colspan="1">V292</td><td rowspan="1" colspan="1">A322</td></tr><tr><td rowspan="1" colspan="1">1</td><td rowspan="1" colspan="1">1</td><td rowspan="1" colspan="1">2</td><td rowspan="1" colspan="1">H*H*</td><td rowspan="1" colspan="1">3</td><td rowspan="1" colspan="1">HH</td><td rowspan="1" colspan="1">1</td><td rowspan="1" colspan="1">1</td><td rowspan="1" colspan="1">3</td><td rowspan="1" colspan="1">H; 2</td><td rowspan="1" colspan="1">H*</td><td rowspan="1" colspan="1">3</td><td rowspan="1" colspan="1">3</td></tr><tr><td rowspan="2" colspan="1">Tail
component</td><td rowspan="1" colspan="1">A202</td><td rowspan="1" colspan="1">A204</td><td rowspan="1" colspan="1">V241</td><td rowspan="1" colspan="1">M256</td><td rowspan="1" colspan="1">I266</td><td rowspan="1" colspan="1">T294</td><td rowspan="1" colspan="1">Y318</td><td rowspan="1" colspan="1">G320</td><td rowspan="1" colspan="1">G321</td><td rowspan="1" colspan="1"> </td><td rowspan="1" colspan="1"> </td><td rowspan="1" colspan="1"> </td><td rowspan="1" colspan="1"> </td></tr><tr><td rowspan="1" colspan="1">3</td><td rowspan="1" colspan="1">3</td><td rowspan="1" colspan="1">3</td><td rowspan="1" colspan="1">3</td><td rowspan="1" colspan="1">3</td><td rowspan="1" colspan="1">3</td><td rowspan="1" colspan="1">3</td><td rowspan="1" colspan="1">3</td><td rowspan="1" colspan="1">3</td><td rowspan="1" colspan="1"> </td><td rowspan="1" colspan="1"> </td><td rowspan="1" colspan="1"> </td><td rowspan="1" colspan="1"> </td></tr></tbody></table><table-wrap-foot><fn id="TF2-0"><p>* 1, 2, and 3: relative strength of hydrophobic interactions between iP
and AHK4/CRE1; H, and HH: 1–2 hydrogen bonds, H*: hydrogen bond
via water molecule</p></fn></table-wrap-foot></table-wrap><p>The amino acids that play a significant role in binding appeared to be appreciably
conserved in different cytokinin receptors; substitution of these conserved residues
in the CHASE domain of CRE1/AHK4 typically resulted in receptor inactivation [<xref ref-type="bibr" rid="R89">89</xref>].</p><p>In plants, cytokinins can be glycosylated at nitrogen atoms of the adenine moiety,
whereas the OH group of the isoprenoid component of the ligand can be acylated or
glycosylated. As previously mentioned, all these modifications render cytokinins
inactive [<xref ref-type="bibr" rid="R30">30</xref>, <xref ref-type="bibr" rid="R59">59</xref>]. The X-ray structure of the receptor supports these results, since
the limited volume of the ligand-binding cavity is not sufficient to enclose
cytokinins carrying additional glycosyl or other groups.</p><p>As opposed to <italic>cis</italic> -zeatin, <italic>trans</italic> -zeatin forms an
additional hydrogen bond with Thr294 via the OH group of the side chain. This fact
makes it clear why CRE1/AHK4 binds <italic>trans</italic> -zeatin with higher
affinity than <italic>cis</italic> -zeatin. The binding mode for cytokinins carrying
more bulky aromatic tail components was demonstrated by the example of kinetin and
benzyladenine. The furfuryl moiety of kinetin, similar to the isoprenyl group of
<italic>trans</italic> -zeatin, forms a hydrogen bond with Thr294 in the case of
kinetin via water molecule. Using thidiazuron (3T4T structure) as an example it has
been confirmed that the CRE1/AHK4 receptor uses the same site for binding synthetic
and natural cytokinins, synthetic cytokinins forming hydrogen bonds with the same
amino acids as cytokinins - N <sup>6</sup> -adenine derivatives.</p><p>The general principles used to design compounds with cytokinin activity are as
follows: such compounds need to have a planar ring structure occupying the
“adenine” part of the ligand binding cavity, with a linker that is
capable of forming hydrogen bonds with Asn262 and attaching a small planar aliphatic
or aromatic tail group [<xref ref-type="bibr" rid="R89">89</xref>].</p></sec><sec><title>phylogenetic analysis of cytokinin receptors</title><p>Until recently, cytokinin receptors had been studied in detail only in two plant
species (although phylogenetically rather distant): Arabidopsis and corn. Therefore,
it became of interest to elucidate the features of the cytokinin perception
apparatus in other plants species and trace back the formation of the cytokinin
signalling system during plant evolution. Such research became possible thanks to
the complete genome sequencing of a number of plant species.</p><p>The results of the phylogenetic analysis of a number of genomes has enabled
researchers to conclude that the pathway of perception and transduction of the
cytokinin signal based on two-component system emerged in metaphytes after
transition to terrestrial life as one of the aspects of their biochemical adaptation
to new living conditions [<xref ref-type="bibr" rid="R93">93</xref>]. The genes
encoding sensor histidine kinases with the CHASE domain and A-type response
regulators in the genomes of studied species of lower and higher plants have been
found starting from mosses and spikemosses. In higher organized plants the number of
components of the cytokinin signalling system is usually higher compared to that in
more primitive plants. In particular, this applies to phosphotransmitters and
response regulators. It has been noted that the cytokinin receptors of all flowering
plants analyzed fall into three individual branches of the phylogenetic tree,
corresponding to the Arabidopsis receptors CRE1/AHK4, AHK3, and AHK2. In the
evolutionary tree the receptors in archegoniates (moss, spikemoss) keep aloof,
attesting to the fact that three major types of receptors presumably emerged
together with flowering plants but before their split into monocotyledonous and
dicotyledonous plants [<xref ref-type="bibr" rid="R93">93</xref>].</p><p>A broader phylogenetic analysis based on the sequenced genomes of 30 species of
multicellular land plants provided further insight into the evolution of cytokinin
receptors. Among the annotated genes 112 were revealed which encode proteins with a
typical for cytokinin receptors domain organisation, including the CHASE domain,
histidine kinase, and receiver domains ( <italic><xref ref-type="fig" rid="F6">Fig.
6</xref></italic> ). The genes of these sensor histidine kinases are present
in the genomes of all higher plants that have been sequenced. The number of sensor
histidine kinases comprising the CHASE domain varies from one in potato
<italic>Solanum tuberosum </italic> and the common monkey-flower <italic>Mimulus
guttatus </italic> to eight in cultured soybean <italic> Glycine max</italic> .
Several branches of closely related genes have been revealed in flowering plants via
a phylogenetic analysis. Three branches corresponding to the Arabidopsis receptors
АНК2, АНК3, and CRE1/AHK4 have turned out again
to include the largest number of genes. A subdivision into groups of
monocotyledonous and dicotyledonous orthologues has been observed in these branches.
Moreover, certain small branches kept aloof; in particular, the group of
monocotyledonous orthologues ZmHK3. In general, cytokinin receptors can be
phylogenetically subdivided into three and four groups for dicotyledonous and
monocotyledonous plants, respectively. The receptors of one plant species belonging
to different groups are more similar to the group orthologues from other species
than to each other within the same species. These receptor groups are non-identical
in different plant species. As mentioned above, only one receptor belonging to the
orthologues CRE1/AHK4 and AHK3, respectively, has been found in each of the
dicotyledonous plants: potato and the common monkey-flower. If additional genes are
identified in the genomes of these species, it might be that these species contain
the other receptors, too. The StHK4 receptor from potato contains the phenylalanine
residue instead of the conserved Tyr318. However, no direct evidence of a
significant role played by this residue in receptor functioning has been offered
[<xref ref-type="bibr" rid="R89">89</xref>]. It is of interest that tomato, a
close relative of potato, carries the normal representatives of receptors belonging
to all three major evolutionary branches. The CRE1/AHK4 orthologue is duplicated in
the Leguminosae; four orthologues of CRE1/AHK4 (two in each duplication group) have
been identified ( <italic><xref ref-type="fig" rid="F6">Fig. 6</xref></italic> ).
The two other branches contain two representatives of the soybean receptors, each.
