Structural and Biochemical Analysis of the Hordeum vulgare L. HvGR-RBP1 Protein, a Glycine-Rich RNA-Binding Protein Involved in the Regulation of Barley Plant Development and Stress Response
Identifieur interne : 001944 ( Ncbi/Merge ); précédent : 001943; suivant : 001945Structural and Biochemical Analysis of the Hordeum vulgare L. HvGR-RBP1 Protein, a Glycine-Rich RNA-Binding Protein Involved in the Regulation of Barley Plant Development and Stress Response
Auteurs : Brian X0a P. Tripet ; Katelyn E. Mason ; Brian J. Eilers ; Jennifer Burns ; Paul Powell ; Andreas M. Fischer [États-Unis] ; Valérie CopiéSource :
- Biochemistry [ 0006-2960 ] ; 2014.
Abstract
The timing of whole-plant senescence
influences important agricultural
traits such as yield and grain protein content. Post-transcriptional
regulation by plant RNA-binding proteins is essential for proper control
of gene expression, development, and stress responses. Here, we report
the three-dimensional solution NMR structure and nucleic acid-binding
properties of the barley glycine-rich RNA-binding protein
Url:
DOI: 10.1021/bi5007223
PubMed: 25495582
PubMed Central: 4278681
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Structural and Biochemical Analysis of the <italic>Hordeum vulgare</italic> L. <italic>Hv</italic>GR-RBP1 Protein,
a Glycine-Rich RNA-Binding Protein Involved in the Regulation of Barley
Plant Development and Stress Response</title><author><name sortKey="Tripet, Brian X0a P" sort="Tripet, Brian X0a P" uniqKey="Tripet B" first="Brian X0a P." last="Tripet">Brian X0a P. Tripet</name><affiliation><nlm:aff wicri:cut=" and" id="aff1a">Department of Chemistry and Biochemistry</nlm:aff></affiliation></author><author><name sortKey="Mason, Katelyn E" sort="Mason, Katelyn E" uniqKey="Mason K" first="Katelyn E." last="Mason">Katelyn E. Mason</name><affiliation><nlm:aff wicri:cut=" and" id="aff1a">Department of Chemistry and Biochemistry</nlm:aff></affiliation></author><author><name sortKey="Eilers, Brian J" sort="Eilers, Brian J" uniqKey="Eilers B" first="Brian J." last="Eilers">Brian J. Eilers</name><affiliation><nlm:aff wicri:cut=" and" id="aff1a">Department of Chemistry and Biochemistry</nlm:aff></affiliation></author><author><name sortKey="Burns, Jennifer" sort="Burns, Jennifer" uniqKey="Burns J" first="Jennifer" last="Burns">Jennifer Burns</name><affiliation><nlm:aff wicri:cut=" and" id="aff1a">Department of Chemistry and Biochemistry</nlm:aff></affiliation></author><author><name sortKey="Powell, Paul" sort="Powell, Paul" uniqKey="Powell P" first="Paul" last="Powell">Paul Powell</name><affiliation><nlm:aff wicri:cut=" and" id="aff1a">Department of Chemistry and Biochemistry</nlm:aff></affiliation></author><author><name sortKey="Fischer, Andreas M" sort="Fischer, Andreas M" uniqKey="Fischer A" first="Andreas M." last="Fischer">Andreas M. Fischer</name><affiliation wicri:level="1"><nlm:aff id="aff1a">Department of Plant Sciences and Plant Pathology,<institution>Montana State University</institution>, Bozeman, Montana 59717,<country>United States</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Copie, Valerie" sort="Copie, Valerie" uniqKey="Copie V" first="Valérie" last="Copié">Valérie Copié</name><affiliation><nlm:aff wicri:cut=" and" id="aff1a">Department of Chemistry and Biochemistry</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">25495582</idno><idno type="pmc">4278681</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4278681</idno><idno type="RBID">PMC:4278681</idno><idno type="doi">10.1021/bi5007223</idno><date when="2014">2014</date><idno type="wicri:Area/Pmc/Corpus">000436</idno><idno type="wicri:Area/Pmc/Curation">000435</idno><idno type="wicri:Area/Pmc/Checkpoint">000700</idno><idno type="wicri:Area/Ncbi/Merge">001944</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Structural and Biochemical Analysis of the <italic>Hordeum vulgare</italic> L. <italic>Hv</italic>GR-RBP1 Protein,
a Glycine-Rich RNA-Binding Protein Involved in the Regulation of Barley
