Proteomics of Heat-Stress and Ethylene-Mediated Thermotolerance Mechanisms in Tomato Pollen Grains.
Identifieur interne : 000231 ( Main/Exploration ); précédent : 000230; suivant : 000232Proteomics of Heat-Stress and Ethylene-Mediated Thermotolerance Mechanisms in Tomato Pollen Grains.
Auteurs : Sridharan Jegadeesan [Israël] ; Palak Chaturvedi [Autriche] ; Arindam Ghatak [Autriche] ; Etan Pressman [Israël] ; Shimon Meir [Israël] ; Adi Faigenboim [Israël] ; Nicholas Rutley [Israël] ; Avital Beery [Israël] ; Arye Harel [Israël] ; Wolfram Weckwerth [Autriche] ; Nurit Firon [Israël]Source :
- Frontiers in plant science [ 1664-462X ] ; 2018.
Abstract
Heat stress is a major cause for yield loss in many crops, including vegetable crops. Even short waves of high temperature, becoming more frequent during recent years, can be detrimental. Pollen development is most heat-sensitive, being the main cause for reduced productivity under heat-stress across a wide range of crops. The molecular mechanisms involved in pollen heat-stress response and thermotolerance are however, not fully understood. Recently, we have demonstrated that ethylene, a gaseous plant hormone, plays a role in tomato (Solanum lycopersicum) pollen thermotolerance. These results were substantiated in the current work showing that increasing ethylene levels by using an ethylene-releasing substance, ethephon, prior to heat-stress exposure, increased pollen quality. A proteomic approach was undertaken, to unravel the mechanisms underlying pollen heat-stress response and ethylene-mediated pollen thermotolerance in developing pollen grains. Proteins were extracted and analyzed by means of a gel LC-MS fractionation protocol, and a total of 1,355 proteins were identified. A dataset of 721 proteins, detected in three biological replicates of at least one of the applied treatments, was used for all analyses. Quantitative analysis was performed based on peptide count. The analysis revealed that heat-stress affected the developmental program of pollen, including protein homeostasis (components of the translational and degradation machinery), carbohydrate, and energy metabolism. Ethephon-pre-treatment shifted the heat-stressed pollen proteome closer to the proteome under non-stressful conditions, namely, by showing higher abundance of proteins involved in protein synthesis, degradation, tricarboxylic acid cycle, and RNA regulation. Furthermore, up-regulation of protective mechanisms against oxidative stress was observed following ethephon-treatment (including higher abundance of glutathione-disulfide reductase, glutaredoxin, and protein disulfide isomerase). Taken together, the findings identified systemic and fundamental components of pollen thermotolerance, and serve as a valuable quantitative protein database for further research.
DOI: 10.3389/fpls.2018.01558
PubMed: 30483278
PubMed Central: PMC6240657
Affiliations:
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Thermotolerance Mechanisms in Tomato Pollen Grains.</title><author><name sortKey="Jegadeesan, Sridharan" sort="Jegadeesan, Sridharan" uniqKey="Jegadeesan S" first="Sridharan" last="Jegadeesan">Sridharan Jegadeesan</name><affiliation wicri:level="1"><nlm:affiliation>Institute of Plant Sciences, Agricultural Research Organization, Volcani Center, Rishon LeZion, Israel.</nlm:affiliation><country xml:lang="fr">Israël</country><wicri:regionArea>Institute of Plant Sciences, Agricultural Research Organization, Volcani Center, Rishon LeZion</wicri:regionArea><wicri:noRegion>Rishon LeZion</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>The Robert H. Smith Faculty of Agriculture, Food and Environment, The Robert H. Smith Institute of Plant Sciences and Genetics in Agriculture of The Hebrew University of Jerusalem, Rehovot, Israel.</nlm:affiliation><country xml:lang="fr">Israël</country><wicri:regionArea>The Robert H. Smith Faculty of Agriculture, Food and Environment, The Robert H. Smith Institute of Plant Sciences and Genetics in Agriculture of The Hebrew University of Jerusalem, Rehovot</wicri:regionArea><wicri:noRegion>Rehovot</wicri:noRegion></affiliation></author><author><name sortKey="Chaturvedi, Palak" sort="Chaturvedi, Palak" uniqKey="Chaturvedi P" first="Palak" last="Chaturvedi">Palak Chaturvedi</name><affiliation wicri:level="3"><nlm:affiliation>Department of Ecogenomics and Systems Biology, Faculty of Life Sciences, University of Vienna, Vienna, Austria.</nlm:affiliation><country xml:lang="fr">Autriche</country><wicri:regionArea>Department of Ecogenomics and Systems Biology, Faculty of Life Sciences, University of Vienna, Vienna</wicri:regionArea><placeName><settlement type="city">Vienne (Autriche)</settlement><region nuts="2" type="province">Vienne (Autriche)</region></placeName></affiliation><affiliation wicri:level="3"><nlm:affiliation>Vienna Metabolomics Center, University of Vienna, Vienna, Austria.