In lucerne <italic>Medicago truncatula</italic> the only orthologue of CRE1/AHK4
belongs to either one of the two duplication groups. The common bean
<italic>Phaseolus vulgaris</italic> and <italic>Lotus japonicus </italic> have
two representatives of the orthologue of CRE1/AHK4, each, but they do not have
orthologues of AHK3 or AHK2, respectively. However, the highly conserved leucine in
the PvHK4a from the common bean is substituted with tryptophan, which raises some
doubt as to whether this protein can act as a cytokinin receptor. Few substitutions
of the conserved amino acids have also been revealed in some other dicotyledonous
species (sweet orange <italic>Citrus sinensis</italic> , cucumber <italic>Cucumis
sativus</italic> , and cassave <italic>Manihot esculenta</italic> ). The common
feature of all the dicotyledonous species (with the exception of the common
monkey-flower) is the mandatory presence of orthologues of the CRE1/AHK4
receptor.</p><p>The monocotyledonous species rice and corn also has representatives of two
evolutionary branches of receptors, the orthologues of AHK3 and AHK4. The AHK4 group
can be divided into two subgroups, corresponding to ZmHK1a and ZmHK1b. In corn, two
receptors belong to each of these groups/subgroups. However, the foxtail millet (
<italic>Setaria italica</italic> ) has no orthologues of CRE1/AHK4 in one of the
subgroups (ZmHK1a), whereas sorghum ( <italic>Sorghum bicolour</italic> ) and
<italic>Brachypodium distachyon</italic> have no orthologues of ZmHK3a (
<italic><xref ref-type="fig" rid="F6">Fig. 6</xref></italic> ). Thus, all
the known genomes of monocotyledonous plants encode at least one of the
representatives of CRE1/AHK4 orthologues. It should be mentioned that the
orthologues of CRE1/AHK4 are present in the sequenced genomes of almost all
monocotyledonous plants in two versions. However, it is not improbable that this
feature is typical only of the family Gramineae (for which the genomes have already
been sequenced), whereas the other monocotyledonous families may contain a different
number of CRE1/AHK4 isoforms. But in either case, orthologues of CRE1/AHK4 appear to
be the most important cytokinin receptors in flowering plants at this point.</p></sec><sec sec-type="conclusions"><title>CONCLUSIONS</title><fig id="F6" orientation="portrait" position="float"><label>Fig. 6</label><caption><p>Phylogenetic analysis of cytokinin receptors. The sequence alignment was
performed using the ClustalW program. The phylogenetic tree was built using
the MEGA 5.05 software; the bootstrap analysis includes 1,000 replicates.
Bootstrap supports for the individual branches are given as a percentage
based on 1,000 bootstrap trials.</p></caption><graphic xlink:href="AN20758251-04-031-g006"></graphic></fig><p>Although the major plant hormones have been known since the mid-20th century, just in
the past decades research in phytohormones has undergone a renaissance. This is due
primarily to the elucidation of the molecular mechanism of their action on a cell;
i.e., the discovery of the receptors and genes that encode them, and to the fact
that it is now possible to clone and insert genes for cytokinin perception,
biosynthesis and signal transduction, as well as to obtain targeted mutations
[94–<xref ref-type="bibr" rid="R101">101</xref>]. The fundamentals for
intracellular signalling of phytohormones are similar to those for the signalling of
animal and human hormones. The role of receptors is to recognize the hormone; and
some of the receptor properties are altered upon formation of the hormone-receptor
complex, which results in signal transduction to the primary cellular target via the
corresponding signal transduction system. Similarly to animals, the receptors in
plant cells are mostly localized in two compartments: anchored on membranes or
inside the nucleus (soluble receptors). The main cellular target for hormone
signalling in plants and animals is a set of primary response genes, which is
specific for each hormone. However, the molecular mechanisms of intracellular signal
transduction have been found to be considerably different in plants and animals.
Therefore the results of plant studies have significantly contributed to molecular
hormonology as a field of science.</p><p>For cytokinin signalling, plants use a bacterial-type analogue of the two-component
system of signal transduction, which presumably was borrowed from cyanobacteria
[<xref ref-type="bibr" rid="R20">20</xref>, <xref ref-type="bibr" rid="R24">24</xref>, <xref ref-type="bibr" rid="R94">94</xref>, <xref ref-type="bibr" rid="R102">102</xref>]. It is believed that the symbiosis of cyanobacteria and
eukaryotic cells allowed plants to acquire chloroplasts and to use bacterial genes
for this purposes [<xref ref-type="bibr" rid="R103">103</xref>, <xref ref-type="bibr" rid="R104">104</xref>]. The landfall was a powerful stimulus for
multicellular plants to form new hormonal regulation systems, including the
cytokinin system. As animal cells contain no chloroplast-type organelles, animals
lack the two-component signal transduction system, evidently because of the absence
of symbiosis with the corresponding bacterial progenitors (cyanobacteria).</p><p>It is not by mere chance that the significant progress in revealing the molecular
mechanisms of the action of phytohormones has been achieved in
“post-genomic” 21st century. This was due to whole-plant genome
sequencing, the Arabidopsis genome being the first study of the kind in 2000 [<xref ref-type="bibr" rid="R11">11</xref>]. As a result, Arabidopsis is as yet the
only species whose cytokinin signal perception and transduction system has been
thoroughly characterized. However, a host of questions remain unanswered even as
regards this plant. In this respect, it is worth mentioning that studies devoted to
the investigation of the cytokinin regulatory system are currently under way using
various models and ultra-modern methods of molecular biology, hormonology, genetic
engineering, bioinformatics, etc. The fact that we stand to soon witness new
discoveries in this intriguing and promising field of natural sciences is beyond
question. </p></sec></body><back><ack><p>This work was supported by the RAS Presidium Program “Molecular and Cellular
Biology” and the Russian Foundation for Basic Research
(grants №
10-04-00638, 11-04-00614,
and 11-04-90491).</p></ack><glossary><def-list><title>Abbreviations</title><term-head>Abbreviation</term-head><def-head>Expansion</def-head><def-item><term id="G1">HK</term><def><p>histidine kinase</p></def></def-item><def-item><term id="G2">HP</term><def><p>phosphotransmitter</p></def></def-item><def-item><term id="G3">RR</term><def><p>response regulator</p></def></def-item><def-item><term id="G4">ER</term><def><p>endoplasmic reticulum</p></def></def-item></def-list></glossary><ref-list><title>References</title><ref id="R1"><label>1</label><element-citation publication-type="journal"><name><surname>Miller</surname><given-names>C.O.</given-names></name><name><surname>Skoog</surname><given-names>F.</given-names></name><name><surname>von Saltza</surname><given-names>N.M.</given-names></name><name><surname>Strong</surname><given-names>F.M.</given-names></name><source>J. Am. Soc.</source><volume>77</volume><year>1955</year><page-range>1392</page-range></element-citation></ref><ref id="R2"><label>2</label><element-citation publication-type="journal"><name><surname>Mok</surname><given-names>M.C.</given-names></name><source>Cytokinins. Chemistry, Activity, and Function. Boca Raton, Ann Arbor,
London, Tokyo: CRC Press,</source><year>1994</year><fpage>155</fpage><lpage>166</lpage></element-citation></ref><ref id="R3"><label>3</label><element-citation publication-type="journal"><name><surname>Taiz</surname><given-names>L.</given-names></name><name><surname>Zeiger</surname><given-names>E.</given-names></name><source>Plant Physiology,</source><year>2010</year></element-citation></ref><ref id="R4"><label>4</label><element-citation publication-type="journal"><name><surname>Romanov</surname><given-names>G.A.</given-names></name><source>Russian J. Plant Physiol.</source><volume>56</volume><year>2009</year><fpage>268</fpage><lpage>290</lpage></element-citation></ref><ref id="R5"><label>5</label><element-citation publication-type="journal"><name><surname>Romanov</surname><given-names>G.A.</given-names></name><source>McGraw Hill Encyclopedia of Science & Technol.</source><volume>5</volume><year>2012</year><fpage>205</fpage><lpage>207</lpage></element-citation></ref><ref id="R6"><label>6</label><element-citation publication-type="journal"><name><surname>Choi</surname><given-names>J.</given-names></name><name><surname>Choi</surname><given-names>D.</given-names></name><name><surname>Lee</surname><given-names>S.</given-names></name><name><surname>Ryu</surname><given-names>C.-M.</given-names></name><name><surname>Hwang</surname><given-names>I.</given-names></name><source>Trends Plant Sci.</source><volume>16</volume><year>2011</year><fpage>388</fpage><lpage>394</lpage><pub-id pub-id-type="pmid">21470894</pub-id></element-citation></ref><ref id="R7"><label>7</label><element-citation publication-type="journal"><name><surname>Zalabák</surname><given-names>D.</given-names></name><name><surname>Pospíšilová</surname><given-names>H.</given-names></name><name><surname>Smehilová</surname><given-names>M.</given-names></name><name><surname>Mrízová</surname><given-names>K.