Overexpression of an apple LysM-containing protein gene, MdCERK1-2, confers improved resistance to the pathogenic fungus, Alternaria alternata, in Nicotiana benthamiana.
Identifieur interne : 000093 ( Main/Exploration ); précédent : 000092; suivant : 000094Overexpression of an apple LysM-containing protein gene, MdCERK1-2, confers improved resistance to the pathogenic fungus, Alternaria alternata, in Nicotiana benthamiana.
Auteurs : Qiming Chen [République populaire de Chine] ; Chaohua Dong [République populaire de Chine] ; Xiaohong Sun [République populaire de Chine] ; Yugang Zhang [République populaire de Chine] ; Hongyi Dai [République populaire de Chine] ; Suhua Bai [République populaire de Chine]Source :
- BMC plant biology [ 1471-2229 ] ; 2020.
Abstract
BACKGROUND
Lysin motif (LysM)-containing proteins are involved in the recognition of fungal and bacterial pathogens. However, few studies have reported on their roles in the defense responses of woody plants against pathogens. A previous study reported that the apple MdCERK1 gene was induced by chitin and Rhizoctonia solani, and its protein can bind to chitin. However, its effect on defense responses has not been investigated.
RESULTS
In this study, a new apple CERK gene, designated as MdCERK1-2, was identified. It encodes a protein that shares high sequence identity with the previously reported MdCERK1 and AtCERK1. Its chitin binding ability and subcellular location are similar to MdCERK1 and AtCERK1, suggesting that MdCERK1-2 may play a role in apple immune defense responses as a pattern recognition receptor (PRR). MdCERK1-2 expression in apple was induced by 2 fungal pathogens, Botryosphaeria dothidea and Glomerella cingulate, but not by the bacterial pathogen, Erwinia amylovora, indicating that MdCERK1-2 is involved in apple anti-fungal defense responses. Further functional analysis by heterologous overexpression (OE) in Nicotiana benthamiana (Nb) demonstrated that MdCERK1-2 OE improved Nb resistance to the pathogenic fungus, Alternaria alternata. H
CONCLUSIONS
Heterologous MdCERK1-2 OE affects multiple defense responses in Nb plants and increased their resistance to fungal pathogens. This result also suggests that MdCERK1-2 is involved in apple defense responses against pathogenic fungi.
DOI: 10.1186/s12870-020-02361-z
PubMed: 32268888
PubMed Central: PMC7386173
Affiliations:
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Genetic Improvement and Breeding in Horticultural Plants, Qingdao Agricultural University, Qingdao, 266109, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Qingdao Key Laboratory of Genetic Improvement and Breeding in Horticultural Plants, Qingdao Agricultural University, Qingdao, 266109</wicri:regionArea><wicri:noRegion>266109</wicri:noRegion></affiliation></author><author><name sortKey="Zhang, Yugang" sort="Zhang, Yugang" uniqKey="Zhang Y" first="Yugang" last="Zhang">Yugang Zhang</name><affiliation wicri:level="1"><nlm:affiliation>Qingdao Key Laboratory of Genetic Improvement and Breeding in Horticultural Plants, Qingdao Agricultural University, Qingdao, 266109, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Qingdao Key Laboratory of Genetic Improvement and Breeding in Horticultural Plants, Qingdao Agricultural University, Qingdao, 266109</wicri:regionArea><wicri:noRegion>266109</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>College of Horticulture, Qingdao Agricultural University, Qingdao, 266109, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>College of Horticulture, Qingdao Agricultural University, Qingdao, 266109</wicri:regionArea><wicri:noRegion>266109</wicri:noRegion></affiliation></author><author><name sortKey="Dai, Hongyi" sort="Dai, Hongyi" uniqKey="Dai H" first="Hongyi" last="Dai">Hongyi Dai</name><affiliation wicri:level="1"><nlm:affiliation>Qingdao Key Laboratory of Genetic Improvement and Breeding in Horticultural Plants, Qingdao Agricultural University, Qingdao, 266109, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Qingdao Key Laboratory of Genetic Improvement and Breeding in Horticultural Plants, Qingdao Agricultural University, Qingdao, 266109</wicri:regionArea><wicri:noRegion>266109</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>College of Horticulture, Qingdao Agricultural University, Qingdao, 266109, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>College of Horticulture, Qingdao Agricultural University, Qingdao, 266109</wicri:regionArea><wicri:noRegion>266109</wicri:noRegion></affiliation></author><author><name sortKey="Bai, Suhua" sort="Bai, Suhua" uniqKey="Bai S" first="Suhua" last="Bai">Suhua Bai</name><affiliation wicri:level="1"><nlm:affiliation>College of Life Sciences, Key Laboratory of Plant Biotechnology of Shandong Province, Qingdao Agricultural University, 700 Changcheng Road, Qingdao, 266109, China. shbai0402@126.com.