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Functional Divergence of Poplar Histidine-Aspartate Kinase HK1 Paralogs in Response to Osmotic Stress.

Identifieur interne : 001872 ( Main/Exploration ); précédent : 001871; suivant : 001873

Functional Divergence of Poplar Histidine-Aspartate Kinase HK1 Paralogs in Response to Osmotic Stress.

Auteurs : François Héricourt [France] ; Françoise Chefdor [France] ; Inès Djeghdir [France] ; Mélanie Larcher [France] ; Florent Lafontaine [France] ; Vincent Courdavault [France] ; Daniel Auguin [France] ; Franck Coste [France] ; Christiane Depierreux [France] ; Mirai Tanigawa [Japon] ; Tatsuya Maeda [Japon] ; Gaëlle Glévarec [France] ; Sabine Carpin [France]

Source :

RBID : pubmed:27941652

Descripteurs français

English descriptors

Abstract

Previous works have shown the existence of protein partnerships belonging to a MultiStep Phosphorelay (MSP) in Populus putatively involved in osmosensing. This study is focused on the identification of a histidine-aspartate kinase, HK1b, paralog of HK1a. The characterization of HK1b showed its ability to homo- and hetero-dimerize and to interact with a few Histidine-containing Phosphotransfer (HPt) proteins, suggesting a preferential partnership in poplar MSP linked to drought perception. Furthermore, determinants for interaction specificity between HK1a/1b and HPts were studied by mutagenesis analysis, identifying amino acids involved in this specificity. The HK1b expression analysis in different poplar organs revealed its co-expression with three HPts, reinforcing the hypothesis of partnership participation in the MSP in planta. Moreover, HK1b was shown to act as an osmosensor with kinase activity in a functional complementation assay of an osmosensor deficient yeast strain. These results revealed that HK1b showed a different behaviour for canonical phosphorylation of histidine and aspartate residues. These phosphorylation modularities of canonical amino acids could explain the improved osmosensor performances observed in yeast. As conserved duplicates reflect the selective pressures imposed by the environmental requirements on the species, our results emphasize the importance of HK1 gene duplication in poplar adaptation to drought stress.