</given-names></name><name><surname>Frébort</surname><given-names>I.</given-names></name><name><surname>Galuszka</surname><given-names>P.</given-names></name><source>Biotechnol. Advances.</source><year>2012</year></element-citation></ref><ref id="R8"><label>8</label><element-citation publication-type="journal"><name><surname>Ha</surname><given-names>S.</given-names></name><name><surname>Vankova</surname><given-names>R.</given-names></name><name><surname>Yamaguchi-Shinozaki</surname><given-names>K.</given-names></name><name><surname>Shinozaki</surname><given-names>K.</given-names></name><name><surname>Tran</surname><given-names>L.S.</given-names></name><source>Trends Plant Sci.</source><volume>17</volume><year>2012</year><fpage>172</fpage><lpage>179</lpage><pub-id pub-id-type="pmid">22236698</pub-id></element-citation></ref><ref id="R9"><label>9</label><element-citation publication-type="journal"><name><surname>Gold-von Simson</surname><given-names>G.</given-names></name><name><surname>Goldberg</surname><given-names>J.D.</given-names></name><name><surname>Rolnitzky</surname><given-names>L.M.</given-names></name><name><surname>Mull</surname><given-names>J.</given-names></name><name><surname>Leyne</surname><given-names>M.</given-names></name><name><surname>Voustianiouk</surname><given-names>A.</given-names></name><name><surname>Slaugenhaupt</surname><given-names>S.A.</given-names></name><name><surname>Axelrod</surname><given-names>F.B.</given-names></name><source>Pediatr. Res.</source><volume>65</volume><year>2009</year><fpage>341</fpage><lpage>346</lpage><pub-id pub-id-type="pmid">19033881</pub-id></element-citation></ref><ref id="R10"><label>10</label><element-citation publication-type="journal"><name><surname>Kolyachkina</surname><given-names>S.V.</given-names></name><name><surname>Tararov</surname><given-names>V.I.</given-names></name><name><surname>Alexeev</surname><given-names>C.S.</given-names></name><name><surname>Krivosheev</surname><given-names>D.M.</given-names></name><name><surname>Romanov</surname><given-names>G.A.</given-names></name><name><surname>Stepanova</surname><given-names>E.V.</given-names></name><name><surname>Solomko</surname><given-names>E.S.</given-names></name><name><surname>Inshakov</surname><given-names>A.N.</given-names></name><name><surname>Mikhailov</surname><given-names>S.N.</given-names></name><source>Collect. Czech. Chem. Commun.</source><volume>76</volume><year>2011</year><fpage>1361</fpage><lpage>1378</lpage></element-citation></ref><ref id="R11"><label>11</label><element-citation publication-type="journal"><source>Nature.</source><volume>408</volume><year>2000</year><fpage>796</fpage><lpage>815</lpage><pub-id pub-id-type="pmid">11130711</pub-id></element-citation></ref><ref id="R12"><label>12</label><element-citation publication-type="journal"><name><surname>Inoue</surname><given-names>T.</given-names></name><name><surname>Higuchi</surname><given-names>M.</given-names></name><name><surname>Hashimoto</surname><given-names>Y.</given-names></name><name><surname>Seki</surname><given-names>M.</given-names></name><name><surname>Kobayashi</surname><given-names>M.</given-names></name><name><surname>Kato</surname><given-names>T.</given-names></name><name><surname>Tabata</surname><given-names>S.</given-names></name><name><surname>Shinozaki</surname><given-names>K.</given-names></name><name><surname>Kakimoto</surname><given-names>T.</given-names></name><source>Nature.</source><volume>409</volume><year>2001</year><fpage>1060</fpage><lpage>1063</lpage><pub-id pub-id-type="pmid">11234017</pub-id></element-citation></ref><ref id="R13"><label>13</label><element-citation publication-type="journal"><name><surname>Suzuki</surname><given-names>T.</given-names></name><name><surname>Miwa</surname><given-names>K.</given-names></name><name><surname>Ishikawa</surname><given-names>K.</given-names></name><name><surname>Yamada</surname><given-names>H.</given-names></name><name><surname>Aiba</surname><given-names>H.</given-names></name><name><surname>Mizuno</surname><given-names>T.</given-names></name><source>Plant Cell Physiol.</source><volume>42</volume><year>2001</year><fpage>107</fpage><lpage>113</lpage><pub-id pub-id-type="pmid">11230563</pub-id></element-citation></ref><ref id="R14"><label>14</label><element-citation publication-type="journal"><name><surname>Ueguchi</surname><given-names>C.</given-names></name><name><surname>Sato</surname><given-names>S.</given-names></name><name><surname>Kato</surname><given-names>T.</given-names></name><name><surname>Tabata</surname><given-names>S.</given-names></name><source>Plant Cell Physiol.</source><volume>42</volume><year>2001</year><fpage>751</fpage><lpage>755</lpage><pub-id pub-id-type="pmid">11479382</pub-id></element-citation></ref><ref id="R15"><label>15</label><element-citation publication-type="journal"><name><surname>Yamada</surname><given-names>H.</given-names></name><name><surname>Suzuki</surname><given-names>T.</given-names></name><name><surname>Terada</surname><given-names>K.</given-names></name><name><surname>Takei</surname><given-names>K.</given-names></name><name><surname>Ishikawa</surname><given-names>K.</given-names></name><name><surname>Miwa</surname><given-names>K.</given-names></name><name><surname>Yamashino</surname><given-names>T.</given-names></name><name><surname>Mizuno</surname><given-names>T.</given-names></name><source>Plant Cell Physiol.</source><volume>42</volume><year>2001</year><fpage>1017</fpage><lpage>1023</lpage><pub-id pub-id-type="pmid">11577198</pub-id></element-citation></ref><ref id="R16"><label>16</label><element-citation publication-type="journal"><name><surname>Mähönen</surname><given-names>A.P.</given-names></name><name><surname>Bonke</surname><given-names>M.</given-names></name><name><surname>Kauppinen</surname><given-names>L.</given-names></name><name><surname>Riikonen</surname><given-names>M.</given-names></name><name><surname>Benfey</surname><given-names>P.N.</given-names></name><name><surname>Helariutta</surname><given-names>Y.</given-names></name><source>Genes Dev.</source><volume>14</volume><year>2000</year><fpage>2938</fpage><lpage>2943</lpage><pub-id pub-id-type="pmid">11114883</pub-id></element-citation></ref><ref id="R17"><label>17</label><element-citation publication-type="journal"><name><surname>Ueguchi</surname><given-names>C.</given-names></name><name><surname>Koizumi</surname><given-names>H.</given-names></name><name><surname>Suzuki</surname><given-names>T.</given-names></name><name><surname>Mizuno</surname><given-names>T.</given-names></name><source>Plant Cell Physiol.</source><volume>42</volume><year>2001</year><fpage>231</fpage><lpage>235</lpage><pub-id pub-id-type="pmid">11230578</pub-id></element-citation></ref><ref id="R18"><label>18</label><element-citation publication-type="journal"><name><surname>Anantharaman</surname><given-names>V.</given-names></name><name><surname>Aravind</surname><given-names>L.</given-names></name><source>Trends Biochem Sci.</source><volume>26</volume><year>2001</year><fpage>579</fpage><lpage>582</lpage><pub-id pub-id-type="pmid">11590000</pub-id></element-citation></ref><ref id="R19"><label>19</label><element-citation publication-type="journal"><name><surname>Mougel</surname><given-names>C.</given-names></name><name><surname>Zhulin</surname><given-names>I.B.</given-names></name><source>Trends Biochem Sci.</source><volume>26</volume><year>2001</year><fpage>582</fpage><lpage>584</lpage><pub-id pub-id-type="pmid">11590001</pub-id></element-citation></ref><ref id="R20"><label>20</label><element-citation publication-type="journal"><name><surname>Wolanin</surname><given-names>P.M.</given-names></name><name><surname>Thomason</surname><given-names>P.A.</given-names></name><name><surname>Stock</surname><given-names>J.B.</given-names></name><source>Genome Biol.</source><volume>3</volume><year>2002</year><page-range>3013</page-range></element-citation></ref><ref id="R21"><label>21</label><element-citation publication-type="journal"><name><surname>Heyl</surname><given-names>A.</given-names></name><name><surname>Schmülling</surname><given-names>T.</given-names></name><source>Cur. Opin. Plant Biol.</source><volume>6</volume><year>2003</year><fpage>480</fpage><lpage>488</lpage></element-citation></ref><ref id="R22"><label>22</label><element-citation publication-type="journal"><name><surname>Maxwell</surname><given-names>B.B.</given-names></name><name><surname>Kieber</surname><given-names>J.J.</given-names></name><source>Plant Hormones: Biosynthesis, Signal Transduction, Action! P.J. Davies,