Plant Development and Stress Response</title><author><name sortKey="Tripet, Brian X0a P" sort="Tripet, Brian X0a P" uniqKey="Tripet B" first="Brian X0a P." last="Tripet">Brian X0a P. Tripet</name><affiliation><nlm:aff wicri:cut=" and" id="aff1a">Department of Chemistry and Biochemistry</nlm:aff></affiliation></author><author><name sortKey="Mason, Katelyn E" sort="Mason, Katelyn E" uniqKey="Mason K" first="Katelyn E." last="Mason">Katelyn E. Mason</name><affiliation><nlm:aff wicri:cut=" and" id="aff1a">Department of Chemistry and Biochemistry</nlm:aff></affiliation></author><author><name sortKey="Eilers, Brian J" sort="Eilers, Brian J" uniqKey="Eilers B" first="Brian J." last="Eilers">Brian J. Eilers</name><affiliation><nlm:aff wicri:cut=" and" id="aff1a">Department of Chemistry and Biochemistry</nlm:aff></affiliation></author><author><name sortKey="Burns, Jennifer" sort="Burns, Jennifer" uniqKey="Burns J" first="Jennifer" last="Burns">Jennifer Burns</name><affiliation><nlm:aff wicri:cut=" and" id="aff1a">Department of Chemistry and Biochemistry</nlm:aff></affiliation></author><author><name sortKey="Powell, Paul" sort="Powell, Paul" uniqKey="Powell P" first="Paul" last="Powell">Paul Powell</name><affiliation><nlm:aff wicri:cut=" and" id="aff1a">Department of Chemistry and Biochemistry</nlm:aff></affiliation></author><author><name sortKey="Fischer, Andreas M" sort="Fischer, Andreas M" uniqKey="Fischer A" first="Andreas M." last="Fischer">Andreas M. Fischer</name><affiliation wicri:level="1"><nlm:aff id="aff1a">Department of Plant Sciences and Plant Pathology,<institution>Montana State University</institution>, Bozeman, Montana 59717,<country>United States</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Copie, Valerie" sort="Copie, Valerie" uniqKey="Copie V" first="Valérie" last="Copié">Valérie Copié</name><affiliation><nlm:aff wicri:cut=" and" id="aff1a">Department of Chemistry and Biochemistry</nlm:aff></affiliation></author></analytic><series><title level="j">Biochemistry</title><idno type="ISSN">0006-2960</idno><idno type="eISSN">1520-4995</idno><imprint><date when="2014">2014</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p content-type="toc-graphic"><graphic xlink:href="bi-2014-007223_0012" id="ab-tgr1"></graphic></p><p>The timing of whole-plant senescence
influences important agricultural
traits such as yield and grain protein content. Post-transcriptional
regulation by plant RNA-binding proteins is essential for proper control
of gene expression, development, and stress responses. Here, we report
the three-dimensional solution NMR structure and nucleic acid-binding
properties of the barley glycine-rich RNA-binding protein <italic>Hv</italic>GR-RBP1, whose transcript has been identified as being
>45-fold up-regulated in early—as compared to late—senescing
near-isogenic barley germplasm. NMR analysis reveals that <italic>Hv</italic>GR-RBP1 is a multidomain protein comprising a well-folded
N-terminal RNA Recognition Motif (RRM) and a structurally disordered
C-terminal glycine-rich domain. Chemical shift differences observed
in 2D <sup>1</sup>H–<sup>15</sup>N correlation (HSQC) NMR spectra
of full-length <italic>Hv</italic>GR-RBP1 and N-<italic>Hv</italic>GR-RBP1 (RRM domain only) suggest that the two domains can interact
both in-trans and intramolecularly, similar to what is observed in
the tobacco <italic>Nt</italic>GR-RBP1 protein. Further, we show that
the RRM domain of <italic>Hv</italic>GR-RBP1 binds single-stranded
DNA nucleotide fragments containing the consensus nucleotide sequence
5′-TTCTGX-3′ with low micromolar affinity <italic>in
vitro</italic>. We also demonstrate that the C-terminal glycine-rich
(<italic>Hv</italic>GR) domain of <italic>Hv</italic>-GR-RBP1 can
interact nonspecifically with ssRNA <italic>in vitro</italic>. Structural
similarities with other plant glycine-rich RNA-binding proteins suggest
that <italic>Hv</italic>GR-RBP1 may be multifunctional. Based on gene
expression analysis following cold stress in barley and <italic>E. coli</italic> growth studies following cold shock treatment,
