NAD + -dependent Formate Dehydrogenase from Plants
Identifieur interne : 001347 ( Pmc/Corpus ); précédent : 001346; suivant : 001348NAD + -dependent Formate Dehydrogenase from Plants
Auteurs : A. A. Alekseeva ; S. S. Savin ; V. I. TishkovSource :
- Acta Naturae [ 2075-8251 ] ; 2011.
Abstract
NAD+-dependent formate dehydrogenase (FDH, EC 1.2.1.2) widely occurs in nature. FDH consists of two identical subunits and contains neither prosthetic groups nor metal ions. This type of FDH was found in different microorganisms (including pathogenic ones), such as bacteria, yeasts, fungi, and plants. As opposed to microbiological FDHs functioning in cytoplasm, plant FDHs localize in mitochondria. Formate dehydrogenase activity was first discovered as early as in 1921 in plant; however, until the past decade FDHs from plants had been considerably less studied than the enzymes from microorganisms. This review summarizes the recent results on studying the physiological role, properties, structure, and protein engineering of plant formate dehydrogenases.
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PubMed: 22649703
PubMed Central: 3347622
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PMC:3347622Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">NAD <sup>+</sup> -dependent Formate Dehydrogenase from Plants
</title><author><name sortKey="Alekseeva, A A" sort="Alekseeva, A A" uniqKey="Alekseeva A" first="A. A." last="Alekseeva">A. A. Alekseeva</name><affiliation><nlm:aff id="AF1">Chemistry Department, Lomonosov Moscow State University</nlm:aff></affiliation><affiliation><nlm:aff id="AF2">Innovations and High Technologies MSU Ltd</nlm:aff></affiliation><affiliation><nlm:aff id="AF3">Bach Institute of Biochemistry, Russian Academy of Sciences</nlm:aff></affiliation></author><author><name sortKey="Savin, S S" sort="Savin, S S" uniqKey="Savin S" first="S. S." last="Savin">S. S. Savin</name><affiliation><nlm:aff id="AF2">Innovations and High Technologies MSU Ltd</nlm:aff></affiliation><affiliation><nlm:aff id="AF3">Bach Institute of Biochemistry, Russian Academy of Sciences</nlm:aff></affiliation></author><author><name sortKey="Tishkov, V I" sort="Tishkov, V I" uniqKey="Tishkov V" first="V. I." last="Tishkov">V. I. Tishkov</name><affiliation><nlm:aff id="AF1">Chemistry Department, Lomonosov Moscow State University</nlm:aff></affiliation><affiliation><nlm:aff id="AF2">Innovations and High Technologies MSU Ltd</nlm:aff></affiliation><affiliation><nlm:aff id="AF3">Bach Institute of Biochemistry, Russian Academy of Sciences</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">22649703</idno><idno type="pmc">3347622</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3347622</idno><idno type="RBID">PMC:3347622</idno><date when="2011">2011</date><idno type="wicri:Area/Pmc/Corpus">001347</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">NAD <sup>+</sup> -dependent Formate Dehydrogenase from Plants
</title><author><name sortKey="Alekseeva, A A" sort="Alekseeva, A A" uniqKey="Alekseeva A" first="A. A." last="Alekseeva">A. A. Alekseeva</name><affiliation><nlm:aff id="AF1">Chemistry Department, Lomonosov Moscow State University</nlm:aff></affiliation><affiliation><nlm:aff id="AF2">Innovations and High Technologies MSU Ltd</nlm:aff></affiliation><affiliation><nlm:aff id="AF3">Bach Institute of Biochemistry, Russian Academy of Sciences</nlm:aff></affiliation></author><author><name sortKey="Savin, S S" sort="Savin, S S" uniqKey="Savin S" first="S. S." last="Savin">S. S. Savin</name><affiliation><nlm:aff id="AF2">Innovations and High Technologies MSU Ltd</nlm:aff></affiliation><affiliation><nlm:aff id="AF3">Bach Institute of Biochemistry, Russian Academy of Sciences</nlm:aff></affiliation></author><author><name sortKey="Tishkov, V I" sort="Tishkov, V I" uniqKey="Tishkov V" first="V. I." last="Tishkov">V. I. Tishkov</name><affiliation><nlm:aff id="AF1">Chemistry Department, Lomonosov Moscow State University</nlm:aff></affiliation><affiliation><nlm:aff id="AF2">Innovations and High Technologies MSU Ltd</nlm:aff></affiliation><affiliation><nlm:aff id="AF3">Bach Institute of Biochemistry, Russian Academy of Sciences</nlm:aff></affiliation></author></analytic><series><title level="j">Acta Naturae</title><idno type="ISSN">2075-8251</idno><imprint><date when="2011">2011</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>NAD<sup>+</sup>-dependent formate dehydrogenase (FDH, EC 1.2.1.2) widely occurs
in nature. FDH consists of two identical subunits and contains neither
prosthetic groups nor metal ions. This type of FDH was found in different
microorganisms (including pathogenic ones), such as bacteria, yeasts, fungi, and
plants. As opposed to microbiological FDHs functioning in cytoplasm, plant FDHs
localize in mitochondria. Formate dehydrogenase activity was first discovered as
early as in 1921 in plant; however, until the past decade FDHs from plants had
been considerably less studied than the enzymes from microorganisms. This review
summarizes the recent results on studying the physiological role, properties,
structure, and protein engineering of plant formate dehydrogenases.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Rodionov, Yu V" uniqKey="Rodionov Y">Yu.V. Rodionov</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Ferry, J G" uniqKey="Ferry J">J.G. Ferry</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Vinals, C" uniqKey="Vinals C">C. Vinals</name></author><author><name sortKey="Depiereux, E" uniqKey="Depiereux E">E. Depiereux</name></author><author><name sortKey="Feytmans, E" uniqKey="Feytmans E">E. Feytmans</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Tishkov, V I" uniqKey="Tishkov V">V.I. Tishkov</name></author><author><name sortKey="Galkin, A G" uniqKey="Galkin A">A.G. Galkin</name></author><author><name sortKey="Egorov, A M" uniqKey="Egorov A">A.M. Egorov</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Tishkov, V I" uniqKey="Tishkov V">V.I. Tishkov</name></author><author><name sortKey="Popov, V O" uniqKey="Popov V">V.O. Popov</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Tishkov, V I" uniqKey="Tishkov V">V.I. Tishkov</name></author><author><name sortKey="Popov, V O" uniqKey="Popov V">V.O. Popov</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hourton Cabassa, C" uniqKey="Hourton Cabassa C">C. Hourton-Cabassa</name></author><author><name sortKey="Ambard Bretteville, F" uniqKey="Ambard Bretteville F">F. Ambard-Bretteville</name></author><author><name sortKey="Moreau, F" uniqKey="Moreau F">F. Moreau</name></author><author><name sortKey="Davy De Virville, J" uniqKey="Davy De Virville J">J. Davy de Virville</name></author><author><name sortKey="Remy, R" uniqKey="Remy R">R. Remy</name></author><author><name sortKey="Colas Des Francs Small, C" uniqKey="Colas Des Francs Small C">C. Colas des Francs-Small</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Suzuki, K" uniqKey="Suzuki K">K. Suzuki</name></author><author><name sortKey="Itai, R" uniqKey="Itai R">R. Itai</name></author><author><name sortKey="Suzuki, K" uniqKey="Suzuki K">K. Suzuki</name></author><author><name sortKey="Nakanishi, H" uniqKey="Nakanishi H">H. Nakanishi</name></author><author><name sortKey="Nishizawa, N K" uniqKey="Nishizawa N">N.-K. Nishizawa</name></author><author><name sortKey="Yoshimura, E" uniqKey="Yoshimura E">E. Yoshimura</name></author><author><name sortKey="Mori, S" uniqKey="Mori S">S. Mori</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Thompson, P" uniqKey="Thompson P">P. Thompson</name></author><author><name sortKey="Bowsher, C G" uniqKey="Bowsher C">C.G. Bowsher</name></author><author><name sortKey="Tobin, A K" uniqKey="Tobin A">A.K. Tobin</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Andreadeli, A" uniqKey="Andreadeli A">A. Andreadeli</name></author><author><name sortKey="Flemetakis, E" uniqKey="Flemetakis E">E. Flemetakis</name></author><author><name sortKey="Axarli, I" uniqKey="Axarli I">I. Axarli</name></author><author><name sortKey="Dimou, M" uniqKey="Dimou M">M. Dimou</name></author><author><name sortKey="Udvardi, M K" uniqKey="Udvardi M">M.K. Udvardi</name></author><author><name sortKey="Katinakis, P" uniqKey="Katinakis P">P. Katinakis</name></author><author><name sortKey="Labrou, N E" uniqKey="Labrou N">N.E. Labrou</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="David, P" uniqKey="David P">P. David</name></author><author><name sortKey="Colas Des Francs Small, C" uniqKey="Colas Des Francs Small C">C. Colas des Francs-Small</name></author><author><name sortKey="Sevignac, M" uniqKey="Sevignac M">M. Sevignac</name></author><author><name sortKey="Thareau, V" uniqKey="Thareau V">V. Thareau</name></author><author><name sortKey="Macadre, C" uniqKey="Macadre C">C. Macadre</name></author><author><name sortKey="Langin, T" uniqKey="Langin T">T. Langin</name></author><author><name sortKey="Geffroy, V" uniqKey="Geffroy V">V. Geffroy</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Thunberg, T" uniqKey="Thunberg T">T. Thunberg</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Davison, D C" uniqKey="Davison D">D.C. Davison</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Davies, D D" uniqKey="Davies D">D.D. Davies</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Mazelis, M" uniqKey="Mazelis M">M. Mazelis</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Halliwell, B" uniqKey="Halliwell B">B. Halliwell</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Jansch, L" uniqKey="Jansch L">L. Jansch</name></author><author><name sortKey="Kruft, V" uniqKey="Kruft V">V. Kruft</name></author><author><name sortKey="Schmitz, U K" uniqKey="Schmitz U">U.K. Schmitz</name></author><author><name sortKey="Braun, H P" uniqKey="Braun H">H.-P. Braun</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Oliver, D J" uniqKey="Oliver D">D.J. Oliver</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hanson, A D" uniqKey="Hanson A">A.D. Hanson</name></author><author><name sortKey="Nelsen, C E" uniqKey="Nelsen C">C.E. Nelsen</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Colas Des Francs Small, C" uniqKey="Colas Des Francs Small C">C. Colas des Francs-Small</name></author><author><name sortKey="Ambard Bretteville, F" uniqKey="Ambard Bretteville F">F. Ambard-Bretteville</name></author><author><name sortKey="Darpas, A" uniqKey="Darpas A">A. Darpas</name></author><author><name sortKey="Sallantin, M" uniqKey="Sallantin M">M. Sallantin</name></author><author><name sortKey="Huet, J C" uniqKey="Huet J">J.-C. Huet</name></author><author><name sortKey="Pernollet, J C" uniqKey="Pernollet J">J.-C. Pernollet</name></author><author><name sortKey="Remy, R" uniqKey="Remy R">R. Remy</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Colas Des Francs Small, C" uniqKey="Colas Des Francs Small C">C. Colas des Francs-Small</name></author><author><name sortKey="Ambard Bretteville, F" uniqKey="Ambard Bretteville F">F. Ambard-Bretteville</name></author><author><name sortKey="Small, I D" uniqKey="Small I">I.D. Small</name></author><author><name sortKey="Remy, R" uniqKey="Remy R">R. Remy</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Herbik, A" uniqKey="Herbik A">A. Herbik</name></author><author><name sortKey="Giritch, A" uniqKey="Giritch A">A. Giritch</name></author><author><name sortKey="Horstmann, C" uniqKey="Horstmann C">C. Horstmann</name></author><author><name sortKey="Becker, R" uniqKey="Becker R">R. Becker</name></author><author><name sortKey="Balzer, H J" uniqKey="Balzer H">H.-J. Balzer</name></author><author><name sortKey="Baumlein, H" uniqKey="Baumlein H">H. Baumlein</name></author><author><name sortKey="Stephan, U W" uniqKey="Stephan U">U.W. Stephan</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Dubos, C" uniqKey="Dubos C">C. Dubos</name></author><author><name sortKey="Plomion, C" uniqKey="Plomion C">C. Plomion</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Minami, A" uniqKey="Minami A">A. Minami</name></author><author><name sortKey="Fujikawa, S" uniqKey="Fujikawa S">S. Fujikawa</name></author><author><name sortKey="Takezawa, D" uniqKey="Takezawa D">D. Takezawa</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Yin, L" uniqKey="Yin L">L. Yin</name></author><author><name sortKey="Lan, Y" uniqKey="Lan Y">Y. Lan</name></author><author><name sortKey="Zhu, L" uniqKey="Zhu L">L. Zhu</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Fukusaki, E" uniqKey="Fukusaki E">E. Fukusaki</name></author><author><name sortKey="Ikeda, T" uniqKey="Ikeda T">T. Ikeda</name></author><author><name sortKey="Shiraishi, T" uniqKey="Shiraishi T">T. Shiraishi</name></author><author><name sortKey="Nishikawa, T" uniqKey="Nishikawa T">T. Nishikawa</name></author><author><name sortKey="Kobayashi, A" uniqKey="Kobayashi A">A. Kobayashi</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Olson, B J" uniqKey="Olson B">B.J. Olson</name></author><author><name sortKey="Skavdahl, M" uniqKey="Skavdahl M">M. Skavdahl</name></author><author><name sortKey="Ramberg, H" uniqKey="Ramberg H">H. Ramberg</name></author><author><name sortKey="Osterman, J C" uniqKey="Osterman J">J.C. Osterman</name></author><author><name sortKey="Markwell, J" uniqKey="Markwell J">J. Markwell</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Herman, P L" uniqKey="Herman P">P.L. Herman</name></author><author><name sortKey="Ramberg, H" uniqKey="Ramberg H">H. Ramberg</name></author><author><name sortKey="Baack, R D" uniqKey="Baack R">R.D. Baack</name></author><author><name sortKey="Markwell, J" uniqKey="Markwell J">J. Markwell</name></author><author><name sortKey="Osterman, J C" uniqKey="Osterman J">J.C. Osterman</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Ambard Bretteville, F" uniqKey="Ambard Bretteville F">F. Ambard-Bretteville</name></author><author><name sortKey="Sorin, C" uniqKey="Sorin C">C. Sorin</name></author><author><name sortKey="Rebeille, F" uniqKey="Rebeille F">F. Rebeille</name></author><author><name sortKey="Hourton Cabassa, C" uniqKey="Hourton Cabassa C">C. Hourton-Cabassa</name></author><author><name sortKey="Colas Des Francs Small, C" uniqKey="Colas Des Francs Small C">C. Colas des Francs-Small</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Igamberdiev, A U" uniqKey="Igamberdiev A">A.U. Igamberdiev</name></author><author><name sortKey="Bykova, N V" uniqKey="Bykova N">N.V. Bykova</name></author><author><name sortKey="Kleczkowski, L A" uniqKey="Kleczkowski L">L.A. Kleczkowski</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Li, R" uniqKey="Li R">R. Li</name></author><author><name sortKey="Moore, M" uniqKey="Moore M">M. Moore</name></author><author><name sortKey="King, J" uniqKey="King J">J. King</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Perales, M" uniqKey="Perales M">M. Perales</name></author><author><name sortKey="Eubel, H" uniqKey="Eubel H">H. Eubel</name></author><author><name sortKey="Heinemeyer, J" uniqKey="Heinemeyer J">J. Heinemeyer</name></author><author><name sortKey="Colaneri, A" uniqKey="Colaneri A">A. Colaneri</name></author><author><name sortKey="Zabaleta, E" uniqKey="Zabaleta E">E. Zabaleta</name></author><author><name sortKey="Braun, H P" uniqKey="Braun H">H.P. Braun</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Bykova, N V" uniqKey="Bykova N">N.V. Bykova</name></author><author><name sortKey="Egsgaard, H" uniqKey="Egsgaard H">H. Egsgaard</name></author><author><name sortKey="Miller, I M" uniqKey="Miller I">I.M. Miller</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Bykova, N V" uniqKey="Bykova N">N.V. Bykova</name></author><author><name sortKey="Stensballe, A" uniqKey="Stensballe A">A. Stensballe</name></author><author><name sortKey="Egsgaard, H" uniqKey="Egsgaard H">H. Egsgaard</name></author><author><name sortKey="Jensen, O N" uniqKey="Jensen O">O.N. Jensen</name></author><author><name sortKey="Moller, I M" uniqKey="Moller I">I.M. Moller</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Kruger, A" uniqKey="Kruger A">A. Kruger</name></author><author><name sortKey="Peskan Berghofer, T" uniqKey="Peskan Berghofer T">T. Peskan-Berghofer</name></author><author><name sortKey="Frettinger, P" uniqKey="Frettinger P">P. Frettinger</name></author><author><name sortKey="Herrmann, S" uniqKey="Herrmann S">S. Herrmann</name></author><author><name sortKey="Buscot, F" uniqKey="Buscot F">F. Buscot</name></author><author><name sortKey="Oelmuller, R" uniqKey="Oelmuller R">R. Oelmuller</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Bruggmann, R" uniqKey="Bruggmann R">R. Bruggmann</name></author><author><name sortKey="Abderhalden, O" uniqKey="Abderhalden O">O. Abderhalden</name></author><author><name sortKey="Reymond, P" uniqKey="Reymond P">P. Reymond</name></author><author><name sortKey="Dudler, R" uniqKey="Dudler R">R. Dudler</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Giri, A P" uniqKey="Giri A">A.P. Giri</name></author><author><name sortKey="Wunsche, H" uniqKey="Wunsche H">H. Wunsche</name></author><author><name sortKey="Mitra, S" uniqKey="Mitra S">S. Mitra</name></author><author><name sortKey="Zavala, J A" uniqKey="Zavala J">J.A. Zavala</name></author><author><name sortKey="Muck, A" uniqKey="Muck A">A. Muck</name></author><author><name sortKey="Svatos, A" uniqKey="Svatos A">A. Svatos</name></author><author><name sortKey="Baldwin, I T" uniqKey="Baldwin I">I.T. Baldwin</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Umezawa, T" uniqKey="Umezawa T">T. Umezawa</name></author><author><name sortKey="Sakurai, T" uniqKey="Sakurai T">T. Sakurai</name></author><author><name sortKey="Totoki, Y" uniqKey="Totoki Y">Y. Totoki</name></author><author><name sortKey="Toyoda, A" uniqKey="Toyoda A">A. Toyoda</name></author><author><name sortKey="Seki, M" uniqKey="Seki M">M. Seki</name></author><author><name sortKey="Ishiwata, A" uniqKey="Ishiwata A">A. Ishiwata</name></author><author><name sortKey="Akiyama, K" uniqKey="Akiyama K">K. Akiyama</name></author><author><name sortKey="Kurotani, A" uniqKey="Kurotani A">A. Kurotani</name></author><author><name sortKey="Yoshida, T" uniqKey="Yoshida T">T. Yoshida</name></author><author><name sortKey="Mochida, K" uniqKey="Mochida K">K. Mochida</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Kikuchi, S" uniqKey="Kikuchi S">S. Kikuchi</name></author><author><name sortKey="Satoh, K" uniqKey="Satoh K">K. Satoh</name></author><author><name sortKey="Nagata, T" uniqKey="Nagata T">T. Nagata</name></author><author><name sortKey="Kawagashira, N" uniqKey="Kawagashira N">N. Kawagashira</name></author><author><name sortKey="Doi, K" uniqKey="Doi K">K. Doi</name></author><author><name sortKey="Kishimoto, N" uniqKey="Kishimoto N">N. Kishimoto</name></author><author><name sortKey="Yazaki, J" uniqKey="Yazaki J">J. Yazaki</name></author><author><name sortKey="Ishikawa, M" uniqKey="Ishikawa M">M. Ishikawa</name></author><author><name sortKey="Yamada, H" uniqKey="Yamada H">H. Yamada</name></author><author><name sortKey="Ooka, H" uniqKey="Ooka H">H. Ooka</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Liu, X" uniqKey="Liu X">X. Liu</name></author><author><name sortKey="Lu, T" uniqKey="Lu T">T. Lu</name></author><author><name sortKey="Yu, S" uniqKey="Yu S">S. Yu</name></author><author><name sortKey="Li, Y" uniqKey="Li Y">Y. Li</name></author><author><name sortKey="Huang, Y" uniqKey="Huang Y">Y. Huang</name></author><author><name sortKey="Huang, T" uniqKey="Huang T">T. Huang</name></author><author><name sortKey="Zhang, L" uniqKey="Zhang L">L. Zhang</name></author><author><name sortKey="Zhu, J" uniqKey="Zhu J">J. Zhu</name></author><author><name sortKey="Zhao, Q" uniqKey="Zhao Q">Q. Zhao</name></author><author><name sortKey="Fan, D" uniqKey="Fan D">D. Fan</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Shiraishi, T" uniqKey="Shiraishi T">T. Shiraishi</name></author><author><name sortKey="Fukusaki, E" uniqKey="Fukusaki E">E. Fukusaki</name></author><author><name sortKey="Kobayashi, A" uniqKey="Kobayashi A">A. Kobayashi</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="David, P" uniqKey="David P">P. David</name></author><author><name sortKey="Chen, N W G" uniqKey="Chen N">N.W.G. Chen</name></author><author><name sortKey="Pedrosa Harand, A" uniqKey="Pedrosa Harand A">A. Pedrosa-Harand</name></author><author><name sortKey="Thareau, V" uniqKey="Thareau V">V. Thareau</name></author><author><name sortKey="Sevignac, M" uniqKey="Sevignac M">M. Sevignac</name></author><author><name sortKey="Cannon, S B" uniqKey="Cannon S">S.B. Cannon</name></author><author><name sortKey="Debouck, D" uniqKey="Debouck D">D. Debouck</name></author><author><name sortKey="Langin, T" uniqKey="Langin T">T. Langin</name></author><author><name sortKey="Geffroy, V" uniqKey="Geffroy V">V. Geffroy</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Rensing, S A" uniqKey="Rensing S">S.A. Rensing</name></author><author><name sortKey="Lang, D" uniqKey="Lang D">D. Lang</name></author><author><name sortKey="Zimmer, A D" uniqKey="Zimmer A">A.D. Zimmer</name></author><author><name sortKey="Terry, A" uniqKey="Terry A">A. Terry</name></author><author><name sortKey="Salamov, A" uniqKey="Salamov A">A. Salamov</name></author><author><name sortKey="Shapiro, H" uniqKey="Shapiro H">H. Shapiro</name></author><author><name sortKey="Nishiyama, T" uniqKey="Nishiyama T">T. Nishiyama</name></author><author><name sortKey="Perroud, P F" uniqKey="Perroud P">P.