</nlm:affiliation><country 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University of Vienna, Vienna, Austria.</nlm:affiliation><country xml:lang="fr">Autriche</country><wicri:regionArea>Vienna Metabolomics Center, University of Vienna, Vienna</wicri:regionArea><placeName><settlement type="city">Vienne (Autriche)</settlement><region nuts="2" type="province">Vienne (Autriche)</region></placeName></affiliation></author><author><name sortKey="Pressman, Etan" sort="Pressman, Etan" uniqKey="Pressman E" first="Etan" last="Pressman">Etan Pressman</name><affiliation wicri:level="1"><nlm:affiliation>Institute of Plant Sciences, Agricultural Research Organization, Volcani Center, Rishon LeZion, Israel.</nlm:affiliation><country xml:lang="fr">Israël</country><wicri:regionArea>Institute of Plant Sciences, Agricultural Research Organization, Volcani Center, Rishon LeZion</wicri:regionArea><wicri:noRegion>Rishon LeZion</wicri:noRegion></affiliation></author><author><name sortKey="Meir, Shimon" sort="Meir, Shimon" uniqKey="Meir S" first="Shimon" last="Meir">Shimon Meir</name><affiliation wicri:level="1"><nlm:affiliation>Institute of Postharvest and Food Sciences, Agricultural Research Organization, Volcani Center, Rishon LeZion, Israel.</nlm:affiliation><country xml:lang="fr">Israël</country><wicri:regionArea>Institute of Postharvest and Food Sciences, Agricultural Research Organization, Volcani Center, Rishon LeZion</wicri:regionArea><wicri:noRegion>Rishon LeZion</wicri:noRegion></affiliation></author><author><name sortKey="Faigenboim, Adi" sort="Faigenboim, Adi" uniqKey="Faigenboim A" first="Adi" last="Faigenboim">Adi Faigenboim</name><affiliation wicri:level="1"><nlm:affiliation>Institute of Plant Sciences, Agricultural Research Organization, Volcani Center, Rishon LeZion, Israel.</nlm:affiliation><country xml:lang="fr">Israël</country><wicri:regionArea>Institute of Plant Sciences, Agricultural Research Organization, Volcani Center, Rishon LeZion</wicri:regionArea><wicri:noRegion>Rishon LeZion</wicri:noRegion></affiliation></author><author><name sortKey="Rutley, Nicholas" sort="Rutley, Nicholas" uniqKey="Rutley N" first="Nicholas" last="Rutley">Nicholas Rutley</name><affiliation wicri:level="1"><nlm:affiliation>Institute of Plant Sciences, Agricultural Research Organization, Volcani Center, Rishon LeZion, Israel.</nlm:affiliation><country xml:lang="fr">Israël</country><wicri:regionArea>Institute of Plant Sciences, Agricultural Research Organization, Volcani Center, Rishon LeZion</wicri:regionArea><wicri:noRegion>Rishon LeZion</wicri:noRegion></affiliation></author><author><name sortKey="Beery, Avital" sort="Beery, Avital" uniqKey="Beery A" first="Avital" last="Beery">Avital Beery</name><affiliation wicri:level="1"><nlm:affiliation>Institute of Plant Sciences, Agricultural Research Organization, Volcani Center, Rishon LeZion, Israel.</nlm:affiliation><country xml:lang="fr">Israël</country><wicri:regionArea>Institute of Plant Sciences, Agricultural Research Organization, Volcani Center, Rishon LeZion</wicri:regionArea><wicri:noRegion>Rishon LeZion</wicri:noRegion></affiliation></author><author><name sortKey="Harel, Arye" sort="Harel, Arye" uniqKey="Harel A" first="Arye" last="Harel">Arye Harel</name><affiliation wicri:level="1"><nlm:affiliation>Institute of Plant Sciences, Agricultural Research Organization, Volcani Center, Rishon LeZion, Israel.</nlm:affiliation><country xml:lang="fr">Israël</country><wicri:regionArea>Institute of Plant Sciences, Agricultural Research Organization, Volcani Center, Rishon LeZion</wicri:regionArea><wicri:noRegion>Rishon LeZion</wicri:noRegion></affiliation></author><author><name sortKey="Weckwerth, Wolfram" sort="Weckwerth, Wolfram" uniqKey="Weckwerth W" first="Wolfram" last="Weckwerth">Wolfram Weckwerth</name><affiliation wicri:level="3"><nlm:affiliation>Department of Ecogenomics and Systems Biology, Faculty of Life Sciences, University of Vienna, Vienna, Austria.</nlm:affiliation><country xml:lang="fr">Autriche</country><wicri:regionArea>Department of Ecogenomics and Systems Biology, Faculty of Life Sciences, University of Vienna, Vienna</wicri:regionArea><placeName><settlement type="city">Vienne (Autriche)</settlement><region nuts="2" type="province">Vienne (Autriche)</region></placeName></affiliation><affiliation wicri:level="3"><nlm:affiliation>Vienna Metabolomics Center, University of Vienna, Vienna, Austria.</nlm:affiliation><country xml:lang="fr">Autriche</country><wicri:regionArea>Vienna Metabolomics Center, University of Vienna, Vienna</wicri:regionArea><placeName><settlement type="city">Vienne (Autriche)</settlement><region nuts="2" type="province">Vienne (Autriche)</region></placeName></affiliation></author><author><name sortKey="Firon, Nurit" sort="Firon, Nurit" uniqKey="Firon N" first="Nurit" last="Firon">Nurit Firon</name><affiliation wicri:level="1"><nlm:affiliation>Institute of Plant Sciences, Agricultural Research Organization, Volcani Center, Rishon LeZion, Israel.