Tomato expressing Arabidopsis glutaredoxin gene AtGRXS17 confers tolerance to chilling stress via modulating cold responsive components.
Identifieur interne : 000491 ( Main/Exploration ); précédent : 000490; suivant : 000492Tomato expressing Arabidopsis glutaredoxin gene AtGRXS17 confers tolerance to chilling stress via modulating cold responsive components.
Auteurs : Ying Hu [États-Unis] ; Qingyu Wu [États-Unis] ; Stuart A. Sprague [États-Unis] ; Jungeun Park [États-Unis] ; Myungmin Oh [États-Unis] ; C B Rajashekar [États-Unis] ; Hisashi Koiwa [États-Unis] ; Paul A. Nakata [États-Unis] ; Ninghui Cheng [États-Unis] ; Kendal D. Hirschi [États-Unis] ; Frank F. White [États-Unis] ; Sunghun Park [États-Unis]Source :
- Horticulture research [ 2052-7276 ] ; 2015.
Abstract
Chilling stress is a production constraint of tomato, a tropical origin, chilling-sensitive horticultural crop. The development of chilling tolerant tomato thus has significant potential to impact tomato production. Glutaredoxins (GRXs) are ubiquitous oxidoreductases, which utilize the reducing power of glutathione to reduce disulfide bonds of substrate proteins and maintain cellular redox homeostasis. Here, we report that tomato expressing Arabidopsis GRX gene AtGRXS17 conferred tolerance to chilling stress without adverse effects on growth and development. AtGRXS17-expressing tomato plants displayed lower ion leakage, higher maximal photochemical efficiency of photosystem II (Fv/Fm) and increased accumulation of soluble sugar compared with wild-type plants after the chilling stress challenge. Furthermore, chilling tolerance was correlated with increased antioxidant enzyme activities and reduced H2O2 accumulation. At the same time, temporal expression patterns of the endogenous C-repeat/DRE-binding factor 1 (SlCBF1) and CBF mediated-cold regulated genes were not altered in AtGRXS17-expressing plants when compared with wild-type plants, and proline concentrations remained unchanged relative to wild-type plants under chilling stress. Green fluorescent protein -AtGRXS17 fusion proteins, which were initially localized in the cytoplasm, migrated into the nucleus during chilling stress, reflecting a possible role of AtGRXS17 in nuclear signaling of chilling stress responses. Together, our findings demonstrate that genetically engineered tomato plants expressing AtGRXS17 can enhance chilling tolerance and suggest a genetic engineering strategy to improve chilling tolerance without yield penalty across different crop species.
DOI: 10.1038/hortres.2015.51
PubMed: 26623076
PubMed Central: PMC4641303
Affiliations:
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Sprague</name><affiliation wicri:level="2"><nlm:affiliation>Department of Horticulture, Forestry, and Recreation Resources, Kansas State University , Manhattan, KS 66506, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Horticulture, Forestry, and Recreation Resources, Kansas State University , Manhattan, KS 66506</wicri:regionArea><placeName><region type="state">Kansas</region></placeName></affiliation></author><author><name sortKey="Park, Jungeun" sort="Park, Jungeun" uniqKey="Park J" first="Jungeun" last="Park">Jungeun Park</name><affiliation wicri:level="2"><nlm:affiliation>Department of Horticulture, Forestry, and Recreation Resources, Kansas State University , Manhattan, KS 66506, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Horticulture, Forestry, and Recreation Resources, Kansas State University , Manhattan, KS 66506</wicri:regionArea><placeName><region type="state">Kansas</region></placeName></affiliation></author><author><name sortKey="Oh, Myungmin" sort="Oh, Myungmin" uniqKey="Oh M" first="Myungmin" last="Oh">Myungmin Oh</name><affiliation wicri:level="2"><nlm:affiliation>Department of Horticulture, Forestry, and Recreation Resources, Kansas State University , Manhattan, KS 66506, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Horticulture, Forestry, and Recreation Resources, Kansas State University , Manhattan, KS 66506</wicri:regionArea><placeName><region type="state">Kansas</region></placeName></affiliation></author><author><name sortKey="Rajashekar, C B" sort="Rajashekar, C B" uniqKey="Rajashekar C" first="C B" last="Rajashekar">C B Rajashekar</name><affiliation wicri:level="2"><nlm:affiliation>Department of Horticulture, Forestry, and Recreation Resources, Kansas State University , Manhattan, KS 66506, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Horticulture, Forestry, and Recreation Resources, Kansas State University , Manhattan, KS 66506</wicri:regionArea><placeName><region type="state">Kansas</region></placeName></affiliation></author><author><name sortKey="Koiwa, Hisashi" sort="Koiwa, Hisashi" uniqKey="Koiwa H" first="Hisashi" last="Koiwa">Hisashi Koiwa</name><affiliation wicri:level="2"><nlm:affiliation>Department of Horticultural Science, Texas A&M University , College Station, TX 77843, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Horticultural Science, Texas A&M University , College Station, TX 77843</wicri:regionArea><placeName><region type="state">Texas</region></placeName></affiliation></author><author><name sortKey="Nakata, Paul A" sort="Nakata, Paul A" uniqKey="Nakata P" first="Paul A" last="Nakata">Paul A. Nakata</name><affiliation wicri:level="2"><nlm:affiliation>United States Department of Agriculture/Agricultural Research Service, Children's Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine , Houston, TX 