DOI: 10.3390/ijms17122061
PubMed: 27941652
PubMed Central: PMC5187861


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Le document en format XML

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<name sortKey="Maeda, Tatsuya" sort="Maeda, Tatsuya" uniqKey="Maeda T" first="Tatsuya" last="Maeda">Tatsuya Maeda</name>
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<title xml:lang="en">Functional Divergence of Poplar Histidine-Aspartate Kinase HK1 Paralogs in Response to Osmotic Stress.</title>
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<name sortKey="Hericourt, Francois" sort="Hericourt, Francois" uniqKey="Hericourt F" first="François" last="Héricourt">François Héricourt</name>
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<name sortKey="Maeda, Tatsuya" sort="Maeda, Tatsuya" uniqKey="Maeda T" first="Tatsuya" last="Maeda">Tatsuya Maeda</name>
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<nlm:affiliation>Institute of Molecular and Cellular Biosciences, The University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo 113-0032, Japan. maeda@iam.u-tokyo.ac.jp.</nlm:affiliation>
<country xml:lang="fr">Japon</country>
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<region type="région">Région de Kantō</region>
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<placeName>
<settlement type="city">Tokyo</settlement>
<region type="province">Région de Kantō</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Glevarec, Gaelle" sort="Glevarec, Gaelle" uniqKey="Glevarec G" first="Gaëlle" last="Glévarec">Gaëlle Glévarec</name>
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<nlm:affiliation>Biomolécules et Biotechnologies Végétales (BBV), EA 2106, Université François Rabelais de Tours, 31 avenue Monge, 37200 Tours, France. gaelle.glevarec@univ-tours.fr.</nlm:affiliation>
<country xml:lang="fr">France</country>
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</affiliation>
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<author>
<name sortKey="Carpin, Sabine" sort="Carpin, Sabine" uniqKey="Carpin S" first="Sabine" last="Carpin">Sabine Carpin</name>
<affiliation wicri:level="4">
<nlm:affiliation>Laboratoire de Biologie des Ligneux et des Grandes Cultures (LBLGC), Université d'Orléans, INRA, USC1328, 45067 Orléans, France. sabine.carpin@univ-orleans.fr.</nlm:affiliation>
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<title level="j">International journal of molecular sciences</title>
<idno type="eISSN">1422-0067</idno>
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<term>Amino Acids (metabolism)</term>
<term>Aspartic Acid (metabolism)</term>
<term>Gene Duplication (MeSH)</term>
<term>Gene Expression Regulation, Plant (MeSH)</term>
<term>Genetic Complementation Test (MeSH)</term>
<term>Histidine Kinase (MeSH)</term>
<term>Mutant Proteins (metabolism)</term>
<term>Mutation (genetics)</term>
<term>Osmotic Pressure (MeSH)</term>
<term>Phylogeny (MeSH)</term>
<term>Populus (enzymology)</term>
<term>Populus (genetics)</term>
<term>Protein Binding (MeSH)</term>
<term>Protein Multimerization (MeSH)</term>
<term>Reproducibility of Results (MeSH)</term>
<term>Sequence Homology, Amino Acid (MeSH)</term>
<term>Stress, Physiological (genetics)</term>
<term>Substrate Specificity (MeSH)</term>
<term>Two-Hybrid System Techniques (MeSH)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Acide aspartique (métabolisme)</term>
<term>Acides aminés (métabolisme)</term>
<term>Duplication de gène (MeSH)</term>
<term>Histidine kinase (MeSH)</term>
<term>Liaison aux protéines (MeSH)</term>
<term>Multimérisation de protéines (MeSH)</term>
<term>Mutation (génétique)</term>
<term>Phylogenèse (MeSH)</term>
<term>Populus (enzymologie)</term>
<term>Populus (génétique)</term>
<term>Pression osmotique (MeSH)</term>
<term>Protéines mutantes (métabolisme)</term>
<term>Reproductibilité des résultats (MeSH)</term>
<term>Régulation de l'expression des gènes végétaux (MeSH)</term>
<term>Similitude de séquences d'acides aminés (MeSH)</term>
<term>Spécificité du substrat (MeSH)</term>
<term>Stress physiologique (génétique)</term>
<term>Techniques de double hybride (MeSH)</term>
<term>Test de complémentation (MeSH)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en">
<term>Amino Acids</term>
<term>Aspartic Acid</term>
<term>Mutant Proteins</term>
</keywords>
<keywords scheme="MESH" qualifier="enzymologie" xml:lang="fr">
<term>Populus</term>
</keywords>
<keywords scheme="MESH" qualifier="enzymology" xml:lang="en">
<term>Populus</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en">
<term>Mutation</term>
<term>Populus</term>
<term>Stress, Physiological</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr">
<term>Mutation</term>
<term>Populus</term>
<term>Stress physiologique</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Acide aspartique</term>
<term>Acides aminés</term>
<term>Protéines mutantes</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Gene Duplication</term>
<term>Gene Expression Regulation, Plant</term>
<term>Genetic Complementation Test</term>
<term>Histidine Kinase</term>
<term>Osmotic Pressure</term>
<term>Phylogeny</term>
<term>Protein Binding</term>