</nlm:affiliation><country xml:lang="fr">Israël</country><wicri:regionArea>Institute of Plant Sciences, Agricultural Research Organization, Volcani Center, Rishon LeZion</wicri:regionArea><wicri:noRegion>Rishon LeZion</wicri:noRegion></affiliation></author></analytic><series><title level="j">Frontiers in plant science</title><idno type="ISSN">1664-462X</idno><imprint><date when="2018" type="published">2018</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Heat stress is a major cause for yield loss in many crops, including vegetable crops. Even short waves of high temperature, becoming more frequent during recent years, can be detrimental. Pollen development is most heat-sensitive, being the main cause for reduced productivity under heat-stress across a wide range of crops. The molecular mechanisms involved in pollen heat-stress response and thermotolerance are however, not fully understood. Recently, we have demonstrated that ethylene, a gaseous plant hormone, plays a role in tomato (<i>Solanum lycopersicum</i>) pollen thermotolerance. These results were substantiated in the current work showing that increasing ethylene levels by using an ethylene-releasing substance, ethephon, prior to heat-stress exposure, increased pollen quality. A proteomic approach was undertaken, to unravel the mechanisms underlying pollen heat-stress response and ethylene-mediated pollen thermotolerance in developing pollen grains. Proteins were extracted and analyzed by means of a gel LC-MS fractionation protocol, and a total of 1,355 proteins were identified. A dataset of 721 proteins, detected in three biological replicates of at least one of the applied treatments, was used for all analyses. Quantitative analysis was performed based on peptide count. The analysis revealed that heat-stress affected the developmental program of pollen, including protein homeostasis (components of the translational and degradation machinery), carbohydrate, and energy metabolism. Ethephon-pre-treatment shifted the heat-stressed pollen proteome closer to the proteome under non-stressful conditions, namely, by showing higher abundance of proteins involved in protein synthesis, degradation, tricarboxylic acid cycle, and RNA regulation. Furthermore, up-regulation of protective mechanisms against oxidative stress was observed following ethephon-treatment (including higher abundance of glutathione-disulfide reductase, glutaredoxin, and protein disulfide isomerase). Taken together, the findings identified systemic and fundamental components of pollen thermotolerance, and serve as a valuable quantitative protein database for further research.</div></front></TEI><pubmed><MedlineCitation Status="PubMed-not-MEDLINE" Owner="NLM"><PMID Version="1">30483278</PMID><DateRevised><Year>2020</Year><Month>09</Month><Day>30</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Print">1664-462X</ISSN><JournalIssue CitedMedium="Print"><Volume>9</Volume><PubDate><Year>2018</Year></PubDate></JournalIssue><Title>Frontiers in plant science</Title><ISOAbbreviation>Front Plant Sci</ISOAbbreviation></Journal><ArticleTitle>Proteomics of Heat-Stress and Ethylene-Mediated Thermotolerance Mechanisms in Tomato Pollen Grains.</ArticleTitle><Pagination><MedlinePgn>1558</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.3389/fpls.2018.01558</ELocationID><Abstract><AbstractText>Heat stress is a major cause for yield loss in many crops, including vegetable crops. Even short waves of high temperature, becoming more frequent during recent years, can be detrimental. Pollen development is most heat-sensitive, being the main cause for reduced productivity under heat-stress across a wide range of crops. The molecular mechanisms involved in pollen heat-stress response and thermotolerance are however, not fully understood. Recently, we have demonstrated that ethylene, a gaseous plant hormone, plays a role in tomato (<i>Solanum lycopersicum</i>) pollen thermotolerance. These results were substantiated in the current work showing that increasing ethylene levels by using an ethylene-releasing substance, ethephon, prior to heat-stress exposure, increased pollen quality. A proteomic approach was undertaken, to unravel the mechanisms underlying pollen heat-stress response and ethylene-mediated pollen thermotolerance in developing pollen grains. Proteins were extracted and analyzed by means of a gel LC-MS fractionation protocol, and a total of 1,355 proteins were identified. A dataset of 721 proteins, detected in three biological replicates of at least one of the applied treatments, was used for all analyses. Quantitative analysis was performed based