ed. Dordrecht, The Netherlands: Kluwer Academic Publishers.</source><year>2005</year><fpage>321</fpage><lpage>349</lpage></element-citation></ref><ref id="R23"><label>23</label><element-citation publication-type="journal"><name><surname>Schaller</surname><given-names>G.E.</given-names></name><name><surname>Kieber</surname><given-names>J.J.</given-names></name><name><surname>Shiu</surname><given-names>S.-H.</given-names></name><source>The Arabidopsis Book.</source><year>2008</year><fpage>1</fpage><lpage>12</lpage></element-citation></ref><ref id="R24"><label>24</label><element-citation publication-type="journal"><name><surname>Schaller</surname><given-names>G.E.</given-names></name><name><surname>Shiu</surname><given-names>S.-H.</given-names></name><name><surname>Armitage</surname><given-names>J.P.</given-names></name><source>Current Biol.</source><volume>21</volume><year>2011</year></element-citation></ref><ref id="R25"><label>25</label><element-citation publication-type="journal"><name><surname>West</surname><given-names>A.H.</given-names></name><name><surname>Stock</surname><given-names>A.M.</given-names></name><source>Trends Biochem. Sci.</source><volume>26</volume><year>2001</year><fpage>369</fpage><lpage>376</lpage><pub-id pub-id-type="pmid">11406410</pub-id></element-citation></ref><ref id="R26"><label>26</label><element-citation publication-type="journal"><name><surname>Punwani</surname><given-names>J.A.</given-names></name><name><surname>Hutchison</surname><given-names>C.E.</given-names></name><name><surname>Schaller</surname><given-names>G.E.</given-names></name><name><surname>Kieber</surname><given-names>J.J.</given-names></name><source>Plant J.</source><volume>62</volume><year>2010</year><fpage>473</fpage><lpage>482</lpage><pub-id pub-id-type="pmid">20136728</pub-id></element-citation></ref><ref id="R27"><label>27</label><element-citation publication-type="journal"><name><surname>Brandstatter</surname><given-names>I.</given-names></name><name><surname>Kieber</surname><given-names>J.J.</given-names></name><source>Plant Cell.</source><volume>10</volume><year>1998</year><fpage>1009</fpage><lpage>1020</lpage><pub-id pub-id-type="pmid">9634588</pub-id></element-citation></ref><ref id="R28"><label>28</label><element-citation publication-type="journal"><name><surname>Rashotte</surname><given-names>A.M.</given-names></name><name><surname>Carson</surname><given-names>S.D.B.</given-names></name><name><surname>To</surname><given-names>J.P.C.</given-names></name><name><surname>Kieber</surname><given-names>J.J.</given-names></name><source>Plant Physiol.</source><volume>132</volume><year>2003</year><fpage>1998</fpage><lpage>2011</lpage><pub-id pub-id-type="pmid">12913156</pub-id></element-citation></ref><ref id="R29"><label>29</label><element-citation publication-type="journal"><name><surname>Brenner</surname><given-names>W.G.</given-names></name><name><surname>Romanov</surname><given-names>G.A.</given-names></name><name><surname>Köllmer</surname><given-names>I.</given-names></name><name><surname>Bürkle</surname><given-names>L.</given-names></name><name><surname>Schmülling</surname><given-names>T.</given-names></name><source>Plant J.</source><volume>44</volume><year>2005</year><fpage>314</fpage><lpage>333</lpage><pub-id pub-id-type="pmid">16212609</pub-id></element-citation></ref><ref id="R30"><label>30</label><element-citation publication-type="journal"><name><surname>Spíchal</surname><given-names>L.</given-names></name><name><surname>Rakova</surname><given-names>N.Y.</given-names></name><name><surname>Riefler</surname><given-names>M.</given-names></name><name><surname>Mizuno</surname><given-names>T.</given-names></name><name><surname>Romanov</surname><given-names>G.A.</given-names></name><name><surname>Strnad</surname><given-names>M.</given-names></name><name><surname>Schmülling</surname><given-names>T.</given-names></name><source>Plant Cell Physiol.</source><volume>45</volume><year>2004</year><fpage>1299</fpage><lpage>1305</lpage><pub-id pub-id-type="pmid">15509853</pub-id></element-citation></ref><ref id="R31"><label>31</label><element-citation publication-type="journal"><name><surname>Miwa</surname><given-names>K.</given-names></name><name><surname>Ishikawa</surname><given-names>K.</given-names></name><name><surname>Terada</surname><given-names>K.</given-names></name><name><surname>Yamada</surname><given-names>H.</given-names></name><name><surname>Suzuki</surname><given-names>T.</given-names></name><name><surname>Yamashino</surname><given-names>T.</given-names></name><name><surname>Mizuno</surname><given-names>T.</given-names></name><source>Plant Cell Physiol.</source><volume>48</volume><year>2007</year><fpage>1809</fpage><lpage>1814</lpage><pub-id pub-id-type="pmid">17956858</pub-id></element-citation></ref><ref id="R32"><label>32</label><element-citation publication-type="journal"><name><surname>Higuchi</surname><given-names>M.</given-names></name><name><surname>Pischke</surname><given-names>M.S.</given-names></name><name><surname>Mähönen</surname><given-names>A.P.</given-names></name><name><surname>Miyawaki</surname><given-names>K.</given-names></name><name><surname>Hashimoto</surname><given-names>Y.</given-names></name><name><surname>Seki</surname><given-names>M.</given-names></name><name><surname>Kobayashi</surname><given-names>M.</given-names></name><name><surname>Shinozaki</surname><given-names>K.</given-names></name><name><surname>Kato</surname><given-names>T.</given-names></name><name><surname>Tabata</surname><given-names>S.</given-names></name><name><surname>Helariutta</surname><given-names>Y.</given-names></name><name><surname>Sussman</surname><given-names>M.R.</given-names></name><name><surname>Kakimoto</surname><given-names>T.</given-names></name><source>Proc Natl Acad Sci USA.</source><volume>101</volume><year>2004</year><fpage>8821</fpage><lpage>8826</lpage><pub-id pub-id-type="pmid">15166290</pub-id></element-citation></ref><ref id="R33"><label>33</label><element-citation publication-type="journal"><name><surname>Nishimura</surname><given-names>C.</given-names></name><name><surname>Ohashi</surname><given-names>Y.</given-names></name><name><surname>Sato</surname><given-names>S.</given-names></name><name><surname>Kato</surname><given-names>T.</given-names></name><name><surname>Tabata</surname><given-names>S.</given-names></name><name><surname>Ueguchi</surname><given-names>C.</given-names></name><source>Plant Cell.</source><volume>16</volume><year>2004</year><fpage>1365</fpage><lpage>1377</lpage><pub-id pub-id-type="pmid">15155880</pub-id></element-citation></ref><ref id="R34"><label>34</label><element-citation publication-type="journal"><name><surname>Riefler</surname><given-names>M.</given-names></name><name><surname>Novak</surname><given-names>O.</given-names></name><name><surname>Strnad</surname><given-names>M.</given-names></name><name><surname>Schmülling</surname><given-names>T.</given-names></name><source>Plant Cell.</source><volume>18</volume><year>2006</year><fpage>40</fpage><lpage>54</lpage><pub-id pub-id-type="pmid">16361392</pub-id></element-citation></ref><ref id="R35"><label>35</label><element-citation publication-type="journal"><name><surname>Shi</surname><given-names>X.</given-names></name><name><surname>Rashotte</surname><given-names>A.M.</given-names></name><source>Plant Cell Rep.</source><volume>31</volume><year>2012</year><fpage>789</fpage><lpage>799</lpage><pub-id pub-id-type="pmid">22350315</pub-id></element-citation></ref><ref id="R36"><label>36</label><element-citation publication-type="journal"><name><surname>Tanaka</surname><given-names>Y.</given-names></name><name><surname>Suzuki</surname><given-names>T.</given-names></name><name><surname>Yamashino</surname><given-names>T.</given-names></name><name><surname>Mizuno</surname><given-names>T.</given-names></name><source>Biosci. Biotechnol. Biochem.</source><volume>68</volume><year>2004</year><fpage>462</fpage><lpage>465</lpage><pub-id pub-id-type="pmid">14981318</pub-id></element-citation></ref><ref id="R37"><label>37</label><element-citation publication-type="journal"><name><surname>Hutchison</surname><given-names>C.E.</given-names></name><name><surname>Li</surname><given-names>J.</given-names></name><name><surname>Argueso</surname><given-names>C.</given-names></name><name><surname>Gonzalez</surname><given-names>M.</given-names></name><name><surname>Lee</surname><given-names>E.</given-names></name><name><surname>Lewis</surname><given-names>M.W.</given-names></name><name><surname>Maxwell</surname><given-names>B.B.</given-names></name><name><surname>Perdue</surname><given-names>T.D.</given-names></name><name><surname>Schaller</surname><given-names>G.E.</given-names></name><name><surname>Alonso</surname><given-names>J.M.</given-names></name><name><surname>Ecker</surname><given-names>J.R.</given-names></name><name><surname>Kieber</surname><given-names>J.J.</given-names></name><source>Plant Cell.</source><volume>18</volume><year>2006</year><fpage>3073</fpage><lpage>3087</lpage><pub-id pub-id-type="pmid">17122069</pub-id></element-citation></ref><ref id="R38"><label>38</label><element-citation publication-type="journal"><name><surname>Dortay</surname><given-names>H.</given-names></name><name><surname>Mehnert</surname><given-names>N.</given-names></name><name><surname>Bürkle</surname><given-names>L.</given-names></name><name><surname>Schmülling</surname><given-names>T.</given-names></name><name><surname>Heyl</surname><given-names>A.</given-names></name><source>FEBS J.</source><volume>273</volume><year>2006</year><fpage>4631</fpage><lpage>4644</lpage><pub-id pub-id-type="pmid">16965536</pub-id></element-citation></ref><ref id="R39"><label>39</label><element-citation publication-type="journal"><name><surname>Deng</surname><given-names>Y.</given-names></name><name><surname>Dong</surname><given-names>H.</given-names></name><name><surname>Mu</surname><given-names>J.</given-names></name><name><surname>Zheng</surname><given-names>B.</given-names></name><name><surname>Ji</surname><given-names>Z.</given-names></name><name><surname>Yang</surname><given-names>W.-C.</given-names></name><name><surname>Liang</surname><given-names>Y.</given-names></name><name><surname>Zuo</surname><given-names>J.</given-names></name><source>Plant Cell.