-F. Perroud</name></author><author><name sortKey="Lindquist, E A" uniqKey="Lindquist E">E.A. Lindquist</name></author><author><name sortKey="Kamisugi, Y" uniqKey="Kamisugi Y">Y. Kamisugi</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Ralph, S G" uniqKey="Ralph S">S.G. Ralph</name></author><author><name sortKey="Chun, H J" uniqKey="Chun H">H.J. Chun</name></author><author><name sortKey="Kolosova, N" uniqKey="Kolosova N">N. Kolosova</name></author><author><name sortKey="Cooper, D" uniqKey="Cooper D">D. Cooper</name></author><author><name sortKey="Oddy, C" uniqKey="Oddy C">C. Oddy</name></author><author><name sortKey="Ritland, C E" uniqKey="Ritland C">C.E. Ritland</name></author><author><name sortKey="Kirkpatrick, R" uniqKey="Kirkpatrick R">R. Kirkpatrick</name></author><author><name sortKey="Moore, R" uniqKey="Moore R">R. Moore</name></author><author><name sortKey="Barber, S" uniqKey="Barber S">S. Barber</name></author><author><name sortKey="Holt, R A" uniqKey="Holt R">R.A. Holt</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Tuskan, G A" uniqKey="Tuskan G">G.A. Tuskan</name></author><author><name sortKey="Difazio, S" uniqKey="Difazio S">S. Difazio</name></author><author><name sortKey="Jansson, S" uniqKey="Jansson S">S. Jansson</name></author><author><name sortKey="Bohlmann, J" uniqKey="Bohlmann J">J. Bohlmann</name></author><author><name sortKey="Grigoriev, I" uniqKey="Grigoriev I">I. Grigoriev</name></author><author><name sortKey="Hellsten, U" uniqKey="Hellsten U">U. Hellsten</name></author><author><name sortKey="Putnam, N" uniqKey="Putnam N">N. Putnam</name></author><author><name sortKey="Ralph, S" uniqKey="Ralph S">S. Ralph</name></author><author><name sortKey="Rombauts, S" uniqKey="Rombauts S">S. Rombauts</name></author><author><name sortKey="Salamov, A" uniqKey="Salamov A">A. Salamov</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Paterson, A H" uniqKey="Paterson A">A.H. Paterson</name></author><author><name sortKey="Bowers, J E" uniqKey="Bowers J">J.E. Bowers</name></author><author><name sortKey="Bruggmann, R" uniqKey="Bruggmann R">R. Bruggmann</name></author><author><name sortKey="Dubchak, I" uniqKey="Dubchak I">I. Dubchak</name></author><author><name sortKey="Grimwood, J" uniqKey="Grimwood J">J. Grimwood</name></author><author><name sortKey="Gundlach, H" uniqKey="Gundlach H">H. Gundlach</name></author><author><name sortKey="Haberer, G" uniqKey="Haberer G">G. Haberer</name></author><author><name sortKey="Hellsten, U" uniqKey="Hellsten U">U. Hellsten</name></author><author><name sortKey="Mitros, T" uniqKey="Mitros T">T. Mitros</name></author><author><name sortKey="Poliakov, A" uniqKey="Poliakov A">A. Poliakov</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Kawaura, K" uniqKey="Kawaura K">K. Kawaura</name></author><author><name sortKey="Mochida, K" uniqKey="Mochida K">K. Mochida</name></author><author><name sortKey="Enju, A" uniqKey="Enju A">A. Enju</name></author><author><name sortKey="Totoki, Y" uniqKey="Totoki Y">Y. Totoki</name></author><author><name sortKey="Toyoda, A" uniqKey="Toyoda A">A. Toyoda</name></author><author><name sortKey="Sakaki, Y" uniqKey="Sakaki Y">Y. Sakaki</name></author><author><name sortKey="Kai, C" uniqKey="Kai C">C. Kai</name></author><author><name sortKey="Kawai, J" uniqKey="Kawai J">J. Kawai</name></author><author><name sortKey="Hayashizaki, Y" uniqKey="Hayashizaki Y">Y. Hayashizaki</name></author><author><name sortKey="Seki, M" uniqKey="Seki M">M. Seki</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Alexandrov, N N" uniqKey="Alexandrov N">N.N. Alexandrov</name></author><author><name sortKey="Brover, V V" uniqKey="Brover V">V.V. Brover</name></author><author><name sortKey="Freidin, S" uniqKey="Freidin S">S. Freidin</name></author><author><name sortKey="Troukhan, M E" uniqKey="Troukhan M">M.E. Troukhan</name></author><author><name sortKey="Tatarinova, T V" uniqKey="Tatarinova T">T.V. Tatarinova</name></author><author><name sortKey="Zhang, H" uniqKey="Zhang H">H. Zhang</name></author><author><name sortKey="Swaller, T J" uniqKey="Swaller T">T.J. Swaller</name></author><author><name sortKey="Lu, Y P" uniqKey="Lu Y">Y.P. Lu</name></author><author><name sortKey="Bouck, J" uniqKey="Bouck J">J. Bouck</name></author><author><name sortKey="Flavell, R B" uniqKey="Flavell R">R.B. Flavell</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hwang, L" uniqKey="Hwang L">L. Hwang</name></author><author><name sortKey="Hocking Murray, D" uniqKey="Hocking Murray D">D. Hocking-Murray</name></author><author><name sortKey="Bahrami, A K" uniqKey="Bahrami A">A.K. Bahrami</name></author><author><name sortKey="Andersson, M" uniqKey="Andersson M">M. Andersson</name></author><author><name sortKey="Rine, J" uniqKey="Rine J">J. Rine</name></author><author><name sortKey="Sil, A" uniqKey="Sil A">A. Sil</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Tishkov, V I" uniqKey="Tishkov V">V.I. Tishkov</name></author><author><name sortKey="Galkin, A G" uniqKey="Galkin A">A.G. Galkin</name></author><author><name sortKey="Egorov, A M" uniqKey="Egorov A">A.M. Egorov</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hatrongjit, R" uniqKey="Hatrongjit R">R. Hatrongjit</name></author><author><name sortKey="Packdibamrung, K" uniqKey="Packdibamrung K">K. Packdibamrung</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Barnett, M J" uniqKey="Barnett M">M.J. Barnett</name></author><author><name sortKey="Fisher, R F" uniqKey="Fisher R">R.F. Fisher</name></author><author><name sortKey="Jones, T" uniqKey="Jones T">T. Jones</name></author><author><name sortKey="Komp, C" uniqKey="Komp C">C. Komp</name></author><author><name sortKey="Abola, A P" uniqKey="Abola A">A.P. Abola</name></author><author><name sortKey="Barloy Hubler, F" uniqKey="Barloy Hubler F">F. Barloy-Hubler</name></author><author><name sortKey="Bowser, L" uniqKey="Bowser L">L. Bowser</name></author><author><name sortKey="Capela, D" uniqKey="Capela D">D. Capela</name></author><author><name sortKey="Galibert, F" uniqKey="Galibert F">F. Galibert</name></author><author><name sortKey="Gouzyet, J" uniqKey="Gouzyet J">J. Gouzyet</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Ambard Bretteville, F" uniqKey="Ambard Bretteville F">F. Ambard-Bretteville</name></author><author><name sortKey="Small, I" uniqKey="Small I">I. Small</name></author><author><name sortKey="Grandjean, O" uniqKey="Grandjean O">O. Grandjean</name></author><author><name sortKey="Colas Des Francs Small, C" uniqKey="Colas Des Francs Small C">C. Colas des Francs-Small</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Weerasinghe, P A" uniqKey="Weerasinghe P">P.A. Weerasinghe</name></author><author><name sortKey="Van Holm, L H J" uniqKey="Van Holm L">L.H.J. van Holm</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Colic, S" uniqKey="Colic S">S. Colic</name></author><author><name sortKey="Milatovic, D" uniqKey="Milatovic D">D. Milatovic</name></author><author><name sortKey="Nikolic, D" uniqKey="Nikolic D">D. Nikolic</name></author><author><name sortKey="Zec, G" uniqKey="Zec G">G. Zec</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Colich, S" uniqKey="Colich S">S. Colich</name></author><author><name sortKey="Milatovich, D" uniqKey="Milatovich D">D. Milatovich</name></author><author><name sortKey="Nikolich, D" uniqKey="Nikolich D">D. Nikolich</name></author><author><name sortKey="Zec, G" uniqKey="Zec G">G. Zec</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Farinelli, M P" uniqKey="Farinelli M">M.P. Farinelli</name></author><author><name sortKey="Fry, D W" uniqKey="Fry D">D.W. Fry</name></author><author><name sortKey="Richardson, K E" uniqKey="Richardson K">K.E. Richardson</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Sadykhov, E G" uniqKey="Sadykhov E">E.G. Sadykhov</name></author><author><name sortKey="Serov, A E" uniqKey="Serov A">A.E. Serov</name></author><author><name sortKey="Yasnyi, I E" uniqKey="Yasnyi I">I.E. Yasnyi</name></author><author><name sortKey="Petrov, A S" uniqKey="Petrov A">A.S. Petrov</name></author><author><name sortKey="Tishkov, V I" uniqKey="Tishkov V">V.I. Tishkov</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Baack, R D" uniqKey="Baack R">R.D. Baack</name></author><author><name sortKey="Markwell, J" uniqKey="Markwell J">J. Markwell</name></author><author><name sortKey="Herman, P L" uniqKey="Herman P">P.L. Herman</name></author><author><name sortKey="Osterman, J C" uniqKey="Osterman J">J.C. Osterman</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Li, R" uniqKey="Li R">R. Li</name></author><author><name sortKey="Ziola, B" uniqKey="Ziola B">B. Ziola</name></author><author><name sortKey="King, J" uniqKey="King J">J. King</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Uotila, L" uniqKey="Uotila L">L. Uotila</name></author><author><name sortKey="Koivusalo, M" uniqKey="Koivusalo M">M. Koivusalo</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Ohyama, T" uniqKey="Ohyama T">T. Ohyama</name></author><author><name sortKey="Yamazaki, I" uniqKey="Yamazaki I">I. Yamazaki</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Peacock, D" uniqKey="Peacock D">D. Peacock</name></author><author><name sortKey="Boulter, D" uniqKey="Boulter D">D. Boulter</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Romanova, E G" uniqKey="Romanova E">E.G. Romanova</name></author><author><name sortKey="Alekseeva, A A" uniqKey="Alekseeva A">A.A. Alekseeva</name></author><author><name sortKey="Pometun, E V" uniqKey="Pometun E">E.V. Pometun</name></author><author><name sortKey="Tishkov, V I" uniqKey="Tishkov V">V.I. Tishkov</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Slusarczyk, H" uniqKey="Slusarczyk H">H. Slusarczyk</name></author><author><name sortKey="Felber, S" uniqKey="Felber S">S. Felber</name></author><author><name sortKey="Kula, M R" uniqKey="Kula M">M.R. Kula</name></author><author><name sortKey="Pohl, M" uniqKey="Pohl M">M. Pohl</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Karaguler, N G" uniqKey="Karaguler N">N.G. Karaguler</name></author><author><name sortKey="Sessions, R B" uniqKey="Sessions R">R.B. Sessions</name></author><author><name sortKey="Clarke, A R" uniqKey="Clarke A">A.R. Clarke</name></author><author><name sortKey="Holbrook, J" uniqKey="Holbrook J">J. Holbrook</name></author></analytic></biblStruct><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Serov, A E" uniqKey="Serov A">A.E. Serov</name></author><author><name sortKey="Popova, A S" uniqKey="Popova A">A.S. Popova</name></author><author><name sortKey="Fedorchuk, V V" uniqKey="Fedorchuk V">V.V. Fedorchuk</name></author><author><name sortKey="Tishkov, V I" uniqKey="Tishkov V">V.I. Tishkov</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Seelbach, K" uniqKey="Seelbach K">K. Seelbach</name></author><author><name sortKey="Riebel, B" uniqKey="Riebel B">B. Riebel</name></author><author><name sortKey="Hummel, W" uniqKey="Hummel W">W. Hummel</name></author><author><name sortKey="Kula, M R" uniqKey="Kula M">M.-R. Kula</name></author><author><name sortKey="Tishkov, V I" uniqKey="Tishkov V">V.I. Tishkov</name></author><author><name sortKey="Egorov, A M" uniqKey="Egorov A">A.M. Egorov</name></author><author><name sortKey="Wandrey, C" uniqKey="Wandrey C">C. Wandrey</name></author><author><name sortKey="Kragl, U" uniqKey="Kragl U">U. Kragl</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Rissom, S" uniqKey="Rissom S">S. Rissom</name></author><author><name sortKey="Schwarz Linek, U" uniqKey="Schwarz Linek U">U. Schwarz-Linek</name></author><author><name sortKey="Vogel, M" uniqKey="Vogel M">M. Vogel</name></author><author><name sortKey="Tishkov, V I" uniqKey="Tishkov V">V.I. Tishkov</name></author><author><name sortKey="Kragl, U" uniqKey="Kragl U">U. Kragl</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Sadykhov, E G" uniqKey="Sadykhov E">E.G. Sadykhov</name></author><author><name sortKey="Serov, A E" uniqKey="Serov A">A.E. Serov</name></author><author><name sortKey="Voinova, N S" uniqKey="Voinova N">N.S. Voinova</name></author><author><name sortKey="Uglanova, S V" uniqKey="Uglanova S">S.V. Uglanova</name></author><author><name sortKey="Petrov, A S" uniqKey="Petrov A">A.S. Petrov</name></author><author><name sortKey="Kleimenov, S Yu" uniqKey="Kleimenov S">S.Yu. Kleimenov</name></author><author><name sortKey="Popov, V O" uniqKey="Popov V">V.O. Popov</name></author><author><name sortKey="Tishkov, V I" uniqKey="Tishkov V">V.I. Tishkov</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Sadykhov, E G" uniqKey="Sadykhov E">E.G. Sadykhov</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Resch, A" uniqKey="Resch A">A. Resch</name></author><author><name sortKey="Rosenstein, R" uniqKey="Rosenstein R">R. Rosenstein</name></author><author><name sortKey="Nerz, C" uniqKey="Nerz C">C. Nerz</name></author><author><name sortKey="Gotz, F" uniqKey="Gotz F">F. Gotz</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Savin, S S" uniqKey="Savin S">S.S. Savin</name></author><author><name sortKey="Tishkov, V I" uniqKey="Tishkov V">V.I. Tishkov</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Shabalin, I G" uniqKey="Shabalin I">I.G. Shabalin</name></author><author><name sortKey="Serov, A E" uniqKey="Serov A">A.E. Serov</name></author><author><name sortKey="Skirgello, O E" uniqKey="Skirgello O">O.E. Skirgello</name></author><author><name sortKey="Timofeev, V I" uniqKey="Timofeev V">V.I. Timofeev</name></author><author><name sortKey="Samygina, V R" uniqKey="Samygina V">V.R. Samygina</name></author><author><name sortKey="Popov, V O" uniqKey="Popov V">V.O. Popov</name></author><author><name sortKey="Tishkov, V I" uniqKey="Tishkov V">V.I. Tishkov</name></author><author><name sortKey="Kuranova, I P" uniqKey="Kuranova I">I.P. Kuranova</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Alekseeva, A A" uniqKey="Alekseeva A">A.A. Alekseeva</name></author><author><name sortKey="Shabalin, I G" uniqKey="Shabalin I">I.G. Shabalin</name></author><author><name sortKey="Polyakov, K M" uniqKey="Polyakov K">K.M. Polyakov</name></author><author><name sortKey="Tishkov, V I" uniqKey="Tishkov V">V.I. Tishkov</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Tishkov, V I" uniqKey="Tishkov V">V.I. Tishkov</name></author><author><name sortKey="Uglanova, S V" uniqKey="Uglanova S">S.V. Uglanova</name></author><author><name sortKey="Fedorchuk, V V" uniqKey="Fedorchuk V">V.V. Fedorchuk</name></author><author><name sortKey="Savin, S S" uniqKey="Savin S">S.S. Savin</name></author></analytic></biblStruct></listBibl></div1></back></TEI><pmc article-type="review-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">22649703</article-id><article-id pub-id-type="pmc">3347622</article-id><article-categories><subj-group subj-group-type="heading"><subject>Review</subject></subj-group><subj-group><subject>Molecular Biology</subject></subj-group></article-categories><title-group><article-title>NAD <sup>+</sup> -dependent Formate Dehydrogenase from Plants
</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Alekseeva</surname><given-names>A.A.</given-names></name><xref ref-type="aff" rid="AF1"></xref><xref ref-type="aff" rid="AF2"></xref><xref ref-type="aff" rid="AF3"></xref></contrib><contrib contrib-type="author"><name><surname>Savin</surname><given-names>S.S.</given-names></name><xref ref-type="aff" rid="AF2"></xref><xref ref-type="aff" rid="AF3"></xref></contrib><contrib contrib-type="author"><name><surname>Tishkov</surname><given-names>V.I.</given-names></name><xref ref-type="aff" rid="AF1"></xref><xref ref-type="aff" rid="AF2"></xref><xref ref-type="aff" rid="AF3"></xref><email>vitishkov@gmail.com</email></contrib></contrib-group><aff id="AF1">Chemistry Department, Lomonosov Moscow State University</aff><aff id="AF2">Innovations and High Technologies MSU Ltd</aff><aff id="AF3">Bach Institute of Biochemistry, Russian Academy of Sciences</aff><pub-date pub-type="ppub"><season>Oct-Dec</season><year>2011</year></pub-date><volume>3</volume><issue>4</issue><fpage>38</fpage><lpage>54</lpage><permissions><copyright-statement>Copyright © 2011 Park-media Ltd.</copyright-statement><copyright-year>2011</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>NAD<sup>+</sup>-dependent formate dehydrogenase (FDH, EC 1.2.1.2) widely occurs
in nature. FDH consists of two identical subunits and contains neither
prosthetic groups nor metal ions. This type of FDH was found in different
microorganisms (including pathogenic ones), such as bacteria, yeasts, fungi, and
plants. As opposed to microbiological FDHs functioning in cytoplasm, plant FDHs
localize in mitochondria. Formate dehydrogenase activity was first discovered as
early as in 1921 in plant; however, until the past decade FDHs from plants had
been considerably less studied than the enzymes from microorganisms. This review
summarizes the recent results on studying the physiological role, properties,
structure, and protein engineering of plant formate dehydrogenases.</p></abstract><kwd-group kwd-group-type="author"><kwd>plant formate dehydrogenase</kwd><kwd>physiological role</kwd><kwd>properties</kwd><kwd>structure; expression;<italic>Escherichia coli</italic></kwd><kwd>protein engineering</kwd></kwd-group></article-meta></front><body><sec><title>INTRODUCTION</title><p>NAD <sup>+</sup> -dependent formate dehydrogenases (FDHs) [EC 1.2.1.<xref ref-type="bibr" rid="R2">2</xref>] belong to the family of enzymes catalyzing
the oxidation of the formate ion to carbon dioxide, coupled with NAD <sup>+ </sup>reduction to NADH: </p><p>HCOO <sup>-</sup> + NAD <sup>+ </sup> → CO <sub>2</sub> ↑ + NADH. </p><p>It is possible to distinguish two major FDH groups based on the differences in
structure of these enzymes. The first group is comprised of formate dehydrogenases
from anaerobic microorganisms and archae. FDHs in this group are heterooligomers
with a complex quaternary structure and a high molecular weight. They are generally
characterized by the presence of various prosthetic groups (iron–sulphur
clusters, molybdenum and tungsten ions) in the active site and high sensitivity to
oxygen [<xref ref-type="bibr" rid="R1">1</xref>, <xref ref-type="bibr" rid="R2">2</xref>].</p><p>The second group is comprised of NAD <sup>+</sup> -dependent formate dehydrogenases
consisting of two identical subunits, both having two active sites and containing
neither metal ions nor prosthetic groups in the protein globule. FDHs of this group
belong to the superfamily of D-specific dehydrogenases of 2-oxyacids [<xref ref-type="bibr" rid="R3">3</xref>]. The reaction of formate oxidation catalyzed
by a FDH from this group is the simplest example of dehydrogenation of carbonyl
compounds, since there is neither the stage of proton transfer in the catalytic
mechanism nor other stages of acid–base catalysis. The reaction rate is
generally limited by the rate of hydride ion transfer from the substrate to the C4
atom of the nicotinamide ring [<xref ref-type="bibr" rid="R4">4</xref>]. Thus, FDH
can be used as a model enzyme for studying the mechanism of hydride ion transfer in
the active site of dehydrogenases that belong to this superfamily. </p><p>The active and systematic study of FDHs began in the early 1970s and was primarily
devoted to enzymes from microorganisms. The physiological role of microbial FDHs is
different. Thus, in methanol-utilizing bacteria and yeast, this enzyme participates
in the supply of energy to a cell, whereas in pathogenic bacteria and fungi FDH is a
stress protein. The properties and protein engineering of FDH were thoroughly
discussed in [<xref ref-type="bibr" rid="R5">5</xref>, <xref ref-type="bibr" rid="R6">6</xref>].</p><p>NAD <sup>+</sup> -dependent formate dehydrogenases from plants also belong to the
second FDH group. Recent studies have revealed that FDH also belongs to stress
proteins in plants, similar to those found in pathogenic microorganisms. FDH
synthesis strongly increases under the following conditions: drought, with abrupt
changes in temperature, irradiation with hard ultraviolet light, through the action
of chemical agents [7–<xref ref-type="bibr" rid="R9">9</xref>], hypoxia [<xref ref-type="bibr" rid="R10">10</xref>], and action of pathogenic microorganisms
[<xref ref-type="bibr" rid="R11">11</xref>]. The significance of the
physiological role of this enzyme gives rise to the necessity of studying plant
FDHs. Till now, there are no publications in which the data on plant FDHs are
systematized. The major features of plant formate dehydrogenases, as well as their
kinetic properties and stability, are summarized in this review; a detailed
description of the physiological role of FDH is also presented. </p></sec><sec><title>DISCOVERY HISTORY, LOCALIZATION,
AND PHYSIOLOGICAL ROLE OF PLANT
FDHs</title><p>Plant FDH was first found in beans ( <italic>Phaseolus vulgaris</italic> ) in 1921
[<xref ref-type="bibr" rid="R12">12</xref>]. </p><p>The first attempt to provide a detailed description of FDH and to assess the role of
this enzyme in plant metabolism was made by Davison in 1951 [<xref ref-type="bibr" rid="R13">13</xref>], by the example of formate dehydrogenases from pea and bean
seeds. The role of FDH was believed to consist in the production of NADH, which was
subsequently consumed for the formation of ethanol, succinate, and glutamate in
coupled reactions. Thus, the role of FDH as a “supplier” of NADH
molecules to fit the various needs of a cell was first defined. An assumption
concerning the mechanisms of the emergence of formate in a plant cell was made in
the same study. According to the first hypothesis, formate could be formed along
with ethanol and acetic acid as a result of anaerobic respiration. According to an
alternative hypothesis, formate could be formed during the oxidation of glycolic
acid; however, no unambiguous data that would corroborate a certain metabolic
pathway, during which formate is formed, have been obtained thus far.</p><p>The first experiments for determining the localization of FDHs in plant cells were
carried out in 1956. It was revealed that formate dehydrogenase activity was
primarily present in mitochondria [<xref ref-type="bibr" rid="R14">14</xref>].