we conclude that <italic>Hv</italic>GR-RBP1 functions in a manner
similar to cold-shock proteins and harbors RNA chaperone activity. <italic>Hv</italic>GR-RBP1 is therefore not only involved in the regulation
of barley development including senescence, but also functions in
plant responses to environmental stress.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Zhang, H" uniqKey="Zhang H">H. Zhang</name></author><author><name sortKey="Zhou, C" uniqKey="Zhou C">C. Zhou</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Distelfeld, A" uniqKey="Distelfeld A">A. Distelfeld</name></author><author><name sortKey="Avni, R" uniqKey="Avni R">R. Avni</name></author><author><name sortKey="Fischer, A M" uniqKey="Fischer A">A. M. Fischer</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="See, D" uniqKey="See D">D. See</name></author><author><name sortKey="Kanazin, V" uniqKey="Kanazin V">V. Kanazin</name></author><author><name sortKey="Kephart, K" uniqKey="Kephart K">K. Kephart</name></author><author><name sortKey="Black, T" uniqKey="Black T">T. Black</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Gregersen, P L" uniqKey="Gregersen P">P. L. Gregersen</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Jukanti, A" uniqKey="Jukanti A">A. Jukanti</name></author><author><name sortKey="Heidlebaugh, N" uniqKey="Heidlebaugh N">N. Heidlebaugh</name></author><author><name sortKey="Parrott, D" uniqKey="Parrott D">D. Parrott</name></author><author><name sortKey="Fischer, I" uniqKey="Fischer I">I. Fischer</name></author><author><name sortKey="Mcinnerney, K" uniqKey="Mcinnerney K">K. McInnerney</name></author><author><name sortKey="Fischer, A" uniqKey="Fischer A">A. Fischer</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Jukanti, A K" uniqKey="Jukanti A">A. K. Jukanti</name></author><author><name sortKey="Fischer, A M" uniqKey="Fischer A">A. M. Fischer</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Heidlebaugh, N M" uniqKey="Heidlebaugh N">N. M. Heidlebaugh</name></author><author><name sortKey="Trethewey, B R" uniqKey="Trethewey B">B. R. Trethewey</name></author><author><name sortKey="Jukanti, A K" uniqKey="Jukanti A">A. K. Jukanti</name></author><author><name sortKey="Parrott, D L" uniqKey="Parrott D">D. L. Parrott</name></author><author><name sortKey="Martin, J M" uniqKey="Martin J">J. M. Martin</name></author><author><name sortKey="Fischer, A M" uniqKey="Fischer A">A. M. Fischer</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Streitner, C" uniqKey="Streitner C">C. Streitner</name></author><author><name sortKey="Danisman, S" uniqKey="Danisman S">S. Danisman</name></author><author><name sortKey="Wehrle, F" uniqKey="Wehrle F">F. Wehrle</name></author><author><name sortKey="Schoning, J C" uniqKey="Schoning J">J. C. Schoning</name></author><author><name sortKey="Alfano, J R" uniqKey="Alfano J">J. R. Alfano</name></author><author><name sortKey="Staiger, D" uniqKey="Staiger D">D. Staiger</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Gepstein, S" uniqKey="Gepstein S">S. Gepstein</name></author><author><name sortKey="Sabehi, G" uniqKey="Sabehi G">G. Sabehi</name></author><author><name sortKey="Carp, M J" uniqKey="Carp M">M.-J. Carp</name></author><author><name sortKey="Hajouj, T" uniqKey="Hajouj T">T. Hajouj</name></author><author><name sortKey="Nesher, M F O" uniqKey="Nesher M">M. F. O. Nesher</name></author><author><name sortKey="Yariv, I" uniqKey="Yariv I">I. Yariv</name></author><author><name sortKey="Dor, C" uniqKey="Dor C">C. Dor</name></author><author><name sortKey="Bassani, M" uniqKey="Bassani M">M. Bassani</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Lacerenza, J A" uniqKey="Lacerenza J">J. A. Lacerenza</name></author><author><name sortKey="Parrott, D L" uniqKey="Parrott D">D. L. Parrott</name></author><author><name sortKey="Fischer, A M" uniqKey="Fischer A">A. M. Fischer</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Parrott, D X0a L" uniqKey="Parrott D">D.