</source><volume>22</volume><year>2010</year><fpage>1232</fpage><lpage>1248</lpage><pub-id pub-id-type="pmid">20363773</pub-id></element-citation></ref><ref id="R40"><label>40</label><element-citation publication-type="journal"><name><surname>Lu</surname><given-names>J.M.</given-names></name><name><surname>Deschenes</surname><given-names>R.J.</given-names></name><name><surname>Fassler</surname><given-names>J.S.</given-names></name><source>Eukaryot. Cell.</source><volume>2</volume><year>2003</year><fpage>1304</fpage><lpage>1314</lpage><pub-id pub-id-type="pmid">14665464</pub-id></element-citation></ref><ref id="R41"><label>41</label><element-citation publication-type="journal"><name><surname>Mähönen</surname><given-names>A.P.</given-names></name><name><surname>Bishopp</surname><given-names>A.</given-names></name><name><surname>Higuchi</surname><given-names>M.</given-names></name><name><surname>Nieminen</surname><given-names>K.M.</given-names></name><name><surname>Kinoshita</surname><given-names>K.</given-names></name><name><surname>Törmäkangas</surname><given-names>K.</given-names></name><name><surname>Ikeda</surname><given-names>Y.</given-names></name><name><surname>Oka</surname><given-names>A.</given-names></name><name><surname>Kakimoto</surname><given-names>T.</given-names></name><name><surname>Helariutta</surname><given-names>Y.</given-names></name><source>Science.</source><volume>6</volume><year>2006</year><fpage>94</fpage><lpage>98</lpage></element-citation></ref><ref id="R42"><label>42</label><element-citation publication-type="journal"><name><surname>Gupta</surname><given-names>S.</given-names></name><name><surname>Rashotte</surname><given-names>A.M.</given-names></name><source>Plant Cell Rep.</source><volume>31</volume><year>2012</year><fpage>801</fpage><lpage>812</lpage><pub-id pub-id-type="pmid">22315145</pub-id></element-citation></ref><ref id="R43"><label>43</label><element-citation publication-type="journal"><name><surname>Lohrmann</surname><given-names>J.</given-names></name><name><surname>Sweere</surname><given-names>U.</given-names></name><name><surname>Zabaleta</surname><given-names>E.</given-names></name><name><surname>Bäurle</surname><given-names>I.</given-names></name><name><surname>Keitel</surname><given-names>C.</given-names></name><name><surname>Kozma-Bognar</surname><given-names>L.</given-names></name><name><surname>Brennicke</surname><given-names>A.</given-names></name><name><surname>Schäfer</surname><given-names>E.</given-names></name><name><surname>Kudla</surname><given-names>J.</given-names></name><name><surname>Harter</surname><given-names>K.</given-names></name><source>Mol Genet Genomics.</source><volume>265</volume><year>2001</year><fpage>2</fpage><lpage>13</lpage><pub-id pub-id-type="pmid">11370868</pub-id></element-citation></ref><ref id="R44"><label>44</label><element-citation publication-type="journal"><name><surname>Sakai</surname><given-names>H.</given-names></name><name><surname>Aoyama</surname><given-names>T.</given-names></name><name><surname>Bono</surname><given-names>H.</given-names></name><name><surname>Oka</surname><given-names>A.</given-names></name><source>Plant Cell Physiol.</source><volume>39</volume><year>1998</year><fpage>1232</fpage><lpage>1239</lpage><pub-id pub-id-type="pmid">9891419</pub-id></element-citation></ref><ref id="R45"><label>45</label><element-citation publication-type="journal"><name><surname>Sakai</surname><given-names>H.</given-names></name><name><surname>Aoyama</surname><given-names>T.</given-names></name><name><surname>Oka</surname><given-names>A.</given-names></name><source>Plant J.</source><volume>24</volume><year>2000</year><fpage>703</fpage><lpage>711</lpage><pub-id pub-id-type="pmid">11135105</pub-id></element-citation></ref><ref id="R46"><label>46</label><element-citation publication-type="journal"><name><surname>Hosoda</surname><given-names>K.</given-names></name><name><surname>Imamura</surname><given-names>A.</given-names></name><name><surname>Katoh</surname><given-names>E.</given-names></name><name><surname>Hatta</surname><given-names>T.</given-names></name><name><surname>Tachiki</surname><given-names>M.</given-names></name><name><surname>Yamada</surname><given-names>H.</given-names></name><name><surname>Mizuno</surname><given-names>T.</given-names></name><name><surname>Yamazaki</surname><given-names>T.</given-names></name><source>Plant Cell.</source><volume>14</volume><year>2002</year><fpage>2015</fpage><lpage>2029</lpage><pub-id pub-id-type="pmid">12215502</pub-id></element-citation></ref><ref id="R47"><label>47</label><element-citation publication-type="journal"><name><surname>Mason</surname><given-names>M.G.</given-names></name><name><surname>Mathews</surname><given-names>D.E.</given-names></name><name><surname>Argyros</surname><given-names>D.A.</given-names></name><name><surname>Maxwell</surname><given-names>B.B.</given-names></name><name><surname>Kieber</surname><given-names>J.J.</given-names></name><name><surname>Alonso</surname><given-names>J.M.</given-names></name><name><surname>Ecker</surname><given-names>J.R.</given-names></name><name><surname>Schaller</surname><given-names>G.E.</given-names></name><source>Plant Cell.</source><volume>17</volume><year>2005</year><fpage>3007</fpage><lpage>3018</lpage><pub-id pub-id-type="pmid">16227453</pub-id></element-citation></ref><ref id="R48"><label>48</label><element-citation publication-type="journal"><name><surname>Ishida</surname><given-names>K.</given-names></name><name><surname>Yamashino</surname><given-names>T.</given-names></name><name><surname>Yokoyama</surname><given-names>A.</given-names></name><name><surname>Mizuno</surname><given-names>T.</given-names></name><source>Plant Cell Physiol.</source><volume>49</volume><year>2008</year><fpage>47</fpage><lpage>57</lpage><pub-id pub-id-type="pmid">18037673</pub-id></element-citation></ref><ref id="R49"><label>49</label><element-citation publication-type="journal"><name><surname>Argyros</surname><given-names>R.D.</given-names></name><name><surname>Mathews</surname><given-names>D.E.</given-names></name><name><surname>Chiang</surname><given-names>Y.-H.</given-names></name><name><surname>Palmer</surname><given-names>C.M.</given-names></name><name><surname>Thibault</surname><given-names>D.M.</given-names></name><name><surname>Etheridge</surname><given-names>N.</given-names></name><name><surname>Argyros</surname><given-names>D.A.</given-names></name><name><surname>Mason</surname><given-names>M.G.</given-names></name><name><surname>Kieber</surname><given-names>J.J.</given-names></name><name><surname>Schaller</surname><given-names>G.E.</given-names></name><source>Plant Cell.</source><volume>20</volume><year>2008</year><fpage>2102</fpage><lpage>2116</lpage><pub-id pub-id-type="pmid">18723577</pub-id></element-citation></ref><ref id="R50"><label>50</label><element-citation publication-type="journal"><name><surname>Imamura</surname><given-names>A.</given-names></name><name><surname>Hanaki</surname><given-names>N.</given-names></name><name><surname>Nakamura</surname><given-names>A.</given-names></name><name><surname>Suzuki</surname><given-names>T.</given-names></name><name><surname>Taniguchi</surname><given-names>M.</given-names></name><name><surname>Kiba</surname><given-names>T.</given-names></name><name><surname>Ueguchi</surname><given-names>C.</given-names></name><name><surname>Sugiyama</surname><given-names>T.</given-names></name><name><surname>Mizuno</surname><given-names>T.</given-names></name><source>Plant Cell Physiol.</source><volume>40</volume><year>1999</year><fpage>733</fpage><lpage>42</lpage><pub-id pub-id-type="pmid">10501033</pub-id></element-citation></ref><ref id="R51"><label>51</label><element-citation publication-type="journal"><name><surname>Che</surname><given-names>P.</given-names></name><name><surname>Gingerich</surname><given-names>D.J.</given-names></name><name><surname>Lall</surname><given-names>S.</given-names></name><name><surname>Howell</surname><given-names>S.H.</given-names></name><source>Plant Cell.</source><volume>14</volume><year>2002</year><fpage>2771</fpage><lpage>2785</lpage><pub-id pub-id-type="pmid">12417700</pub-id></element-citation></ref><ref id="R52"><label>52</label><element-citation publication-type="journal"><name><surname>Kieber</surname><given-names>JJ.</given-names></name><source>Plant Physiol.</source><volume>124</volume><year>2000</year><fpage>1706</fpage><lpage>1717</lpage><pub-id pub-id-type="pmid">11115887</pub-id></element-citation></ref><ref id="R53"><label>53</label><element-citation publication-type="journal"><name><surname>Hwang</surname><given-names>I.</given-names></name><name><surname>Sheen</surname><given-names>J.</given-names></name><source>Nature.</source><volume>413</volume><year>2001</year><fpage>383</fpage><lpage>389</lpage><pub-id pub-id-type="pmid">11574878</pub-id></element-citation></ref><ref id="R54"><label>54</label><element-citation publication-type="journal"><name><surname>To</surname><given-names>J.P.</given-names></name><name><surname>Haberer</surname><given-names>G.</given-names></name><name><surname>Ferreira</surname><given-names>F.J.</given-names></name><name><surname>Deruère</surname><given-names>J.</given-names></name><name><surname>Mason</surname><given-names>M.G.</given-names></name><name><surname>Schaller</surname><given-names>G.E.</given-names></name><name><surname>Alonso</surname><given-names>J.M.</given-names></name><name><surname>Ecker</surname><given-names>J.R.</given-names></name><name><surname>Kieber</surname><given-names>J.J.</given-names></name><source>Plant Cell.