However, due to the fact that the samples under study were contaminated with other
organelles, it couldn’t be unequivocally proven that FDH is localized in
mitochondria. In 1960, it was demonstrated that FDH was localized not only in seeds,
but also in other plant parts. Formate dehydrogenase activity was revealed in
cabbage and spinach leaves, roots of garden radish and turnip, cauliflower buds, and
pumpkin fruits [<xref ref-type="bibr" rid="R15">15</xref>]. It was demonstrated
using spinach leaves that there were at least two pathways for formate oxidation in
a plant cell: by FDH in mitochondria and by peroxidase in peroxisomes [<xref ref-type="bibr" rid="R16">16</xref>]. It was ascertained in separate experiments
that formate was oxidized by FDH in mitochondria at pH > 6, while peroxidase in
peroxisomes plays the major role in formate oxidation at lower pH values. Later, it
was shown that FDH in mitochondria was a component of a protein complex with a
molecular weight of approximately 200 kDa rather than being an individual molecule
[<xref ref-type="bibr" rid="R17">17</xref>]. These complexes can potentially be
formed by glycine decarboxylase and fumarase; their concentration increasing
synchronically with rising FDH activity [<xref ref-type="bibr" rid="R9">9</xref>].</p><p>It was shown in systematic studies that formate dehydrogenase activity was strongly
dependent both upon a plant and upon a particular plant organ containing the enzyme
[<xref ref-type="bibr" rid="R18">18</xref>]. The dependence of enzymatic
activity on the rate of oxygen consumption by a plant was also revealed. Thus, in
plants with high oxygen consumption (spinach, tobacco, etc.), formate dehydrogenase
activity was higher than that in a plant with low oxygen consumption (the
Leguminosae, lettuce, etc.) [<xref ref-type="bibr" rid="R18">18</xref>]. In this
study, the hypothesis was postulated that in oxidation of NADH obtained via the
formate dehydrogenase reaction, the accumulated energy was consumed for ATP
formation via the electron transport chain, thus satisfying the energy demand of the
cell [<xref ref-type="bibr" rid="R18">18</xref>]. Unfortunately, high variation of
FDH activity in different plants prevents the unambiguous answering of the question
concerning the role of this enzyme in the metabolism. The relationship between
formate metabolism and plant response to stress was first noted in 1978 [<xref ref-type="bibr" rid="R19">19</xref>], the increased formation of labelled carbon
dioxide from formate was observed in barley, which was grown under overwatering
conditions.</p><p>In 1992, research into the physiological role of formate dehydrogenase from plants
was raised to a new level [<xref ref-type="bibr" rid="R20">20</xref>]. It was
revealed that the mitochondria of non-photosynthesizing tissues of potato contained
an unknown peptide with a molecular weight of approximately 40 kDa, which composed
up to 9% of all mitochondrial proteins. cDNA of this polypeptide was cloned in 1993;
the analysis of the amino acid sequence encoded by this cDNA demonstrated 55%
homology with FDH from <italic>Pseudomonas </italic> sp. 101 [<xref ref-type="bibr" rid="R21">21</xref>]. Comparison of the N-terminal sequences of natural FDH and
polypeptide translated from cDNA revealed that the theoretical protein contained an
additional signal peptide consisting of 23 amino acid residues, which provided the
transport of pro-enzyme from cytoplasm inside mitochondria. Polypeptides of the same
molecular mass were found in pea, tomato, and onion; the FDH content in the
mitochondria of non-photosynthetic tissues (tubers and roots) was approximately
eightfold higher than that in leaves [<xref ref-type="bibr" rid="R20">20</xref>].
Moreover, FDH concentration sharply increased in plants which were grown in the dark
(pea stems, chicory leaves, carrot roots, sweet potato tubers, etc.) [<xref ref-type="bibr" rid="R20">20</xref>]. </p><p>Actually, numerous data have been published supporting the fact that FDH is
synthesized at a high concentration under conditions that are unfavourable to plant
growth, e.g.: drought, low temperature, hard ultraviolet radiation, exposure
chemical agents, deficiency of both light and iron, and low oxygen concentration.
However, the response rate strongly depended on the type of interaction. Thus, the
fastest response of potato plants, which manifests itself by mRNA synthesis, was
observed upon direct damage to plant tissue (~20 min), whereas the average response
time for other types of impacts was equal to 8 h [<xref ref-type="bibr" rid="R7">7</xref>]. Under conditions of iron deficiency, the amount of formate
dehydrogenase mRNA in barley roots began to increase after 1 day, attaining the
maximum value after 14 days [<xref ref-type="bibr" rid="R8">8</xref>, <xref ref-type="bibr" rid="R22">22</xref>], whereas the synthesis of formate
dehydrogenase in leaves did not change. Under anaerobic stress, the concentration of
FDH mRNA in barley roots increased as early as after 12 h, attaining the maximum
value by the 48th hour. In maritime pine, the biosynthesis of FDH is enhanced during
a drought [<xref ref-type="bibr" rid="R23">23</xref>]. An increase in the level of
FDH mRNA was also observed in <italic>Lotus japonicиs </italic> plants
cultivated under conditions of hypoxia [<xref ref-type="bibr" rid="R10">10</xref>]. </p><p>The gene expression in moss <italic>Physcomitrella patens </italic> responding to
stress was studied in [<xref ref-type="bibr" rid="R24">24</xref>]. Moss plants were
treated with abscisic acid (hormone inducing the transfer of plants to the rest
period and being capable of decelerating stem growth, which is accumulated in seeds
and buds in Autumn) followed by cooling to +4 <sup>о</sup> С. It was
found that abscisic acid induced an increase in resistance of moss to low
temperatures; it also altered the set of expressed genes. FDH is one of the enzymes
whose gene is expressed under the action of abscisic acid. It turned out that the
level of FDH gene expression increased during several hours following treatment with
abscisic acid and when the plants were stored in cold temperature for 24 h. In the
absence of abscisic acid, the response to the impact of low temperatures occurs much
more slowly. Treatment with sodium chloride at high concentrations (0.125 and
0.25 M) and mannitol (0.25 and 0.5 M) enhanced both the resistance of the moss to
low temperatures and the expression of a number of genes, including the FDH gene. It
was thus demonstrated that formate dehydrogenase was a stress protein both in higher
plants and in mosses; the level of its biosynthesis could be regulated by hormones.
Other plant hormones, such as auxin and cytokinin, also have an effect on FDH
activity in higher plants [<xref ref-type="bibr" rid="R25">25</xref>]. </p><p>The synthesis of FDH was also studied in <italic>Arabidopsis thaliana, </italic>being exposed to various factors. It was the first plant for which the complete
nucleotide sequence of the genome was determined; therefore, in many cases
<italic>A. thaliana </italic> is used as a model plant. The plants were sprayed
with various C1-compounds (methanol, formaldehyde, and formate) followed by the
Northern blot analysis using FDH cDNA as a probe. The most intensive expression of
the FDH gene was observed for treatment with formaldehyde or methanol. A lower level
of expression was observed in the samples sprayed with formate and deionized water.
An increase in the expression of the FDH gene was not recorded, neither in plants
with their leaves pruned nor in the control sample. These data enabled one to
reasonably conclude that the synthesis of FDH was induced to a larger extent not by
the formate substrate, but by its reduced form (formaldehyde) [<xref ref-type="bibr" rid="R26">26</xref>]. It was also demonstrated [<xref ref-type="bibr" rid="R27">27</xref>] that one-carbon compounds (methanol, formaldehyde, and formate)
induced the synthesis of FDH in plant leaves. Methanol has a direct effect on the
synthesis of FDH transcripts, while its oxidized modifications (formaldehyde,
formate) can act as signalling molecules. An analysis of the N-terminal region of
the enzyme allowed one to assume that FDH can also be transported to chloroplasts.
The dual localization of FDH, both in mitochondria and chloroplasts, was shown in
transgenic <italic> A. thaliana</italic> and tobacco plants containing the AthFDH
gene [<xref ref-type="bibr" rid="R28">28</xref>]. </p><p>The origin of formate in cells of the plants exposed to stress remains unknown. The
hypothesis has been put forward suggesting that formate may be synthesized during
photorespiration, in the methanol metabolism, or from glyoxylate formed from
different products of the Krebs cycle [<xref ref-type="bibr" rid="R7">7</xref>]. The
formation of formate by the serine pathway as it takes place in bacteria [<xref ref-type="bibr" rid="R1">1</xref>] has been discussed, since the introduction of
serine resulted in the increase in FDH concentration in potato plants. In further
experiments [<xref ref-type="bibr" rid="R29">29</xref>], the transgenic potato with
suppressed synthesis of FDH was obtained. It was revealed that formate that does not
undergo further oxidation to carbon dioxide was accumulated in the tissues of
transgenic plants. It was also shown that proline and its precursor glutamate were
formed at a high concentration in transgenic potato under conditions of drought.</p><p>The metabolism of formate and its physiological role have been well studied [<xref ref-type="bibr" rid="R30">30</xref>]. In photosynthesizing potato tissues,
formate is the major precursor of all other carbon-containing compounds; it is
basically synthesized via ferredoxin-dependent fixation of carbon dioxide. In other
tissues, formate is a side product of photorespiration and some enzymatic processes;
its formation seems to result from the direct reduction of carbon dioxide in
chloroplasts. In potato plants, the metabolism of formate is associated with the
synthesis of serine.</p><p>A close relationship between the biosynthesis of formate and serine also exists in
<italic>A. thaliana</italic> [<xref ref-type="bibr" rid="R31">31</xref>]. Three
lines of transgenic plants with enhanced expression of FDH were obtained. Formate
concentration in transgenic plants was almost identical to that in wild-type
<italic>A. thaliana</italic> . Following the introduction of labelled formate,
the intensity of formation of radioactively labelled carbon dioxide in transgenic
plants was much higher, whereas serine accumulation remained at the same level.