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<front><journal-meta><journal-id journal-id-type="nlm-ta">Biochemistry</journal-id><journal-id journal-id-type="iso-abbrev">Biochemistry</journal-id><journal-id journal-id-type="publisher-id">bi</journal-id><journal-id journal-id-type="coden">bichaw</journal-id><journal-title-group><journal-title>Biochemistry</journal-title></journal-title-group><issn pub-type="ppub">0006-2960</issn><issn pub-type="epub">1520-4995</issn><publisher><publisher-name>American
Chemical Society</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">25495582</article-id><article-id pub-id-type="pmc">4278681</article-id><article-id pub-id-type="doi">10.1021/bi5007223</article-id><article-categories><subj-group><subject>Article</subject></subj-group></article-categories><title-group><article-title>Structural and Biochemical Analysis of the <italic>Hordeum vulgare</italic> L. <italic>Hv</italic>GR-RBP1 Protein,
a Glycine-Rich RNA-Binding Protein Involved in the Regulation of Barley
Plant Development and Stress Response</article-title></title-group><contrib-group><contrib contrib-type="author" id="ath1"><name><surname>Tripet</surname><given-names>Brian
P.</given-names></name><xref rid="aff1a" ref-type="aff">‡</xref></contrib><contrib contrib-type="author" id="ath2"><name><surname>Mason</surname><given-names>Katelyn E.</given-names></name><xref rid="aff1a" ref-type="aff">‡</xref></contrib><contrib contrib-type="author" id="ath3"><name><surname>Eilers</surname><given-names>Brian J.</given-names></name><xref rid="aff1a" ref-type="aff">‡</xref></contrib><contrib contrib-type="author" id="ath4"><name><surname>Burns</surname><given-names>Jennifer</given-names></name><xref rid="aff1a" ref-type="aff">‡</xref></contrib><contrib contrib-type="author" id="ath5"><name><surname>Powell</surname><given-names>Paul</given-names></name><xref rid="aff1a" ref-type="aff">‡</xref></contrib><contrib contrib-type="author" id="ath6"><name><surname>Fischer</surname><given-names>Andreas M.</given-names></name><xref rid="aff1a" ref-type="aff">§</xref></contrib><contrib contrib-type="author" corresp="yes" id="ath7"><name><surname>Copié</surname><given-names>Valérie</given-names></name><xref rid="cor1" ref-type="other">*</xref><xref rid="aff1a" ref-type="aff">‡</xref></contrib><aff id="aff1a"><sup>‡</sup>Department of Chemistry and Biochemistry and<sup>§</sup>Department of Plant Sciences and Plant Pathology,<institution>Montana State University</institution>, Bozeman, Montana 59717,<country>United States</country></aff></contrib-group><author-notes><corresp id="cor1"><label>*</label>E-mail: <email>vcopie@chemistry.montana.edu</email>. Phone: <phone>(406) 994-7244</phone>. Fax: <fax>(406) 994-5407</fax>.</corresp></author-notes><pub-date pub-type="pmc-release"><day>25</day><month>11</month><year>2015</year></pub-date><pub-date pub-type="epub"><day>25</day><month>11</month><year>2014</year></pub-date><pub-date pub-type="ppub"><day>23</day><month>12</month><year>2014</year></pub-date><volume>53</volume><issue>50</issue><fpage>7945</fpage><lpage>7960</lpage><history><date date-type="received"><day>10</day><month>06</month><year>2014</year></date><date date-type="rev-recd"><day>25</day><month>11</month><year>2014</year></date></history><permissions><copyright-statement>Copyright © 2014 American Chemical
Society</copyright-statement><copyright-year>2014</copyright-year><copyright-holder>American Chemical
Society</copyright-holder><license><license-p>This is an open access article published under an ACS AuthorChoice <ext-link ext-link-type="uri" xlink:href="http://pubs.acs.org/page/policy/authorchoice_termsofuse.html">License</ext-link>, which permits copying and redistribution of the article or any adaptations for non-commercial purposes.</license-p></license></permissions><abstract><p content-type="toc-graphic"><graphic xlink:href="bi-2014-007223_0012" id="ab-tgr1"></graphic></p><p>The timing of whole-plant senescence