</source><volume>16</volume><year>2004</year><fpage>658</fpage><lpage>671</lpage><pub-id pub-id-type="pmid">14973166</pub-id></element-citation></ref><ref id="R55"><label>55</label><element-citation publication-type="journal"><name><surname>Lee</surname><given-names>D.J.</given-names></name><name><surname>Park</surname><given-names>J.Y.</given-names></name><name><surname>Ku</surname><given-names>S.J.</given-names></name><name><surname>Ha</surname><given-names>Y.M.</given-names></name><name><surname>Kim</surname><given-names>S.</given-names></name><name><surname>Kim</surname><given-names>M.D.</given-names></name><name><surname>Oh</surname><given-names>M.H.</given-names></name><name><surname>Kim</surname><given-names>J.</given-names></name><source>Mol Genet Genomics.</source><volume>277</volume><year>2007</year><fpage>115</fpage><lpage>137</lpage><pub-id pub-id-type="pmid">17061125</pub-id></element-citation></ref><ref id="R56"><label>56</label><element-citation publication-type="journal"><name><surname>Müller</surname><given-names>B.</given-names></name><source>J. Exp. Bot.</source><volume>62</volume><year>2011</year><fpage>3273</fpage><lpage>3288</lpage><pub-id pub-id-type="pmid">21212299</pub-id></element-citation></ref><ref id="R57"><label>57</label><element-citation publication-type="journal"><name><surname>Mähönen</surname><given-names>A.P.</given-names></name><name><surname>Higuchi</surname><given-names>M.</given-names></name><name><surname>Törmäkangas</surname><given-names>K.</given-names></name><name><surname>Miyawaki</surname><given-names>K.</given-names></name><name><surname>Pischke</surname><given-names>M.S.</given-names></name><name><surname>Sussman</surname><given-names>M.R.</given-names></name><name><surname>Helariutta</surname><given-names>Y.</given-names></name><name><surname>Kakimoto</surname><given-names>T.</given-names></name><source>Curr Biol.</source><volume>16</volume><year>2006</year><fpage>1116</fpage><lpage>1122</lpage><pub-id pub-id-type="pmid">16753566</pub-id></element-citation></ref><ref id="R58"><label>58</label><element-citation publication-type="journal"><name><surname>Kim</surname><given-names>H.J.</given-names></name><name><surname>Ryu</surname><given-names>H.</given-names></name><name><surname>Hong</surname><given-names>S.H.</given-names></name><name><surname>Woo</surname><given-names>H.R.</given-names></name><name><surname>Lim</surname><given-names>P.O.</given-names></name><name><surname>Lee</surname><given-names>I.C.</given-names></name><name><surname>Sheen</surname><given-names>J.</given-names></name><name><surname>Nam</surname><given-names>H.G.</given-names></name><name><surname>Hwang</surname><given-names>I.</given-names></name><source>Proc. Nat. Acad. Sci. USA.</source><volume>103</volume><year>2006</year><fpage>814</fpage><lpage>819</lpage><pub-id pub-id-type="pmid">16407152</pub-id></element-citation></ref><ref id="R59"><label>59</label><element-citation publication-type="journal"><name><surname>Romanov</surname><given-names>G.A.</given-names></name><name><surname>Lomin</surname><given-names>S.N.</given-names></name><name><surname>Schmülling</surname><given-names>T.</given-names></name><source>J. Exp. Bot.</source><volume>57</volume><year>2006</year><fpage>4051</fpage><lpage>4058</lpage><pub-id pub-id-type="pmid">17075078</pub-id></element-citation></ref><ref id="R60"><label>60</label><element-citation publication-type="journal"><name><surname>Lomin</surname><given-names>S.N.</given-names></name><name><surname>Yonekura-Sakakibara</surname><given-names>K.</given-names></name><name><surname>Romanov</surname><given-names>G.A.</given-names></name><name><surname>Sakakibara</surname><given-names>H.</given-names></name><source>J. Exp. Bot.</source><volume>62</volume><year>2011</year><fpage>5149</fpage><lpage>5159</lpage><pub-id pub-id-type="pmid">21778179</pub-id></element-citation></ref><ref id="R61"><label>61</label><element-citation publication-type="journal"><name><surname>Wulfetange</surname><given-names>K.</given-names></name><name><surname>Lomin</surname><given-names>S.N.</given-names></name><name><surname>Romanov</surname><given-names>G.A.</given-names></name><name><surname>Stolz</surname><given-names>A.</given-names></name><name><surname>Heyl</surname><given-names>A.</given-names></name><name><surname>Schmülling</surname><given-names>T.</given-names></name><source>Plant Physiol.</source><volume>156</volume><year>2011</year><fpage>1808</fpage><lpage>1818</lpage><pub-id pub-id-type="pmid">21709172</pub-id></element-citation></ref><ref id="R62"><label>62</label><element-citation publication-type="journal"><name><surname>Caesar</surname><given-names>K.</given-names></name><name><surname>Thamm</surname><given-names>A.M.</given-names></name><name><surname>Witthöft</surname><given-names>J.</given-names></name><name><surname>Elgass</surname><given-names>K.</given-names></name><name><surname>Huppenberger</surname><given-names>P.</given-names></name><name><surname>Grefen</surname><given-names>C.</given-names></name><name><surname>Horak</surname><given-names>J.</given-names></name><name><surname>Harter</surname><given-names>K.</given-names></name><source>J. Exp. Bot.</source><volume>62</volume><year>2011</year><fpage>5571</fpage><lpage>5580</lpage><pub-id pub-id-type="pmid">21841169</pub-id></element-citation></ref><ref id="R63"><label>63</label><element-citation publication-type="journal"><name><surname>Chen</surname><given-names>Y.-F.</given-names></name><name><surname>Randlett</surname><given-names>M.D.</given-names></name><name><surname>Findell</surname><given-names>J.L.</given-names></name><name><surname>Schaller</surname><given-names>G.E.</given-names></name><source>J. Biol. Chem.</source><volume>277</volume><year>2002</year><fpage>19861</fpage><lpage>19866</lpage><pub-id pub-id-type="pmid">11916973</pub-id></element-citation></ref><ref id="R64"><label>64</label><element-citation publication-type="journal"><name><surname>Grefen</surname><given-names>C.</given-names></name><name><surname>Städele</surname><given-names>K.</given-names></name><name><surname>Růzicka</surname><given-names>K.</given-names></name><name><surname>Obrdlik</surname><given-names>P.</given-names></name><name><surname>Harter</surname><given-names>K.</given-names></name><name><surname>Horák</surname><given-names>J.</given-names></name><source>Mol. Plant.</source><volume>1</volume><year>2008</year><fpage>308</fpage><lpage>320</lpage><pub-id pub-id-type="pmid">19825542</pub-id></element-citation></ref><ref id="R65"><label>65</label><element-citation publication-type="journal"><name><surname>Mok</surname><given-names>D.W.S.</given-names></name><name><surname>Mok</surname><given-names>M.C.</given-names></name><source>Annu. Rev. Plant Physiol. Plant Mol. Biol.</source><volume>52</volume><year>2001</year><fpage>89</fpage><lpage>118</lpage><pub-id pub-id-type="pmid">11337393</pub-id></element-citation></ref><ref id="R66"><label>66</label><element-citation publication-type="journal"><name><surname>Takei</surname><given-names>K.</given-names></name><name><surname>Sakakibara</surname><given-names>H.</given-names></name><name><surname>Taniguchi</surname><given-names>M.</given-names></name><name><surname>Sugiyama</surname><given-names>T.</given-names></name><source>Plant Cell Physiol.</source><volume>42</volume><year>2001</year><fpage>85</fpage><lpage>93</lpage><pub-id pub-id-type="pmid">11158447</pub-id></element-citation></ref><ref id="R67"><label>67</label><element-citation publication-type="journal"><name><surname>Corbesier</surname><given-names>L.</given-names></name><name><surname>Prinsen</surname><given-names>E.</given-names></name><name><surname>Jackmard</surname><given-names>A.</given-names></name><name><surname>Lejeune</surname><given-names>P.</given-names></name><name><surname>van Onckelen</surname><given-names>H.</given-names></name><name><surname>Perilleux</surname><given-names>C.</given-names></name><name><surname>Bernier</surname><given-names>G.</given-names></name><source>J. Exp. Bot.</source><volume>54</volume><year>2003</year><fpage>2511</fpage><lpage>2517</lpage><pub-id pub-id-type="pmid">14512385</pub-id></element-citation></ref><ref id="R68"><label>68</label><element-citation publication-type="journal"><name><surname>Hirose</surname><given-names>N.</given-names></name><name><surname>Takei</surname><given-names>K.</given-names></name><name><surname>Kuroha</surname><given-names>T.</given-names></name><name><surname>Kamada-Nobusada</surname><given-names>T.</given-names></name><name><surname>Hayashi</surname><given-names>H.</given-names></name><name><surname>Sakakibara</surname><given-names>H.</given-names></name><source>J. Exp. Bot.</source><volume>59</volume><year>2008</year><fpage>75</fpage><lpage>83</lpage><pub-id pub-id-type="pmid">17872922</pub-id></element-citation></ref><ref id="R69"><label>69</label><element-citation publication-type="journal"><name><surname>Higuchi</surname><given-names>M.</given-names></name><name><surname>Kakimoto</surname><given-names>T.</given-names></name><name><surname>Mizuno</surname><given-names>T.</given-names></name><source>Plant Hormones: Methods and Protocols,</source><volume>495</volume><year>2009</year><fpage>101</fpage><lpage>109</lpage></element-citation></ref><ref id="R70"><label>70</label><element-citation publication-type="journal"><name><surname>Spíchal</surname><given-names>L.</given-names></name><source>Plant Kinases: Methods and Protocols. Methods in Molecular Biology.