Transgenic <italic>A. thaliana</italic> plants with an enhanced level of FDH gene
expression were also obtained in [<xref ref-type="bibr" rid="R32">32</xref>]. </p><p>Phosphorylation is the most important method of metabolism regulation. 14 proteins of
potato mitochondria, which can be presented in the phosphorylated form, have been
discovered [<xref ref-type="bibr" rid="R33">33</xref>]; among them FDH can also be
found. The amino acid residues of mitochondrial FDH of potato, which undergo
phosphorylation (Thr76 and Thr333) have been identified [<xref ref-type="bibr" rid="R34">34</xref>]. An analysis of the FDH structure demonstrated that these
two threonine residues were located on the surface of a protein globule and could be
easily accessible for kinases catalyzing the phosphorylation process. A high
phosphorylation level is observed in the Е1-α subunit of pyruvate
dehydrogenase (PDH). The phosphorylation of both FDH and pyruvate dehydrogenase is
regulated by the variation of concentrations of NAD <sup>+</sup> , formate, and
pyruvate, which attests to the similarity in the mechanisms of regulation of the
function of these enzymes. The level of phosphorylation of the enzyme is
considerably reduced with increasing concentrations of NAD <sup>+</sup> , formate,
and pyruvate. It is assumed that pyruvate can be converted into formate in the
reaction catalyzed by pyruvate formate lyase (PFL) followed by the oxidation of
formate with the participation of FDH. </p><p>Formate ion takes part in a great number of metabolic processes with complicated
regulation, as can clearly be seen from the data provided. The most complete scheme
of participation of formate in plant metabolism can be found in [<xref ref-type="bibr" rid="R11">11</xref>].</p><p>Recent studies have attested to the fact that FDH content in plant mitochondria
increases in response not only to physical and chemical factors, but also as a
result of a “biological attack”. The activation of biosynthesis of FDH
was observed following infection of the English oak with the pathogenic fungus,
<italic>Piloderma croceum</italic> [<xref ref-type="bibr" rid="R35">35</xref>];
wheat, with fungus <italic>Blumeria graminis f. sp. tritici</italic> [<xref ref-type="bibr" rid="R36">36</xref>]; and the common bean, with fungus
<italic>Colletotrichum lindemuthianum</italic> [<xref ref-type="bibr" rid="R11">11</xref>]. The common bean genome contains three FDH genes; their expression
is regulated by the type of exposure factor. It is assumed that synthesis of FDH in
wheat is induced by methanol as a result of the impact of pectin methylesterase on
pectin. In plants of the common tobacco <italic>Nicotiana attenuate </italic>damaged by <italic>Manduca sexta</italic> caterpillars, fatty acid conjugates
initiating the synthesis of a number of proteins, including FDH, are released [<xref ref-type="bibr" rid="R37">37</xref>]. </p><p>Summarizing this section, let us note that formate dehydrogenase is a universal
enzyme involved in the cell stress response caused by both exogenic (negative
ambient impact) and endogenic (deficiency of essential microelements, exposure to
pathogens) processes. This fact attests to the key role of FDH in metabolism
processes of higher plants. The production of mutant forms of FDH characterized by
an enhanced catalytic activity and the insertion of their genes into the plant
genome instead of wild-type enzyme genes represents a fundamentally new approach to
the design of plants with an enhanced resistance to stress.</p><table-wrap id="T1" orientation="portrait" position="float"><label>Table 1</label><caption><p> The sources and contracted notations of formate dehydrogenases considered in
the present study </p></caption><table frame="hsides" rules="groups"><thead><tr><th colspan="2" rowspan="1">Organism</th><th rowspan="2" colspan="1">FDH</th><th rowspan="2" colspan="1">Reference</th></tr><tr><th rowspan="1" colspan="1">Latin name</th><th rowspan="1" colspan="1">English name</th></tr></thead><tbody><tr><td colspan="4" rowspan="1">PLANTS</td></tr><tr><td rowspan="1" colspan="1"><italic>Antirrhinum majus</italic></td><td rowspan="1" colspan="1">Common Snapdragon</td><td rowspan="1" colspan="1">AmaFDH1</td><td rowspan="1" colspan="1">KEGG: EST 2545</td></tr><tr><td rowspan="2" colspan="1"><italic>Aquilegia formosa x Aquilegia
pubescens</italic></td><td rowspan="2" colspan="1">Buttercup</td><td rowspan="1" colspan="1">ApuFDH1</td><td rowspan="1" colspan="1">KEGG: EST 273</td></tr><tr><td rowspan="1" colspan="1">ApuFDH2</td><td rowspan="1" colspan="1">[11]</td></tr><tr><td rowspan="1" colspan="1"><italic>Arabidopsis thaliana</italic></td><td rowspan="1" colspan="1">Mouse-ear cress</td><td rowspan="1" colspan="1">AthFDH</td><td rowspan="1" colspan="1">EMBL AF208029</td></tr><tr><td rowspan="1" colspan="1"><italic>Brachypodium distachyon</italic></td><td rowspan="1" colspan="1">Purple false brome</td><td rowspan="1" colspan="1">BdiFDH1</td><td rowspan="1" colspan="1">[11]</td></tr><tr><td rowspan="2" colspan="1"><italic>Brassica napus</italic></td><td rowspan="2" colspan="1">Rapeseed</td><td rowspan="1" colspan="1">BnaFDH1</td><td rowspan="1" colspan="1">[11]</td></tr><tr><td rowspan="1" colspan="1">BnaFDH2</td><td rowspan="1" colspan="1">KEGG: EST 21261</td></tr><tr><td rowspan="1" colspan="1"><italic>Brassica oleracea</italic></td><td rowspan="1" colspan="1">Cabbage</td><td rowspan="1" colspan="1">BolFDH1</td><td rowspan="1" colspan="1">[11]</td></tr><tr><td rowspan="1" colspan="1"><italic>Cryptomeria japonica</italic></td><td rowspan="1" colspan="1">Japanese cedar</td><td rowspan="1" colspan="1">CjaFDH1</td><td rowspan="1" colspan="1">KEGG: EST 5066</td></tr><tr><td rowspan="1" colspan="1"><italic>Carica papaya</italic></td><td rowspan="1" colspan="1">Papaya</td><td rowspan="1" colspan="1">CpaFDH1</td><td rowspan="1" colspan="1">KEGG: EST 3924</td></tr><tr><td rowspan="1" colspan="1"><italic>Citrus reticulata</italic></td><td rowspan="1" colspan="1">Tangerine</td><td rowspan="1" colspan="1">CreFDH3</td><td rowspan="1" colspan="1">KEGG: EST 11052</td></tr><tr><td rowspan="1" colspan="1"><italic>Citrus sinensis</italic></td><td rowspan="1" colspan="1">Sweet orange</td><td rowspan="1" colspan="1">CsiFDH1</td><td rowspan="1" colspan="1">[11]</td></tr><tr><td rowspan="1" colspan="1"><italic>Coffea canephora</italic></td><td rowspan="1" colspan="1">Coffea canephora</td><td rowspan="1" colspan="1">CcaFDH1</td><td rowspan="1" colspan="1">KEGG: EST 1007</td></tr><tr><td rowspan="1" colspan="1"><italic>Festuca arundinacea</italic></td><td rowspan="1" colspan="1">Tall fescue</td><td rowspan="1" colspan="1">FarFDH1</td><td rowspan="1" colspan="1">KEGG: EST 5855</td></tr><tr><td rowspan="5" colspan="1"><italic>Glycine max</italic></td><td rowspan="5" colspan="1">Soybean</td><td rowspan="1" colspan="1">SoyFDH1</td><td rowspan="1" colspan="1">GB AK244764, [38]</td></tr><tr><td rowspan="1" colspan="1">SoyFDH2</td><td rowspan="1" colspan="1">GB Bt094321</td></tr><tr><td rowspan="1" colspan="1">SoyFDH3</td><td rowspan="1" colspan="1">GB AK243932, [38]</td></tr><tr><td rowspan="1" colspan="1">SoyFDH4</td><td rowspan="1" colspan="1">GB BT095613</td></tr><tr><td rowspan="1" colspan="1">SoyFDH5</td><td rowspan="1" colspan="1">KEGG: EST 19520</td></tr><tr><td rowspan="1" colspan="1"><italic>Gossypium arboreum</italic></td><td rowspan="1" colspan="1">Tree cotton</td><td rowspan="1" colspan="1">GarFDH1</td><td rowspan="1" colspan="1">KEGG: EST 1085</td></tr><tr><td rowspan="1" colspan="1"><italic>Gossypium hirsutum</italic></td><td rowspan="1" colspan="1">Tree cotton</td><td rowspan="1" colspan="1">GhiFDH1</td><td rowspan="1" colspan="1">KEGG: EST 19680</td></tr><tr><td rowspan="1" colspan="1"><italic>Gossypium raimondii</italic></td><td rowspan="1" colspan="1">Tree cotton</td><td rowspan="1" colspan="1">GraFDH1</td><td rowspan="1" colspan="1">KEGG: EST 213</td></tr><tr><td rowspan="1" colspan="1"><italic>Helianthus annuus</italic></td><td rowspan="1" colspan="1">Common sunflower</td><td rowspan="1" colspan="1">HanFDH1</td><td rowspan="1" colspan="1">[11]</td></tr><tr><td rowspan="1" colspan="1"><italic>Hordeum vulgare</italic></td><td rowspan="1" colspan="1">Barley</td><td rowspan="1" colspan="1">HvuFDH1</td><td rowspan="1" colspan="1">GB D88272, [8]</td></tr><tr><td rowspan="1" colspan="1"><italic>Ipomoea batatas</italic></td><td rowspan="1" colspan="1">Sweet potato</td><td rowspan="1" colspan="1">IbaFDH</td><td rowspan="1" colspan="1">EMBL BM878811</td></tr><tr><td rowspan="1" colspan="1"><italic>Lactuca saligna</italic></td><td rowspan="1" colspan="1">Willowleaf lettuce</td><td rowspan="1" colspan="1">LsaFDH1</td><td rowspan="1" colspan="1">KEGG: EST 1616</td></tr><tr><td rowspan="1" colspan="1"><italic>Lotus japonicus</italic></td><td rowspan="1" colspan="1">–</td><td rowspan="1" colspan="1">LjaFDH1</td><td rowspan="1" colspan="1">GB FM865900, [10]</td></tr><tr><td rowspan="1" colspan="1"><italic>Lycopersicon esculentum</italic></td><td rowspan="1" colspan="1">Tomato</td><td rowspan="1" colspan="1">LesFDH1</td><td rowspan="1" colspan="1">GB AJ849378</td></tr><tr><td rowspan="1" colspan="1"><italic>Malus domestica</italic></td><td rowspan="1" colspan="1">Apple</td><td rowspan="1" colspan="1">MdoFDH</td><td rowspan="1" colspan="1">EMBL CN496368</td></tr><tr><td rowspan="1" colspan="1"><italic>Manihot esculenta</italic></td><td rowspan="1" colspan="1">Cassava</td><td rowspan="1" colspan="1">MesFDH1</td><td rowspan="1" colspan="1">KEGG: EST 2788</td></tr><tr><td rowspan="1" colspan="1"><italic>Medicago truncatula</italic></td><td rowspan="1" colspan="1">Barrel Medic</td><td rowspan="1" colspan="1">MtrFDH1</td><td rowspan="1" colspan="1">KEGG: EST 1503</td></tr><tr><td rowspan="1" colspan="1"><italic>Mesembryanthemum crystallinum</italic></td><td rowspan="1" colspan="1">Common ice plant</td><td rowspan="1" colspan="1">McrFDH</td><td rowspan="1" colspan="1">GB BE035085</td></tr><tr><td rowspan="1" colspan="1"><italic>Nicotiana tabacum</italic></td><td rowspan="1" colspan="1">Common tobacco</td><td rowspan="1" colspan="1">NtaFDH1</td><td rowspan="1" colspan="1">[11]</td></tr><tr><td rowspan="1" colspan="1"><italic>Oryza sativa Japonica group</italic></td><td rowspan="1" colspan="1">Japanese rice</td><td rowspan="1" colspan="1">OsaFDH_Ja</td><td rowspan="1" colspan="1">GB AK065872, [39]</td></tr><tr><td rowspan="1" colspan="1"><italic>Oryza sativa indica cultivar-group</italic></td><td rowspan="1" colspan="1">Indian rice</td><td rowspan="1" colspan="1">OsaFDH_In</td><td rowspan="1" colspan="1">GB CT832868, [40]</td></tr><tr><td rowspan="1" colspan="1"><italic>Oryza sativa</italic></td><td rowspan="1" colspan="1">Rice</td><td rowspan="1" colspan="1">OsaFDH1</td><td rowspan="1" colspan="1">AB019533, [41]</td></tr><tr><td rowspan="1" colspan="1"><italic>Panicum virgatum</italic></td><td rowspan="1" colspan="1">Switchgrass</td><td rowspan="1" colspan="1">PviFDH1</td><td rowspan="1" colspan="1">KEGG: EST 8602</td></tr><tr><td rowspan="1" colspan="1"><italic>Phaseolus vulgaris</italic></td><td rowspan="1" colspan="1">Common bean</td><td rowspan="1" colspan="1">PvuFDH1</td><td rowspan="1" colspan="1">GB ACZ74695, [42]</td></tr><tr><td rowspan="1" colspan="1"><italic>Phyllostachys edulis</italic></td><td rowspan="1" colspan="1">Moso bamboo</td><td rowspan="1" colspan="1">PedFDH</td><td rowspan="1" colspan="1">GB FP093692</td></tr><tr><td rowspan="1" colspan="1"><italic>Physcomitrella patens</italic></td><td rowspan="1" colspan="1">Moss<italic>Physcomitrella patens</italic></td><td rowspan="1" colspan="1">PpaFDH</td><td rowspan="1" colspan="1">GB XM001768721, [43]</td></tr><tr><td rowspan="1" colspan="1"><italic>Picea glauca</italic></td><td rowspan="1" colspan="1">White spruce</td><td rowspan="1" colspan="1">PglFDH1</td><td rowspan="1" colspan="1">KEGG: EST 2327</td></tr><tr><td rowspan="1" colspan="1"><italic>Picea sitchensis</italic></td><td rowspan="1" colspan="1">Sitka spruce</td><td rowspan="1" colspan="1">PsiFDH</td><td rowspan="1" colspan="1">GB EF085163, [44]</td></tr><tr><td rowspan="1" colspan="1"><italic>Pinus pinaster</italic></td><td rowspan="1" colspan="1">Maritime pine</td><td rowspan="1" colspan="1">PpiFDH1</td><td rowspan="1" colspan="1">KEGG: EST 174</td></tr><tr><td rowspan="3" colspan="1"><italic>Pinus taeda</italic></td><td rowspan="3" colspan="1">Loblolly pine</td><td rowspan="1" colspan="1">PtaFDH1</td><td rowspan="1" colspan="1">[11]</td></tr><tr><td rowspan="1" colspan="1">PtaFDH2</td><td rowspan="1" colspan="1">KEGG: EST 2972</td></tr><tr><td rowspan="1" colspan="1">PtaFDH3</td><td rowspan="1" colspan="1">KEGG: EST 15504</td></tr><tr><td rowspan="1" colspan="1"><italic>Populus nigra</italic></td><td rowspan="1" colspan="1">Lombardy poplar</td><td rowspan="1" colspan="1">PniFDH2</td><td rowspan="1" colspan="1">KEGG: EST 7989</td></tr><tr><td rowspan="1" colspan="1"><italic>Populus tremula</italic></td><td rowspan="1" colspan="1">Aspen</td><td rowspan="1" colspan="1">PtmFDH1</td><td rowspan="1" colspan="1">KEGG: EST 4757</td></tr><tr><td rowspan="1" colspan="1"><italic>Populus trichocarpa</italic></td><td rowspan="1" colspan="1">Western balsam poplar</td><td rowspan="1" colspan="1">PtrFDH1</td><td rowspan="1" colspan="1">PtrFDH1 GB XM002320465, [45]</td></tr><tr><td rowspan="1" colspan="1"><italic>Prunus persica</italic></td><td rowspan="1" colspan="1">Peach tree</td><td rowspan="1" colspan="1">PpeFDH1</td><td rowspan="1" colspan="1">KEGG: EST 4281</td></tr><tr><td rowspan="1" colspan="1"><italic>Quercus robur</italic></td><td rowspan="1" colspan="1">English oak</td><td rowspan="1" colspan="1">QroFDH1</td><td rowspan="1" colspan="1">GB AJ577266.2, [35]</td></tr><tr><td rowspan="1" colspan="1"><italic>Raphanus raphanistrum subsp. raphanistrum</italic></td><td rowspan="1" colspan="1">Wild radish</td><td rowspan="1" colspan="1">RraFDH1</td><td rowspan="1" colspan="1">KEGG: EST 15157</td></tr><tr><td rowspan="1" colspan="1"><italic>Ricinus communis</italic></td><td rowspan="1" colspan="1">Castor bean tree</td><td rowspan="1" colspan="1">RcoFDH1</td><td rowspan="1" colspan="1">GB XM_002517292</td></tr><tr><td rowspan="1" colspan="1"><italic>Saccharum officinarum</italic></td><td rowspan="1" colspan="1">Sugarcane</td><td rowspan="1" colspan="1">SofFDH1</td><td rowspan="1" colspan="1">KEGG: EST 18227</td></tr><tr><td rowspan="1" colspan="1"><italic>Solanum tuberosum</italic></td><td rowspan="1" colspan="1">Potato</td><td rowspan="1" colspan="1">StuFDH1</td><td rowspan="1" colspan="1">GB Z21493, [21]</td></tr><tr><td rowspan="2" colspan="1"><italic>Sorghum bicolor</italic></td><td rowspan="2" colspan="1">Sorghum</td><td rowspan="1" colspan="1">SbiFDH1</td><td rowspan="1" colspan="1">GB XM002438363, [46]</td></tr><tr><td rowspan="1" colspan="1">SbiFDH2</td><td rowspan="1" colspan="1">GB XM002454363, [46]</td></tr><tr><td rowspan="1" colspan="1"><italic>Taraxacum officinale</italic></td><td rowspan="1" colspan="1">Common dandelion</td><td rowspan="1" colspan="1">TofFDH1</td><td rowspan="1" colspan="1">[11]</td></tr><tr><td rowspan="1" colspan="1"><italic>Theobroma cacao</italic></td><td rowspan="1" colspan="1">Cacao tree</td><td rowspan="1" colspan="1">TcaFDH1</td><td rowspan="1" colspan="1">KEGG: EST 10274</td></tr><tr><td rowspan="1" colspan="1"><italic>Triphysaria pusilla</italic></td><td rowspan="1" colspan="1">Dwarf owl’s-clover</td><td rowspan="1" colspan="1">TpuFDH1</td><td rowspan="1" colspan="1">KEGG: EST 5550</td></tr><tr><td rowspan="1" colspan="1"><italic>Triticum aestivum</italic></td><td rowspan="1" colspan="1">Common wheat</td><td rowspan="1" colspan="1">TaeFDH1</td><td rowspan="1" colspan="1">TaeFDH1 GB AK332605, [47]</td></tr><tr><td rowspan="1" colspan="1"><italic>Vigna unguiculata</italic></td><td rowspan="1" colspan="1">Cowpea</td><td rowspan="1" colspan="1">VunFDH1</td><td rowspan="1" colspan="1">KEGG: EST 6491</td></tr><tr><td rowspan="1" colspan="1"><italic>Vitis vinifera</italic></td><td rowspan="1" colspan="1">Grape</td><td rowspan="1" colspan="1">VviFDH1</td><td rowspan="1" colspan="1">GB XM002278408</td></tr><tr><td rowspan="1" colspan="1"><italic>Yucca filamentosa</italic></td><td rowspan="1" colspan="1">Bear grass</td><td rowspan="1" colspan="1">YfiFDH1</td><td rowspan="1" colspan="1">YfiFDH1 [11]</td></tr><tr><td rowspan="1" colspan="1"><italic>Zea mays</italic></td><td rowspan="1" colspan="1">Maize</td><td rowspan="1" colspan="1">ZmaFDH</td><td rowspan="1" colspan="1">GB EU967680, [48]</td></tr><tr><td rowspan="1" colspan="1"><italic>Zingiber officinale</italic></td><td rowspan="1" colspan="1">Ginger</td><td rowspan="1" colspan="1">ZofFDH1</td><td rowspan="1" colspan="1">KEGG: EST 5316</td></tr><tr><td colspan="4" rowspan="1">fungi</td></tr><tr><td rowspan="1" colspan="1"><italic>Aspergillus oryzae</italic></td><td rowspan="1" colspan="1">Fungus<italic>Aspergillus oryzae</italic></td><td rowspan="1" colspan="1">AorFDH1</td><td rowspan="1" colspan="1">NCBI XM001827498</td></tr><tr><td rowspan="1" colspan="1"><italic>Mycosphaerella graminicola</italic></td><td rowspan="1" colspan="1">Fungus<italic>Mycosphaerella graminicola</italic></td><td rowspan="1" colspan="1">MgrFDH</td><td rowspan="1" colspan="1">GB AW180713 180985</td></tr><tr><td rowspan="1" colspan="1"><italic>Penicillium marneffei</italic></td><td rowspan="1" colspan="1">Fungus<italic>Penicillium marneffei</italic></td><td rowspan="1" colspan="1">PmaFDH1</td><td rowspan="1" colspan="1">GB XM002153251</td></tr><tr><td rowspan="2" colspan="1"><italic>Ajellomyces capsulatus</italic></td><td rowspan="2" colspan="1">Darling’s disease fungus</td><td rowspan="1" colspan="1">AjcFDH1</td><td rowspan="2" colspan="1">[49]</td></tr><tr><td rowspan="1" colspan="1">AjcFDH3</td></tr><tr><td colspan="4" rowspan="1"><italic>YEASTS</italic></td></tr><tr><td rowspan="1" colspan="1"><italic>Candida boidinii</italic></td><td rowspan="1" colspan="1">Methylotrophic yeast<italic>Candida boidinii</italic></td><td rowspan="1" colspan="1">CboFDH</td><td rowspan="1" colspan="1">EMBL AF004096</td></tr><tr><td rowspan="1" colspan="1"><italic>Saccharomyces cerevisiae</italic></td><td rowspan="1" colspan="1">Baker’s yeast</td><td rowspan="1" colspan="1">SceFDH</td><td rowspan="1" colspan="1">EMBL Z75296</td></tr><tr><td colspan="4" rowspan="1">BACTERIA</td></tr><tr><td rowspan="1" colspan="1"><italic>Pseudomonas sp. 101</italic></td><td rowspan="1" colspan="1">Methylotrophic bacterium<italic>Pseudomonas sp. </italic>101</td><td rowspan="1" colspan="1">PseFDH</td><td rowspan="1" colspan="1">[50]</td></tr><tr><td rowspan="1" colspan="1"><italic>Moraxella sp. С2</italic></td><td rowspan="1" colspan="1">Methylotrophic bacterium<italic>Moraxella sp.</italic></td><td rowspan="1" colspan="1">MorFDH</td><td rowspan="1" colspan="1">EMBL Y13245</td></tr><tr><td rowspan="1" colspan="1"><italic>Burkholderia stabilis</italic></td><td rowspan="1" colspan="1">Bacterium
<italic>Burkholderia stabilis</italic></td><td rowspan="1" colspan="1">BstFDH</td><td rowspan="1" colspan="1">[51]</td></tr><tr><td rowspan="1" colspan="1"><italic>Bordetella bronchiseptica RB50 (Alcaligenes
bronchisepticus)</italic></td><td rowspan="1" colspan="1">Bacterium
<italic>Bordetella bronchiseptica
</italic>RB50<italic> (Alcaligenes
bronchisepticus)</italic></td><td rowspan="1" colspan="1">BbrFDH</td><td rowspan="1" colspan="1">EMBL BX640441</td></tr><tr><td rowspan="1" colspan="1"><italic>Uncultured marine alpha proteobacterium</italic></td><td rowspan="1" colspan="1">Uncultured marine alpha proteobacterium</td><td rowspan="1" colspan="1">BbrFDH</td><td rowspan="1" colspan="1">EMBL BX640441</td></tr><tr><td rowspan="1" colspan="1"><italic>Sinorhizobium meliloti</italic></td><td rowspan="1" colspan="1">Nitrogen-fixing<italic>Sinorhizobium meliloti</italic></td><td rowspan="1" colspan="1">SmeFDH</td><td rowspan="1" colspan="1">Ae006469, [52]</td></tr></tbody></table></table-wrap></sec><sec><title>THE FEATURES OF THE PRIMARY STRUCTURE OF PLANT FDH</title><fig id="F1" orientation="portrait" position="float"><label>Fig. 1</label><caption><p> Signal sequences of plant formate dehydrogenases. Here and in <italic>Figs.
2,3</italic> , abbreviations of enzymes are those from <italic>Table</italic> <italic>1</italic> . Plant enzymes are highlighted in
green; fungi enzymes are highlighted in magenta; FDHs from bacteria are
highlighted in blue. Specific sequences that are responsible for the
transport of the enzyme to mitohondria are underlined. The residue, after
which the signal peptide is eliminated, are highlighted in green italics.
</p></caption><graphic xlink:href="AN20758251-11-038-g001"></graphic></fig><p>Due to the active development of mega-sequencing methods, a new genome structure of
various organisms, including plants, is published almost every day. Searching in
GenBank (GB), EMBL, and KEGG (http://www.genome.jp/) databases enabled us to find
nucleotide sequences of genes (complete or as cDNA) of plant FDH from over
70 sources. Moreover, study [<xref ref-type="bibr" rid="R11">11</xref>] presents a
number of sequences that are not present in the databases. <italic><xref ref-type="table" rid="T1">Table 1</xref></italic> lists the names of the
plants and the contracted notations of FDHs. FDHs that are characteristic of various
microorganisms, such as enzymes from methylotrophic bacteria
<italic>Pseudomonas</italic> sp. 101 (the most well studied FDH to this
moment), <italic>Moraxella</italic> sp. C2, pathogenic bacteria
<italic>Burkholderia stabilis</italic> and <italic>Bordetella
bronchiseptica RB50 (Alcaligenes bronchisepticus)</italic> , uncultured marine
alpha proteobacteria and nitrogen-fixing bacteria <italic>Sinorhizobium
meliloti</italic> , yeasts <italic>Saccharomyces cerevisiae</italic> and
<italic>Candida boidinii</italic> , were used for comparison. </p><fig id="F2" orientation="portrait" position="float"><label>Fig. 2</label><caption><p> Phylogenetic tree of N-terminal sequences for plant formate dehydrogenases.