77030, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>United States Department of Agriculture/Agricultural Research Service, Children's Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine , Houston, TX 77030</wicri:regionArea><placeName><region type="state">Texas</region></placeName></affiliation></author><author><name sortKey="Cheng, Ninghui" sort="Cheng, Ninghui" uniqKey="Cheng N" first="Ninghui" last="Cheng">Ninghui Cheng</name><affiliation wicri:level="2"><nlm:affiliation>United States Department of Agriculture/Agricultural Research Service, Children's Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine , Houston, TX 77030, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>United States Department of Agriculture/Agricultural Research Service, Children's Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine , Houston, TX 77030</wicri:regionArea><placeName><region type="state">Texas</region></placeName></affiliation></author><author><name sortKey="Hirschi, Kendal D" sort="Hirschi, Kendal D" uniqKey="Hirschi K" first="Kendal D" last="Hirschi">Kendal D. Hirschi</name><affiliation wicri:level="2"><nlm:affiliation>United States Department of Agriculture/Agricultural Research Service, Children's Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine , Houston, TX 77030, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>United States Department of Agriculture/Agricultural Research Service, Children's Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine , Houston, TX 77030</wicri:regionArea><placeName><region type="state">Texas</region></placeName></affiliation></author><author><name sortKey="White, Frank F" sort="White, Frank F" uniqKey="White F" first="Frank F" last="White">Frank F. White</name><affiliation wicri:level="2"><nlm:affiliation>Department of Plant Pathology, Kansas State University , Manhattan, KS 66506, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Plant Pathology, Kansas State University , Manhattan, KS 66506</wicri:regionArea><placeName><region type="state">Kansas</region></placeName></affiliation></author><author><name sortKey="Park, Sunghun" sort="Park, Sunghun" uniqKey="Park S" first="Sunghun" last="Park">Sunghun Park</name><affiliation wicri:level="2"><nlm:affiliation>Department of Horticulture, Forestry, and Recreation Resources, Kansas State University , Manhattan, KS 66506, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Horticulture, Forestry, and Recreation Resources, Kansas State University , Manhattan, KS 66506</wicri:regionArea><placeName><region type="state">Kansas</region></placeName></affiliation></author></analytic><series><title level="j">Horticulture research</title><idno type="ISSN">2052-7276</idno><imprint><date when="2015" type="published">2015</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Chilling stress is a production constraint of tomato, a tropical origin, chilling-sensitive horticultural crop. The development of chilling tolerant tomato thus has significant potential to impact tomato production. Glutaredoxins (GRXs) are ubiquitous oxidoreductases, which utilize the reducing power of glutathione to reduce disulfide bonds of substrate proteins and maintain cellular redox homeostasis. Here, we report that tomato expressing Arabidopsis GRX gene AtGRXS17 conferred tolerance to chilling stress without adverse effects on growth and development. AtGRXS17-expressing tomato plants displayed lower ion leakage, higher maximal photochemical efficiency of photosystem II (Fv/Fm) and increased accumulation of soluble sugar compared with wild-type plants after the chilling stress challenge. Furthermore, chilling tolerance was correlated with increased antioxidant enzyme activities and reduced H2O2 accumulation. At the same time, temporal expression patterns of the endogenous C-repeat/DRE-binding factor 1 (SlCBF1) and CBF mediated-cold regulated genes were not altered in AtGRXS17-expressing plants when compared with wild-type plants, and proline concentrations remained unchanged relative to wild-type plants under chilling stress. Green fluorescent protein -AtGRXS17 fusion proteins, which were initially localized in the cytoplasm, migrated into the nucleus during chilling stress, reflecting a possible role of AtGRXS17 in nuclear signaling of chilling stress responses. Together, our findings demonstrate that genetically engineered tomato plants expressing AtGRXS17 can enhance chilling tolerance and suggest a genetic engineering strategy to improve chilling tolerance without yield penalty across different crop species. </div></front></TEI><pubmed><MedlineCitation Status="PubMed-not-MEDLINE" Owner="NLM"><PMID Version="1">26623076</PMID><DateCompleted><Year>2015</Year><Month>12</Month><Day>01</Day></DateCompleted><DateRevised><Year>2020</Year><Month>09</Month><Day>29</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Print">2052-7276</ISSN><JournalIssue CitedMedium="Print"><Volume>2</Volume><PubDate><Year>2015</Year></PubDate></JournalIssue><Title>Horticulture research</Title><ISOAbbreviation>Hortic Res</ISOAbbreviation></Journal><ArticleTitle>Tomato expressing Arabidopsis glutaredoxin gene AtGRXS17 confers tolerance to chilling stress via modulating cold responsive components.