<term>Protein Multimerization</term>
<term>Reproducibility of Results</term>
<term>Sequence Homology, Amino Acid</term>
<term>Substrate Specificity</term>
<term>Two-Hybrid System Techniques</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>Duplication de gène</term>
<term>Histidine kinase</term>
<term>Liaison aux protéines</term>
<term>Multimérisation de protéines</term>
<term>Phylogenèse</term>
<term>Pression osmotique</term>
<term>Reproductibilité des résultats</term>
<term>Régulation de l'expression des gènes végétaux</term>
<term>Similitude de séquences d'acides aminés</term>
<term>Spécificité du substrat</term>
<term>Techniques de double hybride</term>
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<div type="abstract" xml:lang="en">Previous works have shown the existence of protein partnerships belonging to a MultiStep Phosphorelay (MSP) in
<i>Populus</i>
putatively involved in osmosensing. This study is focused on the identification of a histidine-aspartate kinase, HK1b, paralog of HK1a. The characterization of HK1b showed its ability to homo- and hetero-dimerize and to interact with a few Histidine-containing Phosphotransfer (HPt) proteins, suggesting a preferential partnership in poplar MSP linked to drought perception. Furthermore, determinants for interaction specificity between HK1a/1b and HPts were studied by mutagenesis analysis, identifying amino acids involved in this specificity. The
<i>HK1b</i>
expression analysis in different poplar organs revealed its co-expression with three
<i>HPts</i>
, reinforcing the hypothesis of partnership participation in the MSP in planta. Moreover, HK1b was shown to act as an osmosensor with kinase activity in a functional complementation assay of an osmosensor deficient yeast strain. These results revealed that HK1b showed a different behaviour for canonical phosphorylation of histidine and aspartate residues. These phosphorylation modularities of canonical amino acids could explain the improved osmosensor performances observed in yeast. As conserved duplicates reflect the selective pressures imposed by the environmental requirements on the species, our results emphasize the importance of
<i>HK1</i>
gene duplication in poplar adaptation to drought stress.</div>
</front>
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<DateCompleted>
<Year>2017</Year>
<Month>04</Month>
<Day>03</Day>
</DateCompleted>
<DateRevised>
<Year>2018</Year>
<Month>11</Month>
<Day>13</Day>
</DateRevised>
<Article PubModel="Electronic">
<Journal>
<ISSN IssnType="Electronic">1422-0067</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>17</Volume>
<Issue>12</Issue>
<PubDate>
<Year>2016</Year>
<Month>Dec</Month>
<Day>08</Day>
</PubDate>
</JournalIssue>
<Title>International journal of molecular sciences</Title>
<ISOAbbreviation>Int J Mol Sci</ISOAbbreviation>
</Journal>
<ArticleTitle>Functional Divergence of Poplar Histidine-Aspartate Kinase HK1 Paralogs in Response to Osmotic Stress.</ArticleTitle>
<ELocationID EIdType="pii" ValidYN="Y">E2061</ELocationID>
<Abstract>
<AbstractText>Previous works have shown the existence of protein partnerships belonging to a MultiStep Phosphorelay (MSP) in
<i>Populus</i>
putatively involved in osmosensing. This study is focused on the identification of a histidine-aspartate kinase, HK1b, paralog of HK1a. The characterization of HK1b showed its ability to homo- and hetero-dimerize and to interact with a few Histidine-containing Phosphotransfer (HPt) proteins, suggesting a preferential partnership in poplar MSP linked to drought perception. Furthermore, determinants for interaction specificity between HK1a/1b and HPts were studied by mutagenesis analysis, identifying amino acids involved in this specificity. The
<i>HK1b</i>
expression analysis in different poplar organs revealed its co-expression with three
<i>HPts</i>
, reinforcing the hypothesis of partnership participation in the MSP in planta. Moreover, HK1b was shown to act as an osmosensor with kinase activity in a functional complementation assay of an osmosensor deficient yeast strain. These results revealed that HK1b showed a different behaviour for canonical phosphorylation of histidine and aspartate residues. These phosphorylation modularities of canonical amino acids could explain the improved osmosensor performances observed in yeast. As conserved duplicates reflect the selective pressures imposed by the environmental requirements on the species, our results emphasize the importance of
<i>HK1</i>
gene duplication in poplar adaptation to drought stress.</AbstractText>
</Abstract>
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<Author ValidYN="Y">
<LastName>Héricourt</LastName>
<ForeName>François</ForeName>
<Initials>F</Initials>
<AffiliationInfo>
<Affiliation>Laboratoire de Biologie des Ligneux et des Grandes Cultures (LBLGC), Université d'Orléans, INRA, USC1328, 45067 Orléans, France. francois.hericourt@univ-orleans.fr.</Affiliation>
</AffiliationInfo>
</Author>
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<LastName>Chefdor</LastName>
<ForeName>Françoise</ForeName>
<Initials>F</Initials>
<AffiliationInfo>