</p></caption><graphic xlink:href="AN20758251-11-038-g002"></graphic></fig><p>The presence of a signal peptide, which is responsible for FDH transport from the
cytoplasm to mitochondria, at the N-terminus of the synthesized proenzyme is the
distinctive feature of plant FDHs [<xref ref-type="bibr" rid="R21">21</xref>].
Bacterial and yeast FDHs contain no signal peptides. The genes of FDHs from a number
of pathogenic fungi also contain the nucleotide sequence encoding the signal
peptide. However, depending on the condition of a host cell, the RNA synthesized
from the FDH gene undergoes alternative splicing, resulting in the formation of
different mRNAs encoding proteins both with and without the signal peptide [<xref ref-type="bibr" rid="R49">49</xref>].</p><fig id="F3" orientation="portrait" position="float"><label>Fig. 3</label><caption><p> Alignment of formate dehyfrogenases from different sources. Abbreviations of
enzymes see in <italic>Table</italic> 1. Plant enzymes are highlighted in
green; fungi enzymes are highlighted in magenta; FDHs from bacteria are
highlighted in blue. Specific sequences that are responsible for transport
of the enzyme to mitochondria are underlined. The numeration of residues is
the same as for the FDH from <italic>Pseudomonas</italic> sp. 101 (PseFDH).
The asterisk and red font mark the conserved amino acid residue. </p></caption><graphic xlink:href="AN20758251-11-038-g003"></graphic></fig><p><italic><xref ref-type="fig" rid="F1">Fig. 1</xref></italic>shows the signal sequences of formate dehydrogenases from various sources.
The potential specific sequences providing the transport of an enzyme to
mitochondria are underlined. The residue, after which the cleavage of the signal
peptide occurs, is shown in green italics. In the majority of formate
dehydrogenases, it is the arginine residue. Serine residue (FDH from sorghum
SbiFDH1, castor bean tree RcoFDH1), lysine (grape VviFDH1), proline (FDHs from
soybean SoyFDH1 and SoyFDH2, isoforms 1 and 2) can also be found in this position.
The signal sequence of FDH is enriched in amino acid residues containing hydroxyl or
positively charged groups and is capable of forming an amphiphilic α-helix. The
signal sequence is highly conserved. Thus, the deletion of only two N-terminal amino
acids blocks the transport of the enzyme to the mitochondria [<xref ref-type="bibr" rid="R53">53</xref>]. It was ascertained that the N-terminal MAM motif enabled
swift transport of the enzyme to mitochondria to be performed. <italic><xref ref-type="fig" rid="F1">Fig. 1</xref></italic> shows the N-terminal
sequences of 63 plant FDHs; 35 enzymes of those have the MAM motif at
position 1–3. A number of plant FDHs have similar motifs at their N-terminal
fragments: MAAM (in two plant FDHs) and MAS (in eight plant FDHs). The N-terminal
amino acid sequences of isoenzymes 1 and 2 of soybean FDHs are significantly
different from those of other plant formate dehydrogenases, both in terms of their
composition (it starts with MSN an MLN) and size, which attests to the possible
specific function of these FDH isoforms. The N-terminal sequences of FDHs from fungi
<italic>Aspergillus oryzae, As. flavus, Penicillium marneffei</italic> ,
<italic> Mycosphaerella graminicola, </italic> and <italic>Ajellomyces
capsulatus</italic> are also shown in <italic><xref ref-type="fig" rid="F1">Fig.
1</xref></italic> (the names are highlighted in pink). Two enzyme isoforms
from <italic>Aj. capsulatus</italic> (AjcFDH1 and AjcFDH3) are also given, which
result from the alternative splicing of mRNA [<xref ref-type="bibr" rid="R49">49</xref>]. Some sequences also contain an arginine residue, at which the
cleavage of the signal peptide may occur (the residue is highlighted in pink
italics). A similar mechanism of the FDH transport to different cell organelles
seems to exist in fungi. The Lys and Val residues that are totally conserved in all
formate dehydrogenases are shown in red in <italic><xref ref-type="fig" rid="F1">Fig. 1</xref></italic> . The N-terminal sequence of formate dehydrogenase
from <italic>Pseudomonas </italic> sp. 101 that is highly homologous to the
N-terminal region AjcFDH3 without the signal peptide is shown for comparative
purposes. As can be seen in <italic><xref ref-type="fig" rid="F1">Fig.
1</xref></italic> , signal peptide sequences in enzymes from the plants
belonging to one family (the family Solanaceae: tomatoes, potato; the family
Gramineae: rice, barley, rye, etc.) have a high degree of homology. </p><p>In most plants, FDH is located in the mitochondria; however, the thorough study of
the signal peptide of the enzyme from <italic>A. thaliana</italic> has shown that
the enzyme can also be transported to chloroplasts. The N-terminal fragment of this
enzyme strongly differs from the signal sequences of FDHs from potato, barley, and
rice. There is a hypothesis that under certain conditions AthFDH localizing in
chloroplasts is capable of catalyzing the reverse reaction, i.e., the conversion of
carbon dioxide into formate [<xref ref-type="bibr" rid="R27">27</xref>]. It was
shown by using another algorithm to compare the signal peptides of FDHs that all the
enzymes, with the exception of FDH from tomato plants, were capable of being
transported both to mitochondria and chloroplasts [<xref ref-type="bibr" rid="R28">28</xref>]. An analysis of signal sequences carried out using the Predotar,
TargetP, and Mitoprot software [<xref ref-type="bibr" rid="R11">11</xref>] confirmed
the fact that FDH is basically localized in mitochondria. </p><p>In plants, formate dehydrogenase is often represented by several isoforms, also known
as isoenzymes, whose synthesis is determined by the condition of a plant. The
differences in the isoenzyme composition of FDHs in healthy and affected palms
<italic>Pericopsis mooniana</italic> are used to select trees when selective
cutting is performed [<xref ref-type="bibr" rid="R54">54</xref>]. Polymorphism is
also typical for FDH from the almond tree <italic>Prunus dulcis </italic> [<xref ref-type="bibr" rid="R55">55</xref>] or <italic>P. amygdalus</italic> [<xref ref-type="bibr" rid="R56">56</xref>]. Based on the data of the analysis of
isoforms of FDHs and several other dehydrogenases, a method for identifying plant
genotype was proposed. As previously mentioned above, phosphorylation may be the
reason for the formation of different FDH isoforms [<xref ref-type="bibr" rid="R34">34</xref>]. Depending on the modification degree, the formation of numerous
forms of the enzyme with p <italic>I</italic> varying from 6.75 to 7.19 was
observed. Moreover, it was ascertained that the additional isoforms of potato FDH
emerged as a result of post-translational deamidation of Asn329 and Gln330 residues
[<xref ref-type="bibr" rid="R34">34</xref>]. </p><p>The differences in sequences of signal peptides are more strongly pronounced when
compared with those in plant FDHs; the homology level between which is ~80%. It is
most clearly demonstrated in the case of isoenzymes of soybean FDH. Homology of the
sequences of isoenzymes is 98%, whereas for the signal sequences, it is lower than
40%. <italic><xref ref-type="fig" rid="F2">Fig. 2</xref></italic> shows a
phylogenetic tree of the signal peptides of plant FDHs. As can be seen, two
isoenzymes of FDH from soybean <italic>Glycine max</italic> , SoyFDH1 and SoyFDH2,
form an individual group. The N-terminal fragment of these enzymes is much longer
than that in FDHs from other plants ( <italic><xref ref-type="fig" rid="F1">Fig.
1</xref></italic> ) and strongly differs in terms of its amino acid
composition. Next, there is a large branch of the family Gramineae, which includes
the enzymes of rice (OsaFDH), wheat (TaeFDH), barley (HvuFDH), sugarcane, moso
bamboo, etc. A large group is represented by the enzymes of plants belonging to the
family Brassicaceae (Cruciferae), namely, wild radish (RraFDH), cabbage (BolFDH),
rapeseed (BnaFDH), and <italic>A. thaliana</italic> (AthFDH). The other groups are
formed of proteins from Asteroideae, Leguminosae, Solanaceae, Malvaceae, Pinaceae,
and Salicaceae. As previously mentioned, five isoenzymes of soybean FDH do not form
a separate group. Since the signal peptide is basically responsible for the
transport of the enzyme inside the cell, an assumption can be made that different
isoenzymes of soybean FDH are transported into different organelles. </p><p><italic><xref ref-type="fig" rid="F3">Fig. 3</xref></italic> shows the alignment of
some complete sequences of plant FDHs that are known at the present time; the
sequences of a number of similar enzymes from microorganisms are provided for the
purposes of comparison. The absolutely conserved regions are highlighted in red; the
residues repeating only in plant FDHs are highlighted in green. A significant
difference of bacterial enzymes from the plant ones is an N-terminal rigid loop.
This region embraces a considerable part of the enzyme subunit. Its interaction with
other amino acid residues is likely to be accounted for by a higher thermal
stability of bacterial enzymes as compared with the plant ones. In addition, in FDHs
of microbial origin, the C-terminal region is longer than that in plant enzymes.
Meanwhile, the differentiation of FDH into two groups on the basis of its homology
is clearly observed in the remaining part of the amino acid sequence. The first
group contains bacterial and plant enzyme, whereas the second group consists of the
enzymes from yeasts and fungi.</p><table-wrap id="T2" orientation="portrait" position="float"><label>Table 2</label><caption><p> Kinetic parameters of formate dehydrogenases from different sources </p></caption><table frame="hsides" rules="groups"><thead><tr><th rowspan="1" colspan="1">FDH specimen</th><th rowspan="1" colspan="1">Specific activity, U/mg</th><th rowspan="1" colspan="1"><italic>k</italic><sub>cat</sub>,
s<sup>–1</sup></th><th rowspan="1" colspan="1"><italic>K</italic><sub>M</sub>(NAD<sup>+</sup>), µM</th><th rowspan="1" colspan="1"><italic>K</italic><sub>M</sub>
(formate), mM</th><th rowspan="1" colspan="1"><italic>K</italic><sub>M</sub>(NADP<sup>+</sup>), mM</th><th rowspan="1" colspan="1"></th><th rowspan="1" colspan="1">Reference</th></tr></thead><tbody><tr><td rowspan="1" colspan="1"><italic>Arabidopsis thaliana</italic>, native, after affinity
chromatography</td><td rowspan="1" colspan="1">NA*</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">65</td><td rowspan="1" colspan="1">10</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">[27]</td></tr><tr><td rowspan="1" colspan="1"><italic>A. thaliana</italic>, native, from mitochondria</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">76</td><td rowspan="1" colspan="1">11</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">[59]</td></tr><tr><td rowspan="1" colspan="1"><italic>A. thaliana</italic>, recombinant from transgenic
tobacco</td><td rowspan="1" colspan="1">1.3</td><td rowspan="1" colspan="1">0.87</td><td rowspan="1" colspan="1">78</td><td rowspan="1" colspan="1">11</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">[59]</td></tr><tr><td rowspan="1" colspan="1"><italic>A. thaliana</italic>, recombinant from transgenic tobacco +
thermal treatment for 5 min at 60<sup>o</sup>C</td><td rowspan="1" colspan="1">0.1</td><td rowspan="1" colspan="1">0.07</td><td rowspan="1" colspan="1">35</td><td rowspan="1" colspan="1">3.3</td><td rowspan="1" colspan="1">ND</td><td rowspan="1" colspan="1">ND</td><td rowspan="1" colspan="1">[59]</td></tr><tr><td rowspan="1" colspan="1"><italic>A. thaliana</italic>, from mitochondria from leaves</td><td rowspan="1" colspan="1">1.9</td><td rowspan="1" colspan="1">1.27</td><td rowspan="1" colspan="1">34</td><td rowspan="1" colspan="1">1.4</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">[60]</td></tr><tr><td rowspan="1" colspan="1"><italic>A. thaliana</italic>, recombinant from<italic>E.
coli</italic></td><td rowspan="1" colspan="1">6.5</td><td rowspan="1" colspan="1">3.8</td><td rowspan="1" colspan="1">20</td><td rowspan="1" colspan="1">2.8</td><td rowspan="1" colspan="1">10</td><td rowspan="1" colspan="1">5.0 × 10<sup>-5</sup></td><td rowspan="1" colspan="1">[58]</td></tr><tr><td rowspan="1" colspan="1">Pea (seeds)
<italic>Pisum sativum</italic></td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">22</td><td rowspan="1" colspan="1">2 [61]1.67; 6.25 [62]</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">[61, 62]</td></tr><tr><td rowspan="1" colspan="1">Mung bean,<italic>Phaseolus aureus, </italic>native</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">7.2</td><td rowspan="1" colspan="1">1.6</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">[63]</td></tr><tr><td rowspan="1" colspan="1">Soybean,<italic>G. max</italic>, native</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">5.7</td><td rowspan="1" colspan="1">0.6</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">[57]</td></tr><tr><td rowspan="1" colspan="1">Soybean,<italic>G. max</italic>, recombinant</td><td rowspan="1" colspan="1">4.0</td><td rowspan="1" colspan="1">2.83 [64]</td><td rowspan="1" colspan="1">13.2</td><td rowspan="1" colspan="1">1.5</td><td rowspan="1" colspan="1">1</td><td rowspan="1" colspan="1">8.7 × 10<sup>-4</sup></td><td rowspan="1" colspan="1">[58, 64, 76]</td></tr><tr><td rowspan="1" colspan="1">Lotus japonicus</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">1.2 (NAD<sup>+</sup>)0.005 (NADP<sup>+</sup>)</td><td rowspan="1" colspan="1">29.5</td><td rowspan="1" colspan="1">6.1</td><td rowspan="1" colspan="1">29.5</td><td rowspan="1" colspan="1">3.7 × 10<sup>-6</sup></td><td rowspan="1" colspan="1">[10]</td></tr><tr><td rowspan="1" colspan="1">Spinach,<italic>Spinacia oleracea L.</italic>, from leaves</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">1.7</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">[16]</td></tr><tr><td rowspan="1" colspan="1">Potato
<italic>Solanum tuberosum</italic></td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">19</td><td rowspan="1" colspan="1">0.54</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">[29]</td></tr><tr><td rowspan="1" colspan="1"><italic>C. boidinii</italic>,wild-type</td><td rowspan="1" colspan="1">6.3</td><td rowspan="1" colspan="1">3.7</td><td rowspan="1" colspan="1">37</td><td rowspan="1" colspan="1">5.9</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">[65]</td></tr><tr><td rowspan="1" colspan="1"><italic>C. metillica, </italic>wild-type</td><td rowspan="1" colspan="1">2.1</td><td rowspan="1" colspan="1">1.4</td><td rowspan="1" colspan="1">55</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">< 4 × 10<sup>-6</sup></td><td rowspan="1" colspan="1">[66]</td></tr><tr><td rowspan="1" colspan="1"><italic>Saccharomyces cerevisiae</italic>, recombinant</td><td rowspan="1" colspan="1">10</td><td rowspan="1" colspan="1">6.5</td><td rowspan="1" colspan="1">36</td><td rowspan="1" colspan="1">5.5</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">< 3.3 × 10<sup>-10</sup></td><td rowspan="1" colspan="1">[67, 68]</td></tr><tr><td rowspan="1" colspan="1">Burkholderia stabilis</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">1.66 (NAD<sup>+</sup>)4.75 (NADP<sup>+</sup>)</td><td rowspan="1" colspan="1">1430</td><td rowspan="1" colspan="1">55.5</td><td rowspan="1" colspan="1">0.16</td><td rowspan="1" colspan="1">25.0</td><td rowspan="1" colspan="1">[51]</td></tr><tr><td rowspan="1" colspan="1"><italic>Moraxella </italic>sp. C2, recombinant</td><td rowspan="1" colspan="1">10.0</td><td rowspan="1" colspan="1">7.3</td><td rowspan="1" colspan="1">80</td><td rowspan="1" colspan="1">7.5</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">[6]</td></tr><tr><td rowspan="1" colspan="1"><italic>Pseudomonas </italic>sp. 101</td><td rowspan="1" colspan="1">10.0</td><td rowspan="1" colspan="1">7.3</td><td rowspan="1" colspan="1">60</td><td rowspan="1" colspan="1">7</td><td rowspan="1" colspan="1">> 200</td><td rowspan="1" colspan="1">4.2 × 10<sup>-4</sup></td><td rowspan="1" colspan="1">[6]</td></tr></tbody></table><table-wrap-foot><fn id="TF2-0"><p>* NA – Data not available.</p></fn></table-wrap-foot></table-wrap><p>Plant enzymes are highly homologous (approximately 80%); the similarity between the
bacterial and plant FDHs is ~50%.</p></sec><sec><title>OBTAINMENT OF PLANT FORMATE DEHYDROGENASES</title><p>In plants, FDHs are localized in mitochondria; they therefore constitute a small part
of all soluble proteins within a cell, and the isolation of an enzyme directly from
plants is a labour-intensive and time-consuming procedure. Plant FDHs are mostly not
very stable, which results in an appreciably significant inactivation of the enzyme
during the extraction. Therefore, the specific activity of the resulting FDH
specimens is much lower than one may expect ( <italic><xref ref-type="table" rid="T2">Table 2</xref></italic> ). The purified plant FDH was first
obtained in 1951 from pea and French bean [<xref ref-type="bibr" rid="R13">13</xref>]. In 1983, FDH was extracted from soybean <italic>G.max</italic> in
appreciably large amounts; this enabled the determination of the amino acid
composition of plant formate dehydrogenase [<xref ref-type="bibr" rid="R57">57</xref>]. </p><p>Since 1993 several cDNA of plant FDH have been cloned: in 1993 – from potato
[<xref ref-type="bibr" rid="R21">21</xref>], in 1998 – from barley [<xref ref-type="bibr" rid="R8">8</xref>], in 2000 – from rice [<xref ref-type="bibr" rid="R41">41</xref>] and <italic>A. thaliana</italic> [<xref ref-type="bibr" rid="R26">26</xref>, <xref ref-type="bibr" rid="R27">27</xref>].