on peptide count. The analysis revealed that heat-stress affected the developmental program of pollen, including protein homeostasis (components of the translational and degradation machinery), carbohydrate, and energy metabolism. Ethephon-pre-treatment shifted the heat-stressed pollen proteome closer to the proteome under non-stressful conditions, namely, by showing higher abundance of proteins involved in protein synthesis, degradation, tricarboxylic acid cycle, and RNA regulation. Furthermore, up-regulation of protective mechanisms against oxidative stress was observed following ethephon-treatment (including higher abundance of glutathione-disulfide reductase, glutaredoxin, and protein disulfide isomerase). Taken together, the findings identified systemic and fundamental components of pollen thermotolerance, and serve as a valuable quantitative protein database for further research.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Jegadeesan</LastName><ForeName>Sridharan</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Institute of Plant Sciences, Agricultural Research Organization, Volcani Center, Rishon LeZion, Israel.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>The Robert H. Smith Faculty of Agriculture, Food and Environment, The Robert H. Smith Institute of Plant Sciences and Genetics in Agriculture of The Hebrew University of Jerusalem, Rehovot, Israel.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Chaturvedi</LastName><ForeName>Palak</ForeName><Initials>P</Initials><AffiliationInfo><Affiliation>Department of Ecogenomics and Systems Biology, Faculty of Life Sciences, University of Vienna, Vienna, Austria.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Vienna Metabolomics Center, University of Vienna, Vienna, Austria.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ghatak</LastName><ForeName>Arindam</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Department of Ecogenomics and Systems Biology, Faculty of Life Sciences, University of Vienna, Vienna, Austria.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Vienna Metabolomics Center, University of Vienna, Vienna, Austria.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Pressman</LastName><ForeName>Etan</ForeName><Initials>E</Initials><AffiliationInfo><Affiliation>Institute of Plant Sciences, Agricultural Research Organization, Volcani Center, Rishon LeZion, Israel.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Meir</LastName><ForeName>Shimon</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Institute of Postharvest and Food Sciences, Agricultural Research Organization, Volcani Center, Rishon LeZion, Israel.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Faigenboim</LastName><ForeName>Adi</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Institute of Plant Sciences, Agricultural Research Organization, Volcani Center, Rishon LeZion, Israel.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Rutley</LastName><ForeName>Nicholas</ForeName><Initials>N</Initials><AffiliationInfo><Affiliation>Institute of Plant Sciences, Agricultural Research Organization, Volcani Center, Rishon LeZion, Israel.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Beery</LastName><ForeName>Avital</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Institute of Plant Sciences, Agricultural Research Organization, Volcani Center, Rishon LeZion, Israel.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Harel</LastName><ForeName>Arye</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Institute of Plant Sciences, Agricultural Research Organization, Volcani Center, Rishon LeZion, Israel.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Weckwerth</LastName><ForeName>Wolfram</ForeName><Initials>W</Initials><AffiliationInfo><Affiliation>Department of Ecogenomics and Systems Biology, Faculty of Life Sciences, University of Vienna, Vienna, Austria.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Vienna Metabolomics Center, University of Vienna, Vienna, Austria.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Firon</LastName><ForeName>Nurit</ForeName><Initials>N</Initials><AffiliationInfo><Affiliation>Institute of Plant Sciences, Agricultural Research Organization, Volcani Center, Rishon LeZion, Israel.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2018</Year><Month>11</Month><Day>12</Day></ArticleDate></Article><MedlineJournalInfo><Country>Switzerland</Country><MedlineTA>Front Plant Sci</MedlineTA><NlmUniqueID>101568200</NlmUniqueID><ISSNLinking>1664-462X</ISSNLinking></MedlineJournalInfo><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Solanum lycopersicum</Keyword><Keyword MajorTopicYN="N">ethylene</Keyword><Keyword MajorTopicYN="N">heat-stress</Keyword><Keyword MajorTopicYN="N">pollen</Keyword><Keyword 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