influences important agricultural
traits such as yield and grain protein content. Post-transcriptional
regulation by plant RNA-binding proteins is essential for proper control
of gene expression, development, and stress responses. Here, we report
the three-dimensional solution NMR structure and nucleic acid-binding
properties of the barley glycine-rich RNA-binding protein <italic>Hv</italic>GR-RBP1, whose transcript has been identified as being
>45-fold up-regulated in early—as compared to late—senescing
near-isogenic barley germplasm. NMR analysis reveals that <italic>Hv</italic>GR-RBP1 is a multidomain protein comprising a well-folded
N-terminal RNA Recognition Motif (RRM) and a structurally disordered
C-terminal glycine-rich domain. Chemical shift differences observed
in 2D <sup>1</sup>H–<sup>15</sup>N correlation (HSQC) NMR spectra
of full-length <italic>Hv</italic>GR-RBP1 and N-<italic>Hv</italic>GR-RBP1 (RRM domain only) suggest that the two domains can interact
both in-trans and intramolecularly, similar to what is observed in
the tobacco <italic>Nt</italic>GR-RBP1 protein. Further, we show that
the RRM domain of <italic>Hv</italic>GR-RBP1 binds single-stranded
DNA nucleotide fragments containing the consensus nucleotide sequence
5′-TTCTGX-3′ with low micromolar affinity <italic>in
vitro</italic>. We also demonstrate that the C-terminal glycine-rich
(<italic>Hv</italic>GR) domain of <italic>Hv</italic>-GR-RBP1 can
interact nonspecifically with ssRNA <italic>in vitro</italic>. Structural
similarities with other plant glycine-rich RNA-binding proteins suggest
that <italic>Hv</italic>GR-RBP1 may be multifunctional. Based on gene
expression analysis following cold stress in barley and <italic>E. coli</italic> growth studies following cold shock treatment,
we conclude that <italic>Hv</italic>GR-RBP1 functions in a manner
similar to cold-shock proteins and harbors RNA chaperone activity. <italic>Hv</italic>GR-RBP1 is therefore not only involved in the regulation
of barley development including senescence, but also functions in
plant responses to environmental stress.</p></abstract><funding-group><funding-statement><funding-source>National Institutes of Health, United States</funding-source></funding-statement></funding-group><custom-meta-group><custom-meta><meta-name>document-id-old-9</meta-name><meta-value>bi5007223</meta-value></custom-meta><custom-meta><meta-name>document-id-new-14</meta-name><meta-value>bi-2014-007223</meta-value></custom-meta><custom-meta><meta-name>ccc-price</meta-name><meta-value></meta-value></custom-meta></custom-meta-group></article-meta></front></pmc><affiliations><list><country><li>États-Unis</li></country></list><tree><noCountry><name sortKey="Burns, Jennifer" sort="Burns, Jennifer" uniqKey="Burns J" first="Jennifer" last="Burns">Jennifer Burns</name><name sortKey="Copie, Valerie" sort="Copie, Valerie" uniqKey="Copie V" first="Valérie" last="Copié">Valérie Copié</name><name sortKey="Eilers, Brian J" sort="Eilers, Brian J" uniqKey="Eilers B" first="Brian J." last="Eilers">Brian J. Eilers</name><name sortKey="Mason, Katelyn E" sort="Mason, Katelyn E" uniqKey="Mason K" first="Katelyn E." last="Mason">Katelyn E. Mason</name><name sortKey="Powell, Paul" sort="Powell, Paul" uniqKey="Powell P" first="Paul" last="Powell">Paul Powell</name><name sortKey="Tripet, Brian X0a P" sort="Tripet, Brian X0a P" uniqKey="Tripet B" first="Brian X0a P." last="Tripet">Brian X0a P. Tripet</name></noCountry><country name="États-Unis"><noRegion><name sortKey="Fischer, Andreas M" sort="Fischer, Andreas M" uniqKey="Fischer A" first="Andreas M." last="Fischer">Andreas M. Fischer</name></noRegion></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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