<Affiliation>Laboratoire de Biologie des Ligneux et des Grandes Cultures (LBLGC), Université d'Orléans, INRA, USC1328, 45067 Orléans, France. francoise.chefdor@univ-orleans.fr.</Affiliation>
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<LastName>Djeghdir</LastName>
<ForeName>Inès</ForeName>
<Initials>I</Initials>
<AffiliationInfo>
<Affiliation>Laboratoire de Biologie des Ligneux et des Grandes Cultures (LBLGC), Université d'Orléans, INRA, USC1328, 45067 Orléans, France. ines.djeghdir@univ-orleans.fr.</Affiliation>
</AffiliationInfo>
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<LastName>Larcher</LastName>
<ForeName>Mélanie</ForeName>
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<AffiliationInfo>
<Affiliation>Laboratoire de Biologie des Ligneux et des Grandes Cultures (LBLGC), Université d'Orléans, INRA, USC1328, 45067 Orléans, France. melanie.larcher@univ-orleans.fr.</Affiliation>
</AffiliationInfo>
</Author>
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<LastName>Lafontaine</LastName>
<ForeName>Florent</ForeName>
<Initials>F</Initials>
<AffiliationInfo>
<Affiliation>Biomolécules et Biotechnologies Végétales (BBV), EA 2106, Université François Rabelais de Tours, 31 avenue Monge, 37200 Tours, France. fllafontaine@univ-tours.fr.</Affiliation>
</AffiliationInfo>
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<LastName>Courdavault</LastName>
<ForeName>Vincent</ForeName>
<Initials>V</Initials>
<AffiliationInfo>
<Affiliation>Biomolécules et Biotechnologies Végétales (BBV), EA 2106, Université François Rabelais de Tours, 31 avenue Monge, 37200 Tours, France. vincent.courdavault@univ-tours.fr.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Auguin</LastName>
<ForeName>Daniel</ForeName>
<Initials>D</Initials>
<AffiliationInfo>
<Affiliation>Laboratoire de Biologie des Ligneux et des Grandes Cultures (LBLGC), Université d'Orléans, INRA, USC1328, 45067 Orléans, France. daniel.auguin@univ-orleans.fr.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Coste</LastName>
<ForeName>Franck</ForeName>
<Initials>F</Initials>
<AffiliationInfo>
<Affiliation>Centre de Biophysique Moléculaire (CBM), CNRS, 45071 Orléans, France. franck.coste@cnrs-orleans.fr.</Affiliation>
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</Author>
<Author ValidYN="Y">
<LastName>Depierreux</LastName>
<ForeName>Christiane</ForeName>
<Initials>C</Initials>
<AffiliationInfo>
<Affiliation>Laboratoire de Biologie des Ligneux et des Grandes Cultures (LBLGC), Université d'Orléans, INRA, USC1328, 45067 Orléans, France. christiane.depierreux@univ-orleans.fr.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Tanigawa</LastName>
<ForeName>Mirai</ForeName>
<Initials>M</Initials>
<AffiliationInfo>
<Affiliation>Institute of Molecular and Cellular Biosciences, The University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo 113-0032, Japan. las17mirai@yahoo.co.jp.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Maeda</LastName>
<ForeName>Tatsuya</ForeName>
<Initials>T</Initials>
<AffiliationInfo>
<Affiliation>Institute of Molecular and Cellular Biosciences, The University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo 113-0032, Japan. maeda@iam.u-tokyo.ac.jp.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Glévarec</LastName>
<ForeName>Gaëlle</ForeName>
<Initials>G</Initials>
<AffiliationInfo>
<Affiliation>Biomolécules et Biotechnologies Végétales (BBV), EA 2106, Université François Rabelais de Tours, 31 avenue Monge, 37200 Tours, France. gaelle.glevarec@univ-tours.fr.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Carpin</LastName>
<ForeName>Sabine</ForeName>
<Initials>S</Initials>
<AffiliationInfo>
<Affiliation>Laboratoire de Biologie des Ligneux et des Grandes Cultures (LBLGC), Université d'Orléans, INRA, USC1328, 45067 Orléans, France. sabine.carpin@univ-orleans.fr.</Affiliation>
</AffiliationInfo>
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<Year>2016</Year>
<Month>12</Month>
<Day>08</Day>
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<MeshHeading>
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<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
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<MeshHeading>
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<QualifierName UI="Q000201" MajorTopicYN="Y">enzymology</QualifierName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
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<MeshHeading>
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<MeshHeading>
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<Keyword MajorTopicYN="Y">Populus</Keyword>
<Keyword MajorTopicYN="Y">drought signaling</Keyword>
<Keyword MajorTopicYN="Y">histidine-aspartate kinase (HK)</Keyword>
<Keyword MajorTopicYN="Y">histidine-containing phosphotransfer protein (HPt)</Keyword>
<Keyword MajorTopicYN="Y">multistep phosphorelay (MSP)</Keyword>
<Keyword MajorTopicYN="Y">osmosensing</Keyword>
</KeywordList>
<CoiStatement>The authors declare no conflict of interest. The funding sponsors had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, and in the decision to publish the results.</CoiStatement>
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