Transgenic <italic>A. thaliana</italic> and tobacco plants expressing AthFDH were
developed [<xref ref-type="bibr" rid="R28">28</xref>]; however, the yield of the
enzyme was not very high. The expression of full size cDNA of potato FDH in
<italic>Escherichia coli </italic> cells yielded insoluble inclusion bodies
[<xref ref-type="bibr" rid="R21">21</xref>]. </p><p>The active and soluble recombinant formate dehydrogenase from plants was first
obtained in <italic>E. coli </italic> cells, [<xref ref-type="bibr" rid="R41">41</xref>]; however, the protein content was very low, approximately 0.01% of
all soluble proteins within the cell. In our laboratory, we obtained <italic>E. coli
</italic> strains, which are superproducers of active FDHs from
<italic>A. thaliana</italic> (AthFDH) and soybean <italic>G. max</italic>(isoenzyme SoyFDH2) with an enzyme content attaining 40% of all soluble proteins in
the cell [<xref ref-type="bibr" rid="R58">58</xref>] (the gene of soybean FDH was
kindly provided by Professor N. Labrou from the Agricultural University of Athens
(Greece); the FDH gene from <italic>A. thaliana</italic> , by Professor J. Markwell
from the University of Nebraska (Lincoln, USA)). There is no system of transport to
mitochondria in <italic>E. coli </italic> cells; therefore, in order to obtain the
“natural enzyme”, we deleted the sequences encoding the signal peptide
from the cDNA [<xref ref-type="bibr" rid="R58">58</xref>]. After the optimization of
the cultivation conditions, the yield of recombinant FDH from
<italic>A. thaliana</italic> and soybean <italic>G. max </italic> reached
500–600 mg/l of the medium [<xref ref-type="bibr" rid="R6">6</xref>]. A
procedure was developed which enabled the obtaining of several hundred milligrams of
homogenous FDH specimen via a single chromatographic stage per extraction run. Thus,
all necessary conditions for the performance of systematic studies of FDHs from
<italic>A. thaliana</italic> and soybean <italic>G. max</italic> were provided,
including genetic engineering experiments and X-ray diffraction determination of the
structure. The experiments were successfully carried out for the expression of FDH
from <italic>L. japonicas </italic> in <italic>E. coli </italic> cells [<xref ref-type="bibr" rid="R10">10</xref>]. </p></sec><sec><title>KINETIC PROPERTIES OF PLANT FORMATE DEHYDROGENASE</title><p><italic><xref ref-type="table" rid="T2">Table 2</xref></italic> summarizes the
kinetic properties of natural and recombinant plant FDHs. The characteristics of the
most thoroughly studied bacterial and yeast enzymes are provided for comparative
purposes. Several major conclusions can be drawn from the data in <italic><xref ref-type="table" rid="T2">Table 2</xref></italic> : </p><p>1. It is clearly visible that in case of FDH from <italic>A. thaliana </italic> the
multistage extraction of the natural enzyme is accompanied by a considerable loss in
activity. The specific activity of the specimens, even those obtained from
transgenic plants, is several times lower than the activity of recombinant AthFDH
expressed in <italic>E. coli</italic> cells. It is noteworthy that AthFDH belongs to
stable FDHs. In terms of thermal stability, it is even superior to FDH from
<italic>Moraxella </italic> sp. C2 and yeast <italic>C. boidinii</italic> (
<italic><xref ref-type="table" rid="T3">Table 3</xref></italic> ). It is
obvious that the degree of inactivation of less stable, FDHs (in particular, in the
case of SoyFDH) being extracted from natural sources will be higher. This fact
should be taken into consideration when analysing formate dehydrogenase activity in
plants. </p><p>2. The specific activity of recombinant AthFDH and SoyFDH is comparable with that of
formate dehydrogenases from microorganisms; although it is inferior to FDHs from
methylotrophic bacteria and baker’s yeast. As previously mentioned, a partial
inactivation of enzymes may occur during the extraction; therefore, calculation of
the catalytic constant based on the values of specific activity and molecular weight
may give underestimated <italic>k</italic><sub>cat</sub> values. This fact is of particular significance for SoyFDH, the
thermal stability of which is much lower than that of other FDHs (see the thermal
stability section below). Therefore, we developed a procedure for determining the
concentration of active sites of recombinant SoyFDH based on the quenching of the
intrinsic fluorescence of the enzyme as it is titrated with azide ion in the
presence of coenzyme NAD <sup>+</sup> [<xref ref-type="bibr" rid="R64">64</xref>].
The azide ion is a strong competitive inhibitor of SoyFDH (K <italic>I</italic> = 3.6 × 10 <sup>-7</sup> M). Therefore, a linear dependence of quenching of FDH
fluorescence on the azide concentration is observed under the conditions ensuring
the equimolar binding of enzyme and inhibitor. The <italic>k</italic><sub>cat </sub> value determined from these experiments actually coincided with that
calculated using the specific activity and molecular weight. The obtained data
attest to the fact that despite the low thermal stability, SoyFDH extracted using
the designed procedure is not inactivated. Today, this procedure is being actively
used for determining the <italic>k</italic><sub>cat </sub> values of the mutant forms of SoyFDH. </p><table-wrap id="T3" orientation="portrait" position="float"><label>Table 3</label><caption><p> Parameters of thermal inactivation of formate dehydrogenases from different
sources </p></caption><table frame="hsides" rules="groups"><thead><tr><th rowspan="2" colspan="1">FDH source</th><th colspan="2" rowspan="1">Kinetics of thermal inactivation*</th><th colspan="3" rowspan="1">Differential scanning calorimetry* [<xref ref-type="bibr" rid="R72">72</xref>]</th></tr><tr><th rowspan="1" colspan="1">Δ<italic>H</italic><sup>≠</sup>kJ/mol</th><th rowspan="1" colspan="1">Δ<italic>S</italic><sup>≠</sup>, J/(mol·K)</th><th rowspan="1" colspan="1"><italic>C</italic><sub>p</sub>, kJ/mol</th><th rowspan="1" colspan="1"><italic>T</italic><sub>m</sub>,<sup>o</sup>C</th><th rowspan="1" colspan="1"><italic>T</italic><sub>1/2</sub>,<sup>o</sup>C</th></tr></thead><tbody><tr><td rowspan="1" colspan="1"><italic>Pseudomonas sp. 101</italic></td><td rowspan="1" colspan="1">540 [<xref ref-type="bibr" rid="R6">6</xref>]</td><td rowspan="1" colspan="1">1320 [<xref ref-type="bibr" rid="R6">6</xref>]</td><td rowspan="1" colspan="1">2060</td><td rowspan="1" colspan="1">67.6</td><td rowspan="1" colspan="1">5.4</td></tr><tr><td rowspan="1" colspan="1"><italic>Moraxella sp. C2</italic></td><td rowspan="1" colspan="1">NA**</td><td rowspan="1" colspan="1">NA**</td><td rowspan="1" colspan="1">1830</td><td rowspan="1" colspan="1">63.4</td><td rowspan="1" colspan="1">4.9</td></tr><tr><td rowspan="1" colspan="1"><italic>Candida boidinii</italic></td><td rowspan="1" colspan="1">480 [<xref ref-type="bibr" rid="R77">77</xref>]</td><td rowspan="1" colspan="1">1250 [<xref ref-type="bibr" rid="R77">77</xref>]</td><td rowspan="1" colspan="1">1730</td><td rowspan="1" colspan="1">64.4</td><td rowspan="1" colspan="1">5.3</td></tr><tr><td rowspan="1" colspan="1"><italic>Saccharomyces cerevisiae</italic></td><td rowspan="1" colspan="1">420 [<xref ref-type="bibr" rid="R67">67</xref>]</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1">820</td><td rowspan="1" colspan="1">46.4</td><td rowspan="1" colspan="1">3.2</td></tr><tr><td rowspan="1" colspan="1"><italic>Arabidopsis thaliana</italic></td><td rowspan="1" colspan="1">490 [<xref ref-type="bibr" rid="R6">6</xref>]</td><td rowspan="1" colspan="1">1200 [<xref ref-type="bibr" rid="R6">6</xref>]</td><td rowspan="1" colspan="1">1330</td><td rowspan="1" colspan="1">64.9</td><td rowspan="1" colspan="1">5.9</td></tr><tr><td rowspan="1" colspan="1"><italic>Glycine max</italic></td><td rowspan="1" colspan="1">370 [<xref ref-type="bibr" rid="R76">76</xref>]</td><td rowspan="1" colspan="1">860 [<xref ref-type="bibr" rid="R76">76</xref>]</td><td rowspan="1" colspan="1">820</td><td rowspan="1" colspan="1">57.1</td><td rowspan="1" colspan="1">7.5</td></tr></tbody></table><table-wrap-foot><fn id="TF3-0"><p>* All measurements were carried out in the 0.1 M phosphate buffer,
pH 7.0</p></fn><fn id="TF3-1"><p>** Data not available</p></fn></table-wrap-foot></table-wrap><p>3. Plant FDHs are characterized by significantly lower values of the Michaelis
constants with respect to both formate and coenzyme NAD <sup>+</sup> in comparison
with the bacterial and yeast enzymes. It is very important for the practical
application of FDH. Today, recombinant FDHs from <italic>Pseudomonas</italic> sp. 101 and <italic>C. boidinii</italic> , whose chemical and thermal stability
have been enhanced by protein engineering methods, are used for the regeneration of
the reduced coenzyme (NADH or NADPH) in the synthesis of chiral compounds using
dehydrogenases [<xref ref-type="bibr" rid="R6">6</xref>]. </p><p>4. Almost all FDH that have been studied are highly specific to the coenzyme NAD
<sup>+</sup> . Their catalytic activity in the reaction with NAD <sup>+ </sup>is higher than that in the reaction with NADP <sup>+</sup> by a factor of 2500
(PseFDH) to 3 × 10 <sup>9</sup> . The exception is the recently described FDH from
pathogenic bacteria <italic>Burkholderia stabilis</italic> , which is
twenty-six-fold more efficient in the reaction with NADP <sup>+</sup> in comparison
with NAD <sup>+</sup> [<xref ref-type="bibr" rid="R51">51</xref>]. It should be
noted that the mutant PseFDH, whose coenzyme specificity changed from NAD
<sup>+</sup> to NADP <sup>+</sup> , was obtained as early as in 1993 [<xref ref-type="bibr" rid="R6">6</xref>, <xref ref-type="bibr" rid="R68">68</xref>];
this enzyme has been successfully used for NADPH regeneration [<xref ref-type="bibr" rid="R69">69</xref>, <xref ref-type="bibr" rid="R70">70</xref>]. Having the
lowest <italic>К</italic><sub>m </sub> value with respect to NADP <sup>+ </sup> among all NAD <sup>+</sup>-specific wild-type FDHs, SoyFDH has a huge potential for obtaining the NADP
<sup>+</sup> -specific enzyme [<xref ref-type="bibr" rid="R58">58</xref>] (
<italic><xref ref-type="table" rid="T2">Table 2</xref></italic> ). </p></sec><sec><title>THERMAL STABILITY OF PLANT FORMATE DEHYDROGENASES</title><p>Prior to obtaining recombinant AthFDH and SoyFDH in <italic>E. coli </italic> cells,
no systematic studies on the thermal stability of plant FDHs were performed.
According to [<xref ref-type="bibr" rid="R59">59</xref>], the values of К
<sub>M</sub> with respect to formate and NAD <sup>+</sup> decrease after the
incubation of transgenic AthFDH for 5 min at 60°С; however, the specific
activity value decreased by 13 times. We performed systematic studies of the thermal
stability of recombinant AthFDH and SoyFDH using two approaches: determining the
kinetics of thermal inactivation and the differential scanning calorimetry [<xref ref-type="bibr" rid="R71">71</xref>, <xref ref-type="bibr" rid="R72">72</xref>].
It was revealed that the thermal inactivation of plant FDHs occurred via a
monomolecular mechanism, similar to the FDHs from bacteria and yeasts. Time
dependences of decrease in the activity of AthFDH and SoyFDH are described by the
kinetics of the first-order reaction, the observed constant of inactivation rate was
independent of enzyme concentration. The thermal stabilities of AthFDH and SoyFDH
strongly differ. AthFDH lost 50% of its activity after 20 min at 59.5°С,
whereas SoyFDH lost 50% of its activity at 52.8°С. The difference by almost
7°С corresponds to a difference in the inactivation rate constants of more
than 1000 times. AthFDH is actually inferior in terms of its thermal stability only
to FDH from <italic>Pseudomonas </italic> sp. 101 (63.0°С, the most stable FDH
among the known ones) [<xref ref-type="bibr" rid="R6">6</xref>] and
<italic>Staphylococcus aureus</italic> (62.0°С) and is superior to all
known microbial formate dehydrogenases. In contrast, SoyFDH is inferior in terms of
stability to all known FDHs, with the exception of the enzyme from baker’s
yeast that is characterized by another inactivation mechanism. The temperature
dependences of the rate constants of inactivation of AthFDH and SoyFDH are described
by the transition state theory. The calculated values of activation enthalpy Δ
<italic>H <sup>≠</sup></italic> and activation entropy Δ <italic>S <sup>≠ </sup></italic> are listed in <italic><xref ref-type="table" rid="T3">Table 3</xref>. </italic> It can be noticed that
thermal stability of formate dehydrogenases correlates well with the Δ
<italic>H <sup>≠</sup></italic> and Δ <italic>S <sup>≠ </sup></italic> values. The highest values are typical of the most stable PseFDH, whereas
the lowest ones refer to SoyFDH. </p><fig id="F4" orientation="portrait" position="float"><label>Fig. 4</label><caption><p> The structures of apo-(A) and holo-(B) forms of FDH from
<italic>A. thaliana.</italic> Figures were obtained using PDB structures
3JTM and 3N7U, respectively. In the structure of the holo-form, the
molecules of NAD <sup>+</sup> and azide ion are highlighted in magenta and
red, respectively. </p></caption><graphic xlink:href="AN20758251-11-038-g004"></graphic></fig><p>The results of experiments studying the thermal stability of plant FDHs using
differential scanning calorimetry are in close agreement with the data of
inactivation kinetics. In <italic><xref ref-type="table" rid="T3">Table 3</xref></italic> the values of the temperature and heat of the phase transition are shown.
All investigated FDHs are characterized by their high cooperativity of the
denaturation process. PseFDH is characterized by the highest melting point, whereas
this value is lower by a factor of 2.5 for SoyFDH. The melting point of AthFDH is
higher than that of CboFDH and MorFDH. </p><p>Experiments on enhancing the thermal stability of recombinant SoyFDH using genetic
engineering techniques are currently being performed.</p></sec><sec><title>CHEMICAL STABILITY OF PLANT FORMATE DEHYDROGENASES</title><p>FDH has been actively used in the process of synthesizing optically active compounds
catalyzed by dehydrogenases. In these processes, the operational stability (the
operating time of an enzyme) plays the greatest role. Under conditions of
biocatalytic process, the inactivation of FDH is associated with either oxidation
with oxygen or chemical modification of sulfhydryl groups of the enzyme. The
operational stability of PseFDH and CboFDH was enhanced by site-directed mutagenesis
of two Cys residues [<xref ref-type="bibr" rid="R6">6</xref>, <xref ref-type="bibr" rid="R65">65</xref>]. As previously mentioned, the synthesis of FDHs in plants
increased under various stress factors. The concentration of active forms of oxygen
(superoxide radicals, hydrogen peroxide, etc.) is likely to increase in a cell under
the same conditions. It should be expected that in order to ensure high activity
under stress, plant FDHs should be far more resistant to the action of these agents
than formate dehydrogenases functioning under non-stress conditions. In order to
verify this hypothesis, the kinetics of inactivation of recombinant AthFDH, SoyFDH,
PseFDH, FDH from wild-type <italic>S. aureus</italic> (SauFDH) and three mutant
PseFDH, where one or two Cys residues were replaced, under the action of hydrogen
peroxide was studied. FDH from <italic>S. aureus </italic> is a stress protein as
well, since the biosynthesis of this enzyme increases by 20 times when staphylococci
pass from planktonic growth to biofilm formation [<xref ref-type="bibr" rid="R73">73</xref>]. It was revealed that the inactivation rate of AthFDH and SoyFDH
under the action of Н <sub>2</sub> О <sub>2</sub> is virtually equal and
is 18 times lower than that in wild-type PseFDH. Under the same conditions, the
stability of SauFDH was sixfold higher than that in plant enzymes [<xref ref-type="bibr" rid="R74">74</xref>]. PseFDH with the stability identical to
that of SoyFDH was successfully obtained only after double Cys145Ser/Cys255/Ala
replacement. It was thus demonstrated that plant and bacterial FDHs synthesized
under stress impact indeed possess a higher chemical stability than formate
dehydrogenases, whose synthesis is induced by other factors. Moreover, studying the
thermal inactivation of formate dehydrogenase in the presence of hydrogen peroxide
can be used to comparatively assess the <italic> in vivo</italic> chemical stability
of FDHs. </p></sec><sec><title>STRUCTURAL STUDIES OF PLANT FORMATE DEHYDROGENASES</title><p>FDH has not been well studied from a structural perspective. Until recently, only the
FDH structures from three sources, namely, bacteria <italic>Pseudomonas</italic> sp. 101 and <italic>Moraxella</italic> sp. C2 (unbound enzyme, and the
enzyme–NAD <sup>+</sup> –azide ternary complex) and <italic>C. boidinii
</italic> yeast (structures of two mutant forms of an apoenzyme) were deposited into
the protein data bank (PDB). In case of formate dehydrohenases, free enzyme is in
its «open» conformation. When the FDH–NAD <sup>+</sup> –azide ternary
complex is formed (its structure being considered similar to that of the enzyme in
the transition state), a considerable compacting of the protein globule occurs, and
FDH is transformed into the «closed» state. The development of a highly efficient
system of expression of AthFDH and SoyFDH <italic>in E. coli</italic> cells enabled
the transition to their crystallization and identification of their structure.,
Nowadays AthFDH structures both in open and closed conformations (3NAQ and 3N7U,
with resolution of 1.7 and 2.0 Å, respectively) have been identified. Enzyme
crystals were produced in space [<xref ref-type="bibr" rid="R75">75</xref>] in order
to obtain AthFDH structure in open conformation with higher resolution (3JTM,
1.3 Å), <italic>Fig.</italic> 4 shows the structures of apo- and holoFDHs (the open
and closed conformations, respectively). A more detailed analysis of these
structures will be provided in individual articles. The crystals of the
SoyFDH–NAD <sup>+</sup> –azide ternary complex of FDH from soybean
<italic>G. max</italic> have been obtained both on the Earth and in space. The
structures of these complexes were identified with resolution of 1.9 Å; the
deposition of these structures into the PDB data bank is in progress. </p></sec><sec sec-type="conclusions"><title>CONCLUSIONS</title><p>Both our own and the published data attest to the fact that plant FDHs are extremely
significant, in particular when responding to stress factors. Biosynthesis
regulation and the physiological role of FDHs are diverse and complex; they have not
been completely elucidated thus far. The systematic investigation of the structure
and function of these enzymes is still in its infancy. The results of these studies
are of significant interest to fundamental science and are of great practical
importance. Production of mutant forms of FDH with a high activity opens a new
approach for the design of plants with an enhanced resistance to unfavourable
factors. More active mutant enzymes will supply the cell with the energy required to
more efficiently overcome unfavourable effects of stress with the same expression
level of FDH. Soybean FDH is also considered to be an exceptionally promising FDH
for the design of a highly efficient biocatalyst for NAD(P)H regeneration in the
synthesis of optically active compounds using dehydrogenases. The natural enzyme is
notable for its high operational stability and has one of the lowest values of the
Michaelis constant with respect both to NAD <sup>+</sup> and formate among all of
the known FDHs. However, in order to practically implement SoyFDH, its catalytic
activity and thermal stability need to be enhanced. We are currently performing
active research in this direction. </p></sec></body><back><ack><p>This study was supported by the Ministry of Education and Science of the Russian
Federation (State Contract № 16.512.11.2148) and the Russian Foundation for
Basic Research (grant № 11-04-00920).</p></ack><glossary><def-list><title>Abbreviations</title><term-head>Abbreviation</term-head><def-head>Expansion</def-head><def-item><term id="G1">FDH</term><def><p>formate dehydrogenase</p></def></def-item><def-item><term id="G2">PseFDH, CboFDH</term><def><p>formate dehydrogenases from bacteria<italic>Pseudomonas</italic>sp</p></def></def-item><def-item><term id="G3">101 and yeast<italic>Candida boidinii</italic>,
respectively<italic>;</italic>SoyFDH,<italic></italic>AthFDH</term><def><p>plant formate dehydrogenases from soybean<italic>Glycine
max</italic>and<italic>Arabidopsis thaliana</italic>,