</ArticleTitle><Pagination><MedlinePgn>15051</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1038/hortres.2015.51</ELocationID><Abstract><AbstractText>Chilling stress is a production constraint of tomato, a tropical origin, chilling-sensitive horticultural crop. The development of chilling tolerant tomato thus has significant potential to impact tomato production. Glutaredoxins (GRXs) are ubiquitous oxidoreductases, which utilize the reducing power of glutathione to reduce disulfide bonds of substrate proteins and maintain cellular redox homeostasis. Here, we report that tomato expressing Arabidopsis GRX gene AtGRXS17 conferred tolerance to chilling stress without adverse effects on growth and development. AtGRXS17-expressing tomato plants displayed lower ion leakage, higher maximal photochemical efficiency of photosystem II (Fv/Fm) and increased accumulation of soluble sugar compared with wild-type plants after the chilling stress challenge. Furthermore, chilling tolerance was correlated with increased antioxidant enzyme activities and reduced H2O2 accumulation. At the same time, temporal expression patterns of the endogenous C-repeat/DRE-binding factor 1 (SlCBF1) and CBF mediated-cold regulated genes were not altered in AtGRXS17-expressing plants when compared with wild-type plants, and proline concentrations remained unchanged relative to wild-type plants under chilling stress. Green fluorescent protein -AtGRXS17 fusion proteins, which were initially localized in the cytoplasm, migrated into the nucleus during chilling stress, reflecting a possible role of AtGRXS17 in nuclear signaling of chilling stress responses. Together, our findings demonstrate that genetically engineered tomato plants expressing AtGRXS17 can enhance chilling tolerance and suggest a genetic engineering strategy to improve chilling tolerance without yield penalty across different crop species. </AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Hu</LastName><ForeName>Ying</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>Department of Horticulture, Forestry, and Recreation Resources, Kansas State University , Manhattan, KS 66506, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wu</LastName><ForeName>Qingyu</ForeName><Initials>Q</Initials><AffiliationInfo><Affiliation>Department of Horticulture, Forestry, and Recreation Resources, Kansas State University , Manhattan, KS 66506, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Sprague</LastName><ForeName>Stuart A</ForeName><Initials>SA</Initials><AffiliationInfo><Affiliation>Department of Horticulture, Forestry, and Recreation Resources, Kansas State University , Manhattan, KS 66506, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Park</LastName><ForeName>Jungeun</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Department of Horticulture, Forestry, and Recreation Resources, Kansas State University , Manhattan, KS 66506, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Oh</LastName><ForeName>Myungmin</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Department of Horticulture, Forestry, and Recreation Resources, Kansas State University , Manhattan, KS 66506, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Rajashekar</LastName><ForeName>C B</ForeName><Initials>CB</Initials><AffiliationInfo><Affiliation>Department of Horticulture, Forestry, and Recreation Resources, Kansas State University , Manhattan, KS 66506, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Koiwa</LastName><ForeName>Hisashi</ForeName><Initials>H</Initials><AffiliationInfo><Affiliation>Department of Horticultural Science, Texas A&M University , College Station, TX 77843, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Nakata</LastName><ForeName>Paul A</ForeName><Initials>PA</Initials><AffiliationInfo><Affiliation>United States Department of Agriculture/Agricultural Research Service, Children's Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine , Houston, TX 77030, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Cheng</LastName><ForeName>Ninghui</ForeName><Initials>N</Initials><AffiliationInfo><Affiliation>United States Department of Agriculture/Agricultural Research Service, Children's Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine , Houston, TX 77030, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hirschi</LastName><ForeName>Kendal D</ForeName><Initials>KD</Initials><AffiliationInfo><Affiliation>United States Department of Agriculture/Agricultural Research Service, Children's Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine , Houston, TX 77030, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>White</LastName><ForeName>Frank F</ForeName><Initials>FF</Initials><AffiliationInfo><Affiliation>Department of Plant Pathology, Kansas State University , Manhattan, KS 66506, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Park</LastName><ForeName>Sunghun</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Department of Horticulture, Forestry, and Recreation Resources, Kansas State University , Manhattan, KS 66506, USA.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2015</Year><Month>11</Month><Day>11</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>Hortic Res</MedlineTA><NlmUniqueID>101655540</NlmUniqueID><ISSNLinking>2052-7276</ISSNLinking></MedlineJournalInfo></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2015</Year><Month>10</Month><Day>01</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2015</Year><Month>10</Month><Day>04</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2015</Year><Month>12</Month><Day>2</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2015</Year><Month>12</Month><Day>2</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate 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