Springer Science+Business Media.</source><volume>779</volume><year>2011</year><fpage>139</fpage><lpage>147</lpage></element-citation></ref><ref id="R71"><label>71</label><element-citation publication-type="journal"><name><surname>Romanov</surname><given-names>G.A.</given-names></name><name><surname>Spíchal</surname><given-names>L.</given-names></name><name><surname>Lomin</surname><given-names>S.N.</given-names></name><name><surname>Strnad</surname><given-names>M.</given-names></name><name><surname>Schmülling</surname><given-names>T.</given-names></name><source>Anal. Biochem.</source><volume>347</volume><year>2005</year><fpage>129</fpage><lpage>134</lpage><pub-id pub-id-type="pmid">16246292</pub-id></element-citation></ref><ref id="R72"><label>72</label><element-citation publication-type="journal"><name><surname>Romanov</surname><given-names>G.A.</given-names></name><name><surname>Lomin</surname><given-names>S.N.</given-names></name><source>Plant Hormones: Methods and Protocols,</source><volume>495</volume><year>2009</year><fpage>111</fpage><lpage>120</lpage></element-citation></ref><ref id="R73"><label>73</label><element-citation publication-type="journal"><name><surname>Takei</surname><given-names>K.</given-names></name><name><surname>Ueda</surname><given-names>N.</given-names></name><name><surname>Aoki</surname><given-names>K.</given-names></name><name><surname>Kuromori</surname><given-names>T.</given-names></name><name><surname>Hirayama</surname><given-names>T.</given-names></name><name><surname>Shinozaki</surname><given-names>K.</given-names></name><name><surname>Yamaya</surname><given-names>T.</given-names></name><name><surname>Sakakibara</surname><given-names>H.</given-names></name><source>Plant Cell Physiol.</source><volume>45</volume><year>2004</year><fpage>1053</fpage><lpage>1062</lpage><pub-id pub-id-type="pmid">15356331</pub-id></element-citation></ref><ref id="R74"><label>74</label><element-citation publication-type="journal"><name><surname>Lomin</surname><given-names>S.N.</given-names></name><name><surname>Romanov</surname><given-names>G.A.</given-names></name><source>Russian J. Plant Physiol.</source><volume>55</volume><year>2008</year><fpage>244</fpage><lpage>258</lpage></element-citation></ref><ref id="R75"><label>75</label><element-citation publication-type="journal"><name><surname>Stolz</surname><given-names>A.</given-names></name><name><surname>Riefler</surname><given-names>M.</given-names></name><name><surname>Lomin</surname><given-names>S.N.</given-names></name><name><surname>Achazi</surname><given-names>K.</given-names></name><name><surname>Romanov</surname><given-names>G.A.</given-names></name><name><surname>Schmülling</surname><given-names>T.</given-names></name><source>Plant J.</source><volume>67</volume><year>2011</year><fpage>157</fpage><lpage>168</lpage><pub-id pub-id-type="pmid">21426428</pub-id></element-citation></ref><ref id="R76"><label>76</label><element-citation publication-type="journal"><name><surname>Yonekura-Sakakibara</surname><given-names>K.</given-names></name><name><surname>Kojima</surname><given-names>M.</given-names></name><name><surname>Yamaya</surname><given-names>T.</given-names></name><name><surname>Sakakibara</surname><given-names>H.</given-names></name><source>Plant Physiol.</source><volume>134</volume><year>2004</year><fpage>1654</fpage><lpage>1661</lpage><pub-id pub-id-type="pmid">15064375</pub-id></element-citation></ref><ref id="R77"><label>77</label><element-citation publication-type="journal"><name><surname>Veach</surname><given-names>Y.K.</given-names></name><name><surname>Martin</surname><given-names>R.C.</given-names></name><name><surname>Mok</surname><given-names>D.W.S.</given-names></name><name><surname>Malbeck</surname><given-names>J.</given-names></name><name><surname>Vankova</surname><given-names>R.</given-names></name><name><surname>Mok</surname><given-names>M.C.</given-names></name><source>Plant Physiol.</source><volume>131</volume><year>2003</year><fpage>1374</fpage><lpage>1380</lpage><pub-id pub-id-type="pmid">12644686</pub-id></element-citation></ref><ref id="R78"><label>78</label><element-citation publication-type="journal"><name><surname>Vyroubalová</surname><given-names>S.</given-names></name><name><surname>Václaviková</surname><given-names>K.</given-names></name><name><surname>Turečková</surname><given-names>V.</given-names></name><name><surname>Novák</surname><given-names>O.</given-names></name><name><surname>Šmehilová</surname><given-names>M.</given-names></name><name><surname>Hluska</surname><given-names>T.</given-names></name><name><surname>Ohnoutková</surname><given-names>L.</given-names></name><name><surname>Frébort</surname><given-names>I.</given-names></name><name><surname>Galuszka</surname><given-names>P.</given-names></name><source>Plant Physiol.</source><volume>151</volume><year>2009</year><fpage>433</fpage><lpage>447</lpage><pub-id pub-id-type="pmid">19641027</pub-id></element-citation></ref><ref id="R79"><label>79</label><element-citation publication-type="journal"><name><surname>Heyl</surname><given-names>A.</given-names></name><name><surname>Riefler</surname><given-names>M.</given-names></name><name><surname>Romanov</surname><given-names>G.A.</given-names></name><name><surname>Schmülling</surname><given-names>T.</given-names></name><source>Eur. J. Cell Biol.</source><volume>91</volume><year>2012</year><fpage>246</fpage><lpage>256</lpage><pub-id pub-id-type="pmid">21561682</pub-id></element-citation></ref><ref id="R80"><label>80</label><element-citation publication-type="journal"><name><surname>Scheres</surname><given-names>B.</given-names></name><name><surname>Di Laurenzio</surname><given-names>L.</given-names></name><name><surname>Willemsen</surname><given-names>V.</given-names></name><name><surname>Hauser</surname><given-names>M.T.</given-names></name><name><surname>Janmaat</surname><given-names>K.</given-names></name><name><surname>Weisbeek</surname><given-names>P.</given-names></name><name><surname>Benfey</surname><given-names>P.N.</given-names></name><source>Development.</source><volume>121</volume><year>1995</year><fpage>53</fpage><lpage>62</lpage></element-citation></ref><ref id="R81"><label>81</label><element-citation publication-type="journal"><name><surname>De Leon</surname><given-names>B.G.</given-names></name><name><surname>Franco Zorrilla</surname><given-names>J.M.</given-names></name><name><surname>Rubio</surname><given-names>V.</given-names></name><name><surname>Dahiya</surname><given-names>P.</given-names></name><name><surname>Paz-Ares</surname><given-names>J.</given-names></name><source>Plant J.</source><volume>38</volume><year>2004</year><fpage>70</fpage><lpage>79</lpage><pub-id pub-id-type="pmid">15053761</pub-id></element-citation></ref><ref id="R82"><label>82</label><element-citation publication-type="journal"><name><surname>Kuroha</surname><given-names>T.</given-names></name><name><surname>Ueguchi</surname><given-names>C.</given-names></name><name><surname>Sakakibara</surname><given-names>H.</given-names></name><name><surname>Satoh</surname><given-names>S.</given-names></name><source>Plant Cell Physiol.</source><volume>47</volume><year>2006</year><fpage>234</fpage><lpage>243</lpage><pub-id pub-id-type="pmid">16357038</pub-id></element-citation></ref><ref id="R83"><label>83</label><element-citation publication-type="journal"><name><surname>Stock</surname><given-names>A.M.</given-names></name><name><surname>Robinson</surname><given-names>V.L.</given-names></name><name><surname>Goudreau</surname><given-names>P.N.</given-names></name><source>Annu. Rev. Biochem.</source><volume>69</volume><year>2000</year><fpage>183</fpage><lpage>215</lpage><pub-id pub-id-type="pmid">10966457</pub-id></element-citation></ref><ref id="R84"><label>84</label><element-citation publication-type="journal"><name><surname>Heyl</surname><given-names>A.</given-names></name><name><surname>Wulfetange</surname><given-names>K.</given-names></name><name><surname>Pils</surname><given-names>B.</given-names></name><name><surname>Nielsen</surname><given-names>N.</given-names></name><name><surname>Romanov</surname><given-names>G.A.</given-names></name><name><surname>Schmülling</surname><given-names>T.</given-names></name><source>BMC Evol. Biol.</source><year>2007</year></element-citation></ref><ref id="R85"><label>85</label><element-citation publication-type="journal"><name><surname>Franco-Zorrilla</surname><given-names>J.M.</given-names></name><name><surname>Martin</surname><given-names>A.C.