respectively</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>Rodionov</surname><given-names>Yu.V.</given-names></name><source>Uspekhi microbiologii.</source><volume>16</volume><year>1982</year><fpage>104</fpage><lpage>138</lpage></element-citation></ref><ref id="R2"><label>2</label><element-citation publication-type="journal"><name><surname>Ferry</surname><given-names>J.G.</given-names></name><source>FEMS Microbiol. Rev.</source><volume>7</volume><year>1990</year><fpage>377</fpage><lpage>382</lpage><pub-id pub-id-type="pmid">2094290</pub-id></element-citation></ref><ref id="R3"><label>3</label><element-citation publication-type="journal"><name><surname>Vinals</surname><given-names>C.</given-names></name><name><surname>Depiereux</surname><given-names>E.</given-names></name><name><surname>Feytmans</surname><given-names>E.</given-names></name><source>Biochem. Biophys. Res. Commun.</source><volume>192</volume><year>1993</year><fpage>182</fpage><lpage>188</lpage><pub-id pub-id-type="pmid">8476420</pub-id></element-citation></ref><ref id="R4"><label>4</label><element-citation publication-type="journal"><name><surname>Tishkov</surname><given-names>V.I.</given-names></name><name><surname>Galkin</surname><given-names>A.G.</given-names></name><name><surname>Egorov</surname><given-names>A.M.</given-names></name><source>Biochimie.</source><volume>71</volume><year>1989</year><issue>4</issue><fpage>551</fpage><lpage>557</lpage><pub-id pub-id-type="pmid">2503060</pub-id></element-citation></ref><ref id="R5"><label>5</label><element-citation publication-type="journal"><name><surname>Tishkov</surname><given-names>V.I.</given-names></name><name><surname>Popov</surname><given-names>V.O.</given-names></name><source>Biochemistry (Mosc.)</source><volume>69</volume><fpage>1252</fpage><lpage>1267</lpage><pub-id pub-id-type="pmid">15627379</pub-id></element-citation></ref><ref id="R6"><label>6</label><element-citation publication-type="journal"><name><surname>Tishkov</surname><given-names>V.I.</given-names></name><name><surname>Popov</surname><given-names>V.O.</given-names></name><source>Biomol. Eng.</source><volume>23</volume><year>2006</year><fpage>89</fpage><lpage>110</lpage><pub-id pub-id-type="pmid">16546445</pub-id></element-citation></ref><ref id="R7"><label>7</label><element-citation publication-type="journal"><name><surname>Hourton-Cabassa</surname><given-names>C.</given-names></name><name><surname>Ambard-Bretteville</surname><given-names>F.</given-names></name><name><surname>Moreau</surname><given-names>F.</given-names></name><name><surname>Davy de Virville</surname><given-names>J.</given-names></name><name><surname>Remy</surname><given-names>R.</given-names></name><name><surname>Colas des Francs-Small</surname><given-names>C.</given-names></name><source>Plant Physiol.</source><volume>116</volume><year>1998</year><fpage>627</fpage><lpage>635</lpage><pub-id pub-id-type="pmid">9490763</pub-id></element-citation></ref><ref id="R8"><label>8</label><element-citation publication-type="journal"><name><surname>Suzuki</surname><given-names>K.</given-names></name><name><surname>Itai</surname><given-names>R.</given-names></name><name><surname>Suzuki</surname><given-names>K.</given-names></name><name><surname>Nakanishi</surname><given-names>H.</given-names></name><name><surname>Nishizawa</surname><given-names>N.-K.</given-names></name><name><surname>Yoshimura</surname><given-names>E.</given-names></name><name><surname>Mori</surname><given-names>S.</given-names></name><source>Plant Physiol.</source><volume>116</volume><year>1998</year><fpage>725</fpage><lpage>732</lpage><pub-id pub-id-type="pmid">9489019</pub-id></element-citation></ref><ref id="R9"><label>9</label><element-citation publication-type="journal"><name><surname>Thompson</surname><given-names>P.</given-names></name><name><surname>Bowsher</surname><given-names>C.G.</given-names></name><name><surname>Tobin</surname><given-names>A.K.</given-names></name><source>Plant Physiol.</source><volume>118</volume><year>1998</year><fpage>1089</fpage><lpage>1099</lpage><pub-id pub-id-type="pmid">9808754</pub-id></element-citation></ref><ref id="R10"><label>10</label><element-citation publication-type="journal"><name><surname>Andreadeli</surname><given-names>A.</given-names></name><name><surname>Flemetakis</surname><given-names>E.</given-names></name><name><surname>Axarli</surname><given-names>I.</given-names></name><name><surname>Dimou</surname><given-names>M.</given-names></name><name><surname>Udvardi</surname><given-names>M.K.</given-names></name><name><surname>Katinakis</surname><given-names>P.</given-names></name><name><surname>Labrou</surname><given-names>N.E.</given-names></name><source>Biochim. Biophys. Acta.</source><volume>1794</volume><year>2009</year><fpage>976</fpage><lpage>984</lpage><pub-id pub-id-type="pmid">19281876</pub-id></element-citation></ref><ref id="R11"><label>11</label><element-citation publication-type="journal"><name><surname>David</surname><given-names>P.</given-names></name><name><surname>Colas des Francs-Small</surname><given-names>C.</given-names></name><name><surname>Sevignac</surname><given-names>M.</given-names></name><name><surname>Thareau</surname><given-names>V.</given-names></name><name><surname>Macadre</surname><given-names>C.</given-names></name><name><surname>Langin</surname><given-names>T.</given-names></name><name><surname>Geffroy</surname><given-names>V.</given-names></name><source>Theor. Appl. Genet.</source><volume>121</volume><year>2010</year><fpage>87</fpage><lpage>103</lpage><pub-id pub-id-type="pmid">20182695</pub-id></element-citation></ref><ref id="R12"><label>12</label><element-citation publication-type="journal"><name><surname>Thunberg</surname><given-names>T.</given-names></name><source>Arch. Physiol. Biochem.</source><volume>18</volume><year>1921</year><fpage>601</fpage><lpage>606</lpage></element-citation></ref><ref id="R13"><label>13</label><element-citation publication-type="journal"><name><surname>Davison</surname><given-names>D.C.</given-names></name><source>Biochem. J.</source><volume>49</volume><year>1951</year><fpage>520</fpage><lpage>526</lpage><pub-id pub-id-type="pmid">14886318</pub-id></element-citation></ref><ref id="R14"><label>14</label><element-citation publication-type="journal"><name><surname>Davies</surname><given-names>D.D.</given-names></name><source>J. Exp. Bot.</source><volume>7</volume><year>1956</year><fpage>203</fpage><lpage>218</lpage></element-citation></ref><ref id="R15"><label>15</label><element-citation publication-type="journal"><name><surname>Mazelis</surname><given-names>M.</given-names></name><source>Plant Physiol.</source><volume>35</volume><year>1960</year><fpage>386</fpage><lpage>391</lpage><pub-id pub-id-type="pmid">16655361</pub-id></element-citation></ref><ref id="R16"><label>16</label><element-citation publication-type="journal"><name><surname>Halliwell</surname><given-names>B.</given-names></name><source>Biochem. J.</source><volume>138</volume><year>1974</year><fpage>77</fpage><lpage>85</lpage><pub-id pub-id-type="pmid">4840839</pub-id></element-citation></ref><ref id="R17"><label>17</label><element-citation publication-type="journal"><name><surname>Jansch</surname><given-names>L.</given-names></name><name><surname>Kruft</surname><given-names>V.</given-names></name><name><surname>Schmitz</surname><given-names>U.K.</given-names></name><name><surname>Braun</surname><given-names>H.-P.</given-names></name><source>Plant J.</source><volume>9</volume><year>1996</year><issue>3</issue><fpage>357</fpage><lpage>368</lpage><pub-id pub-id-type="pmid">8919912</pub-id></element-citation></ref><ref id="R18"><label>18</label><element-citation publication-type="journal"><name><surname>Oliver</surname><given-names>D.J.</given-names></name><source>Plant Physiol.</source><volume>68</volume><year>1981</year><fpage>703</fpage><lpage>705</lpage><pub-id pub-id-type="pmid">16661983</pub-id></element-citation></ref><ref id="R19"><label>19</label><element-citation publication-type="journal"><name><surname>Hanson</surname><given-names>A.D.</given-names></name><name><surname>Nelsen</surname><given-names>C.E.</given-names></name><source>Plant Physiol.</source><volume>62</volume><year>1978</year><fpage>305</fpage><lpage>312</lpage><pub-id pub-id-type="pmid">16660507</pub-id></element-citation></ref><ref id="R20"><label>20</label><element-citation publication-type="journal"><name><surname>Colas des Francs-Small</surname><given-names>C.</given-names></name><name><surname>Ambard-Bretteville</surname><given-names>F.</given-names></name><name><surname>Darpas</surname><given-names>A.</given-names></name><name><surname>Sallantin</surname><given-names>M.</given-names></name><name><surname>Huet</surname><given-names>J.-C.</given-names></name><name><surname>Pernollet</surname><given-names>J.-C.</given-names></name><name><surname>Remy</surname><given-names>R.</given-names></name><source>Plant Physiol.</source><volume>98</volume><year>1992</year><fpage>273</fpage><lpage>278</lpage><pub-id pub-id-type="pmid">16668624</pub-id></element-citation></ref><ref id="R21"><label>21</label><element-citation publication-type="journal"><name><surname>Colas des Francs-Small</surname><given-names>C.</given-names></name><name><surname>Ambard-Bretteville</surname><given-names>F.</given-names></name><name><surname>Small</surname><given-names>I.D.</given-names></name><name><surname>Remy</surname><given-names>R.</given-names></name><source>Plant Physiol.</source><volume>102</volume><year>1993</year><fpage>1171</fpage><lpage>1177</lpage><pub-id pub-id-type="pmid">8278546</pub-id></element-citation></ref><ref id="R22"><label>22</label><element-citation publication-type="journal"><name><surname>Herbik</surname><given-names>A.</given-names></name><name><surname>Giritch</surname><given-names>A.</given-names></name><name><surname>Horstmann</surname><given-names>C.</given-names></name><name><surname>Becker</surname><given-names>R.</given-names></name><name><surname>Balzer</surname><given-names>H.-J.</given-names></name><name><surname>Baumlein</surname><given-names>H.</given-names></name><name><surname>Stephan</surname><given-names>U.W.</given-names></name><source>Plant Physiol.</source><volume>111</volume><year>1996</year><fpage>533</fpage><lpage>540</lpage><pub-id pub-id-type="pmid">8787027</pub-id></element-citation></ref><ref id="R23"><label>23</label><element-citation publication-type="journal"><name><surname>Dubos</surname><given-names>C.</given-names></name><name><surname>Plomion</surname><given-names>C.</given-names></name><source>Plant Mol. Biol.</source><volume>51</volume><year>2003</year><fpage>249</fpage><lpage>262</lpage><pub-id pub-id-type="pmid">12602883</pub-id></element-citation></ref><ref id="R24"><label>24</label><element-citation publication-type="journal"><name><surname>Minami</surname><given-names>A.</given-names></name><name><surname>Fujikawa</surname><given-names>S.</given-names></name><name><surname>Takezawa</surname><given-names>D.</given-names></name><source>J. Plant Physiol.</source><volume>160</volume><year>2003</year><fpage>475</fpage><lpage>483</lpage><pub-id pub-id-type="pmid">12806775</pub-id></element-citation></ref><ref id="R25"><label>25</label><element-citation publication-type="journal"><name><surname>Yin</surname><given-names>L.</given-names></name><name><surname>Lan</surname><given-names>Y.</given-names></name><name><surname>Zhu</surname><given-names>L.</given-names></name><source>Plant Mol. Biol.</source><volume>68</volume><year>2008</year><fpage>597</fpage><lpage>617</lpage><pub-id pub-id-type="pmid">18815891</pub-id></element-citation></ref><ref id="R26"><label>26</label><element-citation publication-type="journal"><name><surname>Fukusaki</surname><given-names>E.</given-names></name><name><surname>Ikeda</surname><given-names>T.</given-names></name><name><surname>Shiraishi</surname><given-names>T.</given-names></name><name><surname>Nishikawa</surname><given-names>T.</given-names></name><name><surname>Kobayashi</surname><given-names>A.</given-names></name><source>J. Biosci. Bioeng.</source><volume>90</volume><year>2000</year><fpage>691</fpage><lpage>693</lpage><pub-id pub-id-type="pmid">16232936</pub-id></element-citation></ref><ref id="R27"><label>27</label><element-citation publication-type="journal"><name><surname>Olson</surname><given-names>B.J.</given-names></name><name><surname>Skavdahl</surname><given-names>M.</given-names></name><name><surname>Ramberg</surname><given-names>H.</given-names></name><name><surname>Osterman</surname><given-names>J.C.</given-names></name><name><surname>Markwell</surname><given-names>J.</given-names></name><source>Plant Sci.</source><volume>159</volume><year>2000</year><fpage>205</fpage><lpage>212</lpage><pub-id pub-id-type="pmid">11074273</pub-id></element-citation></ref><ref id="R28"><label>28</label><element-citation publication-type="journal"><name><surname>Herman</surname><given-names>P.L.</given-names></name><name><surname>Ramberg</surname><given-names>H.</given-names></name><name><surname>Baack</surname><given-names>R.D.</given-names></name><name><surname>Markwell</surname><given-names>J.</given-names></name><name><surname>Osterman</surname><given-names>J.C.</given-names></name><source>Plant Sci.</source><volume>163</volume><year>2002</year><fpage>1137</fpage><lpage>1145</lpage></element-citation></ref><ref id="R29"><label>29</label><element-citation publication-type="journal"><name><surname>Ambard-Bretteville</surname><given-names>F.</given-names></name><name><surname>Sorin</surname><given-names>C.</given-names></name><name><surname>Rebeille</surname><given-names>F.</given-names></name><name><surname>Hourton-Cabassa</surname><given-names>C.</given-names></name><name><surname>Colas des Francs-Small</surname><given-names>C.</given-names></name><source>Plant Mol. Biol.</source><volume>52</volume><year>2003</year><fpage>1153</fpage><lpage>1168</lpage><pub-id pub-id-type="pmid">14682615</pub-id></element-citation></ref><ref id="R30"><label>30</label><element-citation publication-type="journal"><name><surname>Igamberdiev</surname><given-names>A.U.</given-names></name><name><surname>Bykova</surname><given-names>N.V.</given-names></name><name><surname>Kleczkowski</surname><given-names>L.A.</given-names></name><source>Plant Physiol. Biochem.</source><volume>37</volume><year>1999</year><issue>7</issue><fpage>503</fpage><lpage>513</lpage></element-citation></ref><ref id="R31"><label>31</label><element-citation publication-type="journal"><name><surname>Li</surname><given-names>R.</given-names></name><name><surname>Moore</surname><given-names>M.</given-names></name><name><surname>King</surname><given-names>J.</given-names></name><source>Plant Cell Physiol.</source><volume>44</volume><year>2003</year><issue>3</issue><fpage>233</fpage><lpage>241</lpage><pub-id pub-id-type="pmid">12668769</pub-id></element-citation></ref><ref id="R32"><label>32</label><element-citation publication-type="journal"><name><surname>Perales</surname><given-names>M.</given-names></name><name><surname>Eubel</surname><given-names>H.</given-names></name><name><surname>Heinemeyer</surname><given-names>J.</given-names></name><name><surname>Colaneri</surname><given-names>A.</given-names></name><name><surname>Zabaleta</surname><given-names>E.</given-names></name><name><surname>Braun</surname><given-names>H.P.</given-names></name><source>J. Mol. Biol.</source><volume>350</volume><year>2005</year><fpage>263</fpage><lpage>277</lpage><pub-id pub-id-type="pmid">15935378</pub-id></element-citation></ref><ref id="R33"><label>33</label><element-citation publication-type="journal"><name><surname>Bykova</surname><given-names>N.V.</given-names></name><name><surname>Egsgaard</surname><given-names>H.</given-names></name><name><surname>Miller</surname><given-names>I.M.</given-names></name><source>FEBS Lett.</source><volume>540</volume><year>2003</year><fpage>141</fpage><lpage>146</lpage><pub-id pub-id-type="pmid">12681497</pub-id></element-citation></ref><ref id="R34"><label>34</label><element-citation publication-type="journal"><name><surname>Bykova</surname><given-names>N.V.</given-names></name><name><surname>Stensballe</surname><given-names>A.</given-names></name><name><surname>Egsgaard</surname><given-names>H.</given-names></name><name><surname>Jensen</surname><given-names>O.N.</given-names></name><name><surname>Moller</surname><given-names>I.M.</given-names></name><source>J. Biol. Chem.</source><volume>278</volume><year>2003</year><fpage>26021</fpage><lpage>26030</lpage><pub-id pub-id-type="pmid">12714601</pub-id></element-citation></ref><ref id="R35"><label>35</label><element-citation publication-type="journal"><name><surname>Kruger</surname><given-names>A.</given-names></name><name><surname>Peskan-Berghofer</surname><given-names>T.</given-names></name><name><surname>Frettinger</surname><given-names>P.</given-names></name><name><surname>Herrmann</surname><given-names>S.</given-names></name><name><surname>Buscot</surname><given-names>F.</given-names></name><name><surname>Oelmuller</surname><given-names>R.</given-names></name><source>New Phytol.</source><volume>163</volume><year>2004</year><fpage>149</fpage><lpage>157</lpage></element-citation></ref><ref id="R36"><label>36</label><element-citation publication-type="journal"><name><surname>Bruggmann</surname><given-names>R.</given-names></name><name><surname>Abderhalden</surname><given-names>O.</given-names></name><name><surname>Reymond</surname><given-names>P.</given-names></name><name><surname>Dudler</surname><given-names>R.</given-names></name><source>Plant Mol. Biol.</source><volume>58</volume><year>2005</year><fpage>247</fpage><lpage>267</lpage><pub-id pub-id-type="pmid">16027977</pub-id></element-citation></ref><ref id="R37"><label>37</label><element-citation publication-type="journal"><name><surname>Giri</surname><given-names>A.P.</given-names></name><name><surname>Wunsche</surname><given-names>H.</given-names></name><name><surname>Mitra</surname><given-names>S.</given-names></name><name><surname>Zavala</surname><given-names>J.A.</given-names></name><name><surname>Muck</surname><given-names>A.</given-names></name><name><surname>Svatos</surname><given-names>A.</given-names></name><name><surname>Baldwin</surname><given-names>I.T.</given-names></name><source>Plant Physiol.</source><volume>142</volume><year>2006</year><fpage>1621</fpage><lpage>1641</lpage><pub-id pub-id-type="pmid">17028148</pub-id></element-citation></ref><ref id="R38"><label>38</label><element-citation publication-type="journal"><name><surname>Umezawa</surname><given-names>T.</given-names></name><name><surname>Sakurai</surname><given-names>T.</given-names></name><name><surname>Totoki</surname><given-names>Y.</given-names></name><name><surname>Toyoda</surname><given-names>A.</given-names></name><name><surname>Seki</surname><given-names>M.</given-names></name><name><surname>Ishiwata</surname><given-names>A.</given-names></name><name><surname>Akiyama</surname><given-names>K.</given-names></name><name><surname>Kurotani</surname><given-names>A.</given-names></name><name><surname>Yoshida</surname><given-names>T.</given-names></name><name><surname>Mochida</surname><given-names>K.</given-names></name><source>DNA Res.</source><volume>15</volume><year>2008</year><fpage>333</fpage><lpage>346</lpage><pub-id pub-id-type="pmid">18927222</pub-id></element-citation></ref><ref id="R39"><label>39</label><element-citation publication-type="journal"><name><surname>Kikuchi</surname><given-names>S.</given-names></name><name><surname>Satoh</surname><given-names>K.</given-names></name><name><surname>Nagata</surname><given-names>T.</given-names></name><name><surname>Kawagashira</surname><given-names>N.</given-names></name><name><surname>Doi</surname><given-names>K.</given-names></name><name><surname>Kishimoto</surname><given-names>N.</given-names></name><name><surname>Yazaki</surname><given-names>J.</given-names></name><name><surname>Ishikawa</surname><given-names>M.</given-names></name><name><surname>Yamada</surname><given-names>H.</given-names></name><name><surname>Ooka</surname><given-names>H.</given-names></name><source>Science.</source><volume>301</volume><year>2003</year><fpage>376</fpage><lpage>379</lpage><pub-id pub-id-type="pmid">12869764</pub-id></element-citation></ref><ref id="R40"><label>40</label><element-citation publication-type="journal"><name><surname>Liu</surname><given-names>X.</given-names></name><name><surname>Lu</surname><given-names>T.</given-names></name><name><surname>Yu</surname><given-names>S.</given-names></name><name><surname>Li</surname><given-names>Y.</given-names></name><name><surname>Huang</surname><given-names>Y.</given-names></name><name><surname>Huang</surname><given-names>T.</given-names></name><name><surname>Zhang</surname><given-names>L.</given-names></name><name><surname>Zhu</surname><given-names>J.</given-names></name><name><surname>Zhao</surname><given-names>Q.</given-names></name><name><surname>Fan</surname><given-names>D.</given-names></name><source>Plant Mol. Biol.</source><volume>65</volume><year>2007</year><fpage>403</fpage><lpage>415</lpage><pub-id pub-id-type="pmid">17522955</pub-id></element-citation></ref><ref id="R41"><label>41</label><element-citation publication-type="journal"><name><surname>Shiraishi</surname><given-names>T.</given-names></name><name><surname>Fukusaki</surname><given-names>E.</given-names></name><name><surname>Kobayashi</surname><given-names>A.</given-names></name><source>J. Biosci. Bioeng.</source><volume>89</volume><year>2000</year><fpage>241</fpage><lpage>246</lpage><pub-id pub-id-type="pmid">16232736</pub-id></element-citation></ref><ref id="R42"><label>42</label><element-citation publication-type="journal"><name><surname>David</surname><given-names>P.