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>College of Life Sciences, Key Laboratory of Plant Biotechnology of Shandong Province, Qingdao Agricultural 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uniqKey="Chen Q" first="Qiming" last="Chen">Qiming Chen</name><affiliation wicri:level="1"><nlm:affiliation>College of Life Sciences, Key Laboratory of Plant Biotechnology of Shandong Province, Qingdao Agricultural University, 700 Changcheng Road, Qingdao, 266109, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>College of Life Sciences, Key Laboratory of Plant Biotechnology of Shandong Province, Qingdao Agricultural University, 700 Changcheng Road, Qingdao, 266109</wicri:regionArea><wicri:noRegion>266109</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Qingdao Key Laboratory of Genetic Improvement and Breeding in Horticultural Plants, Qingdao Agricultural University, Qingdao, 266109, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Qingdao Key Laboratory of Genetic Improvement and Breeding in Horticultural Plants, Qingdao Agricultural University, Qingdao, 266109</wicri:regionArea><wicri:noRegion>266109</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Shandong Province Key Laboratory of Applied Mycology, Qingdao, 266109, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Shandong Province Key Laboratory of Applied Mycology, Qingdao, 266109</wicri:regionArea><wicri:noRegion>266109</wicri:noRegion></affiliation></author><author><name sortKey="Dong, Chaohua" sort="Dong, Chaohua" uniqKey="Dong C" first="Chaohua" last="Dong">Chaohua Dong</name><affiliation wicri:level="1"><nlm:affiliation>College of Life Sciences, Key Laboratory of Plant Biotechnology of Shandong Province, Qingdao Agricultural University, 700 Changcheng Road, Qingdao, 266109, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>College of Life Sciences, Key Laboratory of Plant Biotechnology of Shandong Province, Qingdao Agricultural University, 700 Changcheng Road, Qingdao, 266109</wicri:regionArea><wicri:noRegion>266109</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Qingdao Key Laboratory of Genetic Improvement and Breeding in Horticultural Plants, Qingdao Agricultural University, Qingdao, 266109, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Qingdao Key Laboratory of Genetic Improvement and Breeding in Horticultural Plants, Qingdao Agricultural University, Qingdao, 266109</wicri:regionArea><wicri:noRegion>266109</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Shandong Province Key Laboratory of Applied Mycology, Qingdao, 266109, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Shandong Province Key Laboratory of Applied Mycology, Qingdao, 266109</wicri:regionArea><wicri:noRegion>266109</wicri:noRegion></affiliation></author><author><name sortKey="Sun, Xiaohong" sort="Sun, Xiaohong" uniqKey="Sun X" first="Xiaohong" last="Sun">Xiaohong Sun</name><affiliation wicri:level="1"><nlm:affiliation>College of Life Sciences, Key Laboratory of Plant Biotechnology of Shandong Province, Qingdao Agricultural University, 700 Changcheng Road, Qingdao, 266109, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>College of Life Sciences, Key Laboratory of Plant Biotechnology of Shandong Province, Qingdao Agricultural University, 700 Changcheng Road, Qingdao, 266109</wicri:regionArea><wicri:noRegion>266109</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Qingdao Key Laboratory of Genetic Improvement and Breeding in Horticultural Plants, Qingdao Agricultural University, Qingdao, 266109, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Qingdao Key Laboratory of Genetic Improvement and Breeding in Horticultural Plants, Qingdao Agricultural University, Qingdao, 266109</wicri:regionArea><wicri:noRegion>266109</wicri:noRegion></affiliation></author><author><name sortKey="Zhang, Yugang" sort="Zhang, Yugang" uniqKey="Zhang Y" first="Yugang" last="Zhang">Yugang Zhang</name><affiliation wicri:level="1"><nlm:affiliation>Qingdao Key Laboratory of Genetic Improvement and Breeding in Horticultural Plants, Qingdao Agricultural University, Qingdao, 266109, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Qingdao Key Laboratory of Genetic Improvement and Breeding in Horticultural Plants, Qingdao Agricultural University, Qingdao, 266109</wicri:regionArea><wicri:noRegion>266109</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>College of Horticulture, Qingdao Agricultural University, Qingdao, 266109, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>College of Horticulture, Qingdao Agricultural University, Qingdao, 266109</wicri:regionArea><wicri:noRegion>266109</wicri:noRegion></affiliation></author><author><name sortKey="Dai, Hongyi" sort="Dai, Hongyi" uniqKey="Dai H" first="Hongyi" last="Dai">Hongyi Dai</name><affiliation wicri:level="1"><nlm:affiliation>Qingdao Key Laboratory of Genetic Improvement and Breeding in Horticultural Plants, Qingdao Agricultural University, Qingdao, 266109, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Qingdao Key Laboratory of Genetic Improvement and Breeding in Horticultural Plants, Qingdao Agricultural University, Qingdao, 266109</wicri:regionArea><wicri:noRegion>266109</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>College of Horticulture, Qingdao Agricultural University, Qingdao, 266109, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>College of Horticulture, Qingdao Agricultural University, Qingdao, 266109</wicri:regionArea><wicri:noRegion>266109</wicri:noRegion></affiliation></author><author><name sortKey="Bai, Suhua" sort="Bai, Suhua" uniqKey="Bai S" first="Suhua" last="Bai">Suhua Bai</name><affiliation wicri:level="1"><nlm:affiliation>College of Life Sciences, Key Laboratory of Plant Biotechnology of Shandong Province, Qingdao Agricultural University, 700 Changcheng Road, Qingdao, 266109, China. shbai0402@126.com.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>College of Life Sciences, Key Laboratory of Plant Biotechnology of Shandong Province, Qingdao Agricultural University, 700 Changcheng Road, Qingdao, 266109</wicri:regionArea><wicri:noRegion>266109</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Qingdao Key Laboratory of Genetic Improvement and Breeding in Horticultural Plants, Qingdao Agricultural University, Qingdao, 266109, China. shbai0402@126.com.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Qingdao Key Laboratory of Genetic Improvement and Breeding in Horticultural Plants, Qingdao Agricultural University, Qingdao, 266109</wicri:regionArea><wicri:noRegion>266109</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Shandong Province Key Laboratory of Applied Mycology, Qingdao, 266109, China. shbai0402@126.com.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Shandong Province Key Laboratory of Applied Mycology, Qingdao, 266109</wicri:regionArea><wicri:noRegion>266109</wicri:noRegion></affiliation></author></analytic><series><title level="j">BMC plant biology</title><idno type="eISSN">1471-2229</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p><b>BACKGROUND</b></p><p>Lysin motif (LysM)-containing proteins are involved in the recognition of fungal and bacterial pathogens. However, few studies have reported on their roles in the defense responses of woody plants against pathogens. A previous study reported that the apple MdCERK1 gene was induced by chitin and Rhizoctonia solani, and its protein can bind to chitin. However, its effect on defense responses has not been investigated.</p></div><div type="abstract" xml:lang="en"><p><b>RESULTS</b></p><p>In this study, a new apple CERK gene, designated as MdCERK1-2, was identified. It encodes a protein that shares high sequence identity with the previously reported MdCERK1 and AtCERK1. Its chitin binding ability and subcellular location are similar to MdCERK1 and AtCERK1, suggesting that MdCERK1-2 may play a role in apple immune defense responses as a pattern recognition receptor (PRR). MdCERK1-2 expression in apple was induced by 2 fungal pathogens, Botryosphaeria dothidea and Glomerella cingulate, but not by the bacterial pathogen, Erwinia amylovora, indicating that MdCERK1-2 is involved in apple anti-fungal defense responses. Further functional analysis by heterologous overexpression (OE) in Nicotiana benthamiana (Nb) demonstrated that MdCERK1-2 OE improved Nb resistance to the pathogenic fungus, Alternaria alternata. H</p></div><div type="abstract" xml:lang="en"><p><b>CONCLUSIONS</b></p><p>Heterologous MdCERK1-2 OE affects multiple defense responses in Nb plants and increased their resistance to fungal pathogens. This result also suggests that MdCERK1-2 is involved in apple defense responses against pathogenic fungi.</p></div></front></TEI><pubmed><MedlineCitation Status="In-Process" Owner="NLM"><PMID Version="1">32268888</PMID><DateRevised><Year>2020</Year><Month>07</Month><Day>30</Day></DateRevised><Article PubModel="Electronic"><Journal><ISSN IssnType="Electronic">1471-2229</ISSN><JournalIssue CitedMedium="Internet"><Volume>20</Volume><Issue>1</Issue><PubDate><Year>2020</Year