</given-names></name><name><surname>Solano</surname><given-names>R.</given-names></name><name><surname>Paz-Ares</surname><given-names>J.</given-names></name><source>Plant J.</source><volume>32</volume><year>2002</year><fpage>353</fpage><lpage>360</lpage><pub-id pub-id-type="pmid">12410813</pub-id></element-citation></ref><ref id="R86"><label>86</label><element-citation publication-type="journal"><name><surname>Plet</surname><given-names>J.</given-names></name><name><surname>Wasson</surname><given-names>A.</given-names></name><name><surname>Ariel</surname><given-names>F.</given-names></name><name><surname>Le Signor</surname><given-names>C.</given-names></name><name><surname>Baker</surname><given-names>D.</given-names></name><name><surname>Mathesius</surname><given-names>U.</given-names></name><name><surname>Crespi</surname><given-names>M.</given-names></name><name><surname>Frugier</surname><given-names>F.</given-names></name><source>The Plant Journal.</source><volume>65</volume><year>2011</year><fpage>622</fpage><lpage>633</lpage><pub-id pub-id-type="pmid">21244535</pub-id></element-citation></ref><ref id="R87"><label>87</label><element-citation publication-type="journal"><name><surname>Pas</surname><given-names>J.</given-names></name><name><surname>von Grotthuss</surname><given-names>M.</given-names></name><name><surname>Wyrwicz</surname><given-names>L.S.</given-names></name><name><surname>Rychlewski</surname><given-names>L.</given-names></name><name><surname>Barciszewski</surname><given-names>J.</given-names></name><source>FEBS Letters.</source><volume>576</volume><year>2004</year><fpage>287</fpage><lpage>290</lpage><pub-id pub-id-type="pmid">15498549</pub-id></element-citation></ref><ref id="R88"><label>88</label><element-citation publication-type="journal"><name><surname>Wulfetange</surname><given-names>K.</given-names></name><name><surname>Saenger</surname><given-names>W.</given-names></name><name><surname>Schmülling</surname><given-names>T.</given-names></name><name><surname>Heyl</surname><given-names>A.</given-names></name><source>Mol. Biotechnol.</source><volume>47</volume><year>2011</year><fpage>211</fpage><lpage>219</lpage><pub-id pub-id-type="pmid">20886313</pub-id></element-citation></ref><ref id="R89"><label>89</label><element-citation publication-type="journal"><name><surname>Hothorn</surname><given-names>M.</given-names></name><name><surname>Dabi</surname><given-names>T.</given-names></name><name><surname>Chory</surname><given-names>J.</given-names></name><source>Nat. Chem. Biol.</source><volume>7</volume><year>2011</year><fpage>766</fpage><lpage>768</lpage><pub-id pub-id-type="pmid">21964459</pub-id></element-citation></ref><ref id="R90"><label>90</label><element-citation publication-type="journal"><name><surname>Müller-Dieckmann</surname><given-names>H.J.</given-names></name><name><surname>Grantz</surname><given-names>A.A.</given-names></name><name><surname>Kim</surname><given-names>S.H.</given-names></name><source>Structure.</source><volume>7</volume><year>1999</year><fpage>1547</fpage><lpage>1556</lpage><pub-id pub-id-type="pmid">10647185</pub-id></element-citation></ref><ref id="R91"><label>91</label><element-citation publication-type="journal"><name><surname>Pekárová</surname><given-names>B.</given-names></name><name><surname>Klumpler</surname><given-names>T.</given-names></name><name><surname>Třísková</surname><given-names>O.</given-names></name><name><surname>Janda</surname><given-names>L.</given-names></name><source>Plant J.</source><volume>67</volume><year>2011</year><fpage>827</fpage><lpage>839</lpage><pub-id pub-id-type="pmid">21569135</pub-id></element-citation></ref><ref id="R92"><label>92</label><element-citation publication-type="journal"><name><surname>Zhang</surname><given-names>Z.</given-names></name><name><surname>Hendrickson</surname><given-names>W.A.</given-names></name><source>J. Mol. Biol.</source><volume>400</volume><year>2010</year><fpage>335</fpage><lpage>353</lpage><pub-id pub-id-type="pmid">20435045</pub-id></element-citation></ref><ref id="R93"><label>93</label><element-citation publication-type="journal"><name><surname>Pils</surname><given-names>B.</given-names></name><name><surname>Heyl</surname><given-names>A.</given-names></name><source>Plant Physiol.</source><volume>151</volume><year>2009</year><fpage>782</fpage><lpage>791</lpage><pub-id pub-id-type="pmid">19675156</pub-id></element-citation></ref><ref id="R94"><label>94</label><element-citation publication-type="journal"><name><surname>Romanov</surname><given-names>G.A.</given-names></name><source>Russian J. Plant Physiol.</source><volume>49</volume><year>2002</year><fpage>552</fpage><lpage>560</lpage></element-citation></ref><ref id="R95"><label>95</label><element-citation publication-type="journal"><name><surname>Chow</surname><given-names>B.</given-names></name><name><surname>McCourt</surname><given-names>P.</given-names></name><source>Genes & Dev.</source><volume>20</volume><year>2006</year><fpage>1998</fpage><lpage>2008</lpage><pub-id pub-id-type="pmid">16882977</pub-id></element-citation></ref><ref id="R96"><label>96</label><element-citation publication-type="journal"><name><surname>Bishopp</surname><given-names>A.</given-names></name><name><surname>Mähönen</surname><given-names>A.P.</given-names></name><name><surname>Helariutta</surname><given-names>Y.</given-names></name><source>Development.</source><volume>133</volume><year>2006</year><fpage>1857</fpage><lpage>1869</lpage><pub-id pub-id-type="pmid">16651539</pub-id></element-citation></ref><ref id="R97"><label>97</label><element-citation publication-type="journal"><name><surname>Spartz</surname><given-names>A.K.</given-names></name><name><surname>Gray</surname><given-names>W.M.</given-names></name><source>Genes & Devel.</source><volume>22</volume><year>2008</year><fpage>2139</fpage><lpage>2148</lpage><pub-id pub-id-type="pmid">18708574</pub-id></element-citation></ref><ref id="R98"><label>98</label><element-citation publication-type="journal"><name><surname>Santner</surname><given-names>A.</given-names></name><name><surname>Calderon-Villalobos</surname><given-names>L.I.A.</given-names></name><name><surname>Estelle</surname><given-names>M.</given-names></name><source>Nat. Chem. Biol.</source><volume>5</volume><year>2009</year><fpage>301</fpage><lpage>307</lpage><pub-id pub-id-type="pmid">19377456</pub-id></element-citation></ref><ref id="R99"><label>99</label><element-citation publication-type="journal"><name><surname>Santner</surname><given-names>A.</given-names></name><name><surname>Estelle</surname><given-names>M.</given-names></name><source>Nature. V.</source><volume>2009</volume><year>2009</year><fpage>1071</fpage><lpage>1078</lpage></element-citation></ref><ref id="R100"><label>100</label><element-citation publication-type="journal"><name><surname>Jaillais</surname><given-names>Y.</given-names></name><name><surname>Chory</surname><given-names>J.</given-names></name><source>Nat. Struct. Mol. Biol.</source><volume>17</volume><year>2010</year><fpage>642</fpage><lpage>645</lpage><pub-id pub-id-type="pmid">20520656</pub-id></element-citation></ref><ref id="R101"><label>101</label><element-citation publication-type="journal"><name><surname>Kumari</surname><given-names>S.</given-names></name><name><surname>van der Hoorn</surname><given-names>R.A.L.</given-names></name><source>Curr. Opin. Plant Biol.</source><volume>14</volume><year>2011</year><fpage>480</fpage><lpage>488</lpage><pub-id pub-id-type="pmid">21803639</pub-id></element-citation></ref><ref id="R102"><label>102</label><element-citation publication-type="journal"><name><surname>Bleecker</surname><given-names>A.B.</given-names></name><source>Trends Plant Sci.</source><volume>4</volume><year>1999</year><fpage>269</fpage><lpage>274</lpage><pub-id pub-id-type="pmid">10407443</pub-id></element-citation></ref><ref id="R103"><label>103</label><element-citation publication-type="journal"><source>New York: Oxford Univ. Press,</source><year>1994</year></element-citation></ref><ref id="R104"><label>104</label><element-citation publication-type="journal"><name><surname>Danilenko</surname><given-names>N.G.</given-names></name><name><surname>Davidenko</surname><given-names>O.G.</given-names></name><source>Organelle Genome Worlds (in Russian). Minsk, Technalogia,</source><year>2003</year></element-citation></ref></ref-list></back></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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