</given-names></name><name><surname>Chen</surname><given-names>N.W.G.</given-names></name><name><surname>Pedrosa-Harand</surname><given-names>A.</given-names></name><name><surname>Thareau</surname><given-names>V.</given-names></name><name><surname>Sevignac</surname><given-names>M.</given-names></name><name><surname>Cannon</surname><given-names>S.B.</given-names></name><name><surname>Debouck</surname><given-names>D.</given-names></name><name><surname>Langin</surname><given-names>T.</given-names></name><name><surname>Geffroy</surname><given-names>V.</given-names></name><source>Plant Physiol.</source><volume>151</volume><year>2009</year><fpage>1048</fpage><lpage>1065</lpage><pub-id pub-id-type="pmid">19776165</pub-id></element-citation></ref><ref id="R43"><label>43</label><element-citation publication-type="journal"><name><surname>Rensing</surname><given-names>S.A.</given-names></name><name><surname>Lang</surname><given-names>D.</given-names></name><name><surname>Zimmer</surname><given-names>A.D.</given-names></name><name><surname>Terry</surname><given-names>A.</given-names></name><name><surname>Salamov</surname><given-names>A.</given-names></name><name><surname>Shapiro</surname><given-names>H.</given-names></name><name><surname>Nishiyama</surname><given-names>T.</given-names></name><name><surname>Perroud</surname><given-names>P.-F.</given-names></name><name><surname>Lindquist</surname><given-names>E.A.</given-names></name><name><surname>Kamisugi</surname><given-names>Y.</given-names></name><source>Science.</source><volume>319</volume><year>2008</year><issue>5859</issue><fpage>64</fpage><lpage>69</lpage><pub-id pub-id-type="pmid">18079367</pub-id></element-citation></ref><ref id="R44"><label>44</label><element-citation publication-type="journal"><name><surname>Ralph</surname><given-names>S.G.</given-names></name><name><surname>Chun</surname><given-names>H.J.</given-names></name><name><surname>Kolosova</surname><given-names>N.</given-names></name><name><surname>Cooper</surname><given-names>D.</given-names></name><name><surname>Oddy</surname><given-names>C.</given-names></name><name><surname>Ritland</surname><given-names>C.E.</given-names></name><name><surname>Kirkpatrick</surname><given-names>R.</given-names></name><name><surname>Moore</surname><given-names>R.</given-names></name><name><surname>Barber</surname><given-names>S.</given-names></name><name><surname>Holt</surname><given-names>R.A.</given-names></name><source>BMC Genomics.</source><volume>9</volume><year>2008</year></element-citation></ref><ref id="R45"><label>45</label><element-citation publication-type="journal"><name><surname>Tuskan</surname><given-names>G.A.</given-names></name><name><surname>Difazio</surname><given-names>S.</given-names></name><name><surname>Jansson</surname><given-names>S.</given-names></name><name><surname>Bohlmann</surname><given-names>J.</given-names></name><name><surname>Grigoriev</surname><given-names>I.</given-names></name><name><surname>Hellsten</surname><given-names>U.</given-names></name><name><surname>Putnam</surname><given-names>N.</given-names></name><name><surname>Ralph</surname><given-names>S.</given-names></name><name><surname>Rombauts</surname><given-names>S.</given-names></name><name><surname>Salamov</surname><given-names>A.</given-names></name><source>Science.</source><volume>313</volume><year>2006</year><fpage>1596</fpage><lpage>1604</lpage><pub-id pub-id-type="pmid">16973872</pub-id></element-citation></ref><ref id="R46"><label>46</label><element-citation publication-type="journal"><name><surname>Paterson</surname><given-names>A.H.</given-names></name><name><surname>Bowers</surname><given-names>J.E.</given-names></name><name><surname>Bruggmann</surname><given-names>R.</given-names></name><name><surname>Dubchak</surname><given-names>I.</given-names></name><name><surname>Grimwood</surname><given-names>J.</given-names></name><name><surname>Gundlach</surname><given-names>H.</given-names></name><name><surname>Haberer</surname><given-names>G.</given-names></name><name><surname>Hellsten</surname><given-names>U.</given-names></name><name><surname>Mitros</surname><given-names>T.</given-names></name><name><surname>Poliakov</surname><given-names>A.</given-names></name><source>Nature.</source><volume>457</volume><year>2009</year><issue>7229</issue><fpage>551</fpage><lpage>556</lpage><pub-id pub-id-type="pmid">19189423</pub-id></element-citation></ref><ref id="R47"><label>47</label><element-citation publication-type="journal"><name><surname>Kawaura</surname><given-names>K.</given-names></name><name><surname>Mochida</surname><given-names>K.</given-names></name><name><surname>Enju</surname><given-names>A.</given-names></name><name><surname>Totoki</surname><given-names>Y.</given-names></name><name><surname>Toyoda</surname><given-names>A.</given-names></name><name><surname>Sakaki</surname><given-names>Y.</given-names></name><name><surname>Kai</surname><given-names>C.</given-names></name><name><surname>Kawai</surname><given-names>J.</given-names></name><name><surname>Hayashizaki</surname><given-names>Y.</given-names></name><name><surname>Seki</surname><given-names>M.</given-names></name><source>BMC Genomics.</source><volume>10</volume><year>2009</year></element-citation></ref><ref id="R48"><label>48</label><element-citation publication-type="journal"><name><surname>Alexandrov</surname><given-names>N.N.</given-names></name><name><surname>Brover</surname><given-names>V.V.</given-names></name><name><surname>Freidin</surname><given-names>S.</given-names></name><name><surname>Troukhan</surname><given-names>M.E.</given-names></name><name><surname>Tatarinova</surname><given-names>T.V.</given-names></name><name><surname>Zhang</surname><given-names>H.</given-names></name><name><surname>Swaller</surname><given-names>T.J.</given-names></name><name><surname>Lu</surname><given-names>Y.P.</given-names></name><name><surname>Bouck</surname><given-names>J.</given-names></name><name><surname>Flavell</surname><given-names>R.B.</given-names></name><source>Plant Mol. Biol.</source><volume>69</volume><year>2009</year><fpage>179</fpage><lpage>194</lpage><pub-id pub-id-type="pmid">18937034</pub-id></element-citation></ref><ref id="R49"><label>49</label><element-citation publication-type="journal"><name><surname>Hwang</surname><given-names>L.</given-names></name><name><surname>Hocking-Murray</surname><given-names>D.</given-names></name><name><surname>Bahrami</surname><given-names>A.K.</given-names></name><name><surname>Andersson</surname><given-names>M.</given-names></name><name><surname>Rine</surname><given-names>J.</given-names></name><name><surname>Sil</surname><given-names>A.</given-names></name><source>Mol. Biol. Cell.</source><volume>14</volume><year>2003</year><fpage>2314</fpage><lpage>2326</lpage><pub-id pub-id-type="pmid">12808032</pub-id></element-citation></ref><ref id="R50"><label>50</label><element-citation publication-type="journal"><name><surname>Tishkov</surname><given-names>V.I.</given-names></name><name><surname>Galkin</surname><given-names>A.G.</given-names></name><name><surname>Egorov</surname><given-names>A.M.</given-names></name><source>Dokl Acad Nauk USSR.</source><volume>317</volume><year>1991</year><fpage>745</fpage><lpage>748</lpage></element-citation></ref><ref id="R51"><label>51</label><element-citation publication-type="journal"><name><surname>Hatrongjit</surname><given-names>R.</given-names></name><name><surname>Packdibamrung</surname><given-names>K.</given-names></name><source>Enz. Microb. Technol.</source><volume>46</volume><year>2010</year><fpage>557</fpage><lpage>561</lpage></element-citation></ref><ref id="R52"><label>52</label><element-citation publication-type="journal"><name><surname>Barnett</surname><given-names>M.J.</given-names></name><name><surname>Fisher</surname><given-names>R.F.</given-names></name><name><surname>Jones</surname><given-names>T.</given-names></name><name><surname>Komp</surname><given-names>C.</given-names></name><name><surname>Abola</surname><given-names>A.P.</given-names></name><name><surname>Barloy-Hubler</surname><given-names>F.</given-names></name><name><surname>Bowser</surname><given-names>L.</given-names></name><name><surname>Capela</surname><given-names>D.</given-names></name><name><surname>Galibert</surname><given-names>F.</given-names></name><name><surname>Gouzyet</surname><given-names>J.</given-names></name><source>Proc. Natl. Acad. Sci. USA.</source><volume>98</volume><year>2001</year><issue>17</issue><fpage>9883</fpage><lpage>9888</lpage><pub-id pub-id-type="pmid">11481432</pub-id></element-citation></ref><ref id="R53"><label>53</label><element-citation publication-type="journal"><name><surname>Ambard-Bretteville</surname><given-names>F.</given-names></name><name><surname>Small</surname><given-names>I.</given-names></name><name><surname>Grandjean</surname><given-names>O.</given-names></name><name><surname>Colas des Francs-Small</surname><given-names>C.</given-names></name><source>Biochem. Biophys. Res. Commun.</source><volume>311</volume><year>2003</year><fpage>966</fpage><lpage>971</lpage><pub-id pub-id-type="pmid">14623276</pub-id></element-citation></ref><ref id="R54"><label>54</label><element-citation publication-type="journal"><name><surname>Weerasinghe</surname><given-names>P.A.</given-names></name><name><surname>van Holm</surname><given-names>L.H.J.</given-names></name><source>Biologia Plantarum.</source><volume>42</volume><year>1999</year><fpage>541</fpage><lpage>547</lpage></element-citation></ref><ref id="R55"><label>55</label><element-citation publication-type="journal"><name><surname>Colic</surname><given-names>S.</given-names></name><name><surname>Milatovic</surname><given-names>D.</given-names></name><name><surname>Nikolic</surname><given-names>D.</given-names></name><name><surname>Zec</surname><given-names>G.</given-names></name><source>Hort. Sci. (Prague).</source><volume>37</volume><year>2010</year><fpage>56</fpage><lpage>61</lpage></element-citation></ref><ref id="R56"><label>56</label><element-citation publication-type="journal"><name><surname>Colich</surname><given-names>S.</given-names></name><name><surname>Milatovich</surname><given-names>D.</given-names></name><name><surname>Nikolich</surname><given-names>D.</given-names></name><name><surname>Zec</surname><given-names>G.</given-names></name><source>Bulgarian J. Agricul. Sci.</source><volume>15</volume><year>2009</year><fpage>552</fpage><lpage>556</lpage></element-citation></ref><ref id="R57"><label>57</label><element-citation publication-type="journal"><name><surname>Farinelli</surname><given-names>M.P.</given-names></name><name><surname>Fry</surname><given-names>D.W.</given-names></name><name><surname>Richardson</surname><given-names>K.E.</given-names></name><source>Plant Physiol.</source><volume>73</volume><year>1983</year><fpage>858</fpage><lpage>859</lpage><pub-id pub-id-type="pmid">16663314</pub-id></element-citation></ref><ref id="R58"><label>58</label><element-citation publication-type="journal"><name><surname>Sadykhov</surname><given-names>E.G.</given-names></name><name><surname>Serov</surname><given-names>A.E.</given-names></name><name><surname>Yasnyi</surname><given-names>I.E.</given-names></name><name><surname>Petrov</surname><given-names>A.S.</given-names></name><name><surname>Tishkov</surname><given-names>V.I.</given-names></name><source>Moscow University Chemistry Bulletin,</source><volume>47</volume><year>2006</year><issue>1</issue><fpage>31</fpage><lpage>34</lpage></element-citation></ref><ref id="R59"><label>59</label><element-citation publication-type="journal"><name><surname>Baack</surname><given-names>R.D.</given-names></name><name><surname>Markwell</surname><given-names>J.</given-names></name><name><surname>Herman</surname><given-names>P.L.</given-names></name><name><surname>Osterman</surname><given-names>J.C.</given-names></name><source>J. Plant Physiol.</source><volume>160</volume><year>2003</year><fpage>445</fpage><lpage>450</lpage><pub-id pub-id-type="pmid">12806771</pub-id></element-citation></ref><ref id="R60"><label>60</label><element-citation publication-type="journal"><name><surname>Li</surname><given-names>R.</given-names></name><name><surname>Ziola</surname><given-names>B.</given-names></name><name><surname>King</surname><given-names>J.</given-names></name><source>J. Plant Physiol.</source><volume>157</volume><year>2000</year><fpage>161</fpage><lpage>167</lpage></element-citation></ref><ref id="R61"><label>61</label><element-citation publication-type="journal"><name><surname>Uotila</surname><given-names>L.</given-names></name><name><surname>Koivusalo</surname><given-names>M.</given-names></name><source>Arch. Biochem. Biophys.</source><volume>196</volume><year>1979</year><fpage>33</fpage><lpage>45</lpage><pub-id pub-id-type="pmid">574372</pub-id></element-citation></ref><ref id="R62"><label>62</label><element-citation publication-type="journal"><name><surname>Ohyama</surname><given-names>T.</given-names></name><name><surname>Yamazaki</surname><given-names>I.</given-names></name><source>J. Biochem.</source><volume>77</volume><year>1975</year><fpage>845</fpage><lpage>852</lpage><pub-id pub-id-type="pmid">168190</pub-id></element-citation></ref><ref id="R63"><label>63</label><element-citation publication-type="journal"><name><surname>Peacock</surname><given-names>D.</given-names></name><name><surname>Boulter</surname><given-names>D.</given-names></name><source>Biochem. J.</source><volume>120</volume><year>1970</year><fpage>763</fpage><lpage>769</lpage><pub-id pub-id-type="pmid">4322039</pub-id></element-citation></ref><ref id="R64"><label>64</label><element-citation publication-type="journal"><name><surname>Romanova</surname><given-names>E.G.</given-names></name><name><surname>Alekseeva</surname><given-names>A.A.</given-names></name><name><surname>Pometun</surname><given-names>E.V.</given-names></name><name><surname>Tishkov</surname><given-names>V.I.</given-names></name><source>Moscow University Chemistry Bulletin.</source><volume>65</volume><year>2010</year><fpage>127</fpage><lpage>130</lpage></element-citation></ref><ref id="R65"><label>65</label><element-citation publication-type="journal"><name><surname>Slusarczyk</surname><given-names>H.</given-names></name><name><surname>Felber</surname><given-names>S.</given-names></name><name><surname>Kula</surname><given-names>M.R.</given-names></name><name><surname>Pohl</surname><given-names>M.</given-names></name><source>Eur. J. Biochem.</source><volume>267</volume><year>2000</year><fpage>1280</fpage><lpage>1289</lpage><pub-id pub-id-type="pmid">10691964</pub-id></element-citation></ref><ref id="R66"><label>66</label><element-citation publication-type="journal"><name><surname>Karaguler</surname><given-names>N.G.</given-names></name><name><surname>Sessions</surname><given-names>R.B.</given-names></name><name><surname>Clarke</surname><given-names>A.R.</given-names></name><name><surname>Holbrook</surname><given-names>J.</given-names></name><source>Biotechnol. Lett.</source><volume>23</volume><year>2001</year><fpage>283</fpage><lpage>287</lpage></element-citation></ref><ref id="R67"><label>67</label><element-citation publication-type="journal"><source>Ph.D. Disseration. Moscow, Lomonosov Moscow State University,</source><year>2002</year></element-citation></ref><ref id="R68"><label>68</label><element-citation publication-type="journal"><name><surname>Serov</surname><given-names>A.E.</given-names></name><name><surname>Popova</surname><given-names>A.S.</given-names></name><name><surname>Fedorchuk</surname><given-names>V.V.</given-names></name><name><surname>Tishkov</surname><given-names>V.I.</given-names></name><source>Biochem. J.</source><volume>367</volume><year>2002</year><fpage>841</fpage><lpage>847</lpage><pub-id pub-id-type="pmid">12144528</pub-id></element-citation></ref><ref id="R69"><label>69</label><element-citation publication-type="journal"><name><surname>Seelbach</surname><given-names>K.</given-names></name><name><surname>Riebel</surname><given-names>B.</given-names></name><name><surname>Hummel</surname><given-names>W.</given-names></name><name><surname>Kula</surname><given-names>M.-R.</given-names></name><name><surname>Tishkov</surname><given-names>V.I.</given-names></name><name><surname>Egorov</surname><given-names>A.M.</given-names></name><name><surname>Wandrey</surname><given-names>C.</given-names></name><name><surname>Kragl</surname><given-names>U.</given-names></name><source>Tetrahedron Lett.</source><volume>37</volume><year>1996</year><issue>9</issue><fpage>1377</fpage><lpage>1380</lpage></element-citation></ref><ref id="R70"><label>70</label><element-citation publication-type="journal"><name><surname>Rissom</surname><given-names>S.</given-names></name><name><surname>Schwarz-Linek</surname><given-names>U.</given-names></name><name><surname>Vogel</surname><given-names>M.</given-names></name><name><surname>Tishkov</surname><given-names>V.I.</given-names></name><name><surname>Kragl</surname><given-names>U.</given-names></name><source>Tetrahedron: Assymetry.</source><volume>8</volume><year>1997</year><issue>15</issue><fpage>2523</fpage><lpage>2526</lpage></element-citation></ref><ref id="R71"><label>71</label><element-citation publication-type="journal"><name><surname>Sadykhov</surname><given-names>E.G.</given-names></name><name><surname>Serov</surname><given-names>A.E.</given-names></name><name><surname>Voinova</surname><given-names>N.S.</given-names></name><name><surname>Uglanova</surname><given-names>S.V.</given-names></name><name><surname>Petrov</surname><given-names>A.S.</given-names></name><name><surname>Kleimenov</surname><given-names>S.Yu.</given-names></name><name><surname>Popov</surname><given-names>V.O.</given-names></name><name><surname>Tishkov</surname><given-names>V.I.</given-names></name><source>Appl. Biochem. Microbiol.</source><volume>42</volume><year>2006</year><issue>3</issue></element-citation></ref><ref id="R72"><label>72</label><element-citation publication-type="journal"><name><surname>Sadykhov</surname><given-names>E.G.</given-names></name><source>Preparation, thermal stability and structural studies of recombinant
formate dehydrogenases from different sources : Ph.D. Dissertation, Moscow,
A.N.Bach Institute of Biochemistry RAS,</source><year>2007</year></element-citation></ref><ref id="R73"><label>73</label><element-citation publication-type="journal"><name><surname>Resch</surname><given-names>A.</given-names></name><name><surname>Rosenstein</surname><given-names>R.</given-names></name><name><surname>Nerz</surname><given-names>C.</given-names></name><name><surname>Gotz</surname><given-names>F.</given-names></name><source>Appl. Environ. Microbiol.</source><volume>71</volume><year>2005</year><issue>5</issue><fpage>2663</fpage><lpage>2676</lpage><pub-id pub-id-type="pmid">15870358</pub-id></element-citation></ref><ref id="R74"><label>74</label><element-citation publication-type="journal"><name><surname>Savin</surname><given-names>S.S.</given-names></name><name><surname>Tishkov</surname><given-names>V.I.</given-names></name><source>Acta Naturae.</source><volume>2</volume><year>2010</year><fpage>78</fpage><lpage>82</lpage></element-citation></ref><ref id="R75"><label>75</label><element-citation publication-type="journal"><name><surname>Shabalin</surname><given-names>I.G.</given-names></name><name><surname>Serov</surname><given-names>A.E.</given-names></name><name><surname>Skirgello</surname><given-names>O.E.</given-names></name><name><surname>Timofeev</surname><given-names>V.I.</given-names></name><name><surname>Samygina</surname><given-names>V.R.</given-names></name><name><surname>Popov</surname><given-names>V.O.</given-names></name><name><surname>Tishkov</surname><given-names>V.I.</given-names></name><name><surname>Kuranova</surname><given-names>I.P.</given-names></name><source>Crystallography Reports.</source><volume>55</volume><year>2010</year><fpage>806</fpage><lpage>810</lpage></element-citation></ref><ref id="R76"><label>76</label><element-citation publication-type="journal"><name><surname>Alekseeva</surname><given-names>A.A.</given-names></name><name><surname>Shabalin</surname><given-names>I.G.</given-names></name><name><surname>Polyakov</surname><given-names>K.M.</given-names></name><name><surname>Tishkov</surname><given-names>V.I.</given-names></name><source>J. Biotechnol.</source><volume>150</volume><year>2010</year><page-range>476</page-range></element-citation></ref><ref id="R77"><label>77</label><element-citation publication-type="journal"><name><surname>Tishkov</surname><given-names>V.I.</given-names></name><name><surname>Uglanova</surname><given-names>S.V.</given-names></name><name><surname>Fedorchuk</surname><given-names>V.V.</given-names></name><name><surname>Savin</surname><given-names>S.S.</given-names></name><source>Acta Naturae.</source><volume>2</volume><year>2010</year><fpage>82</fpage><lpage>87</lpage></element-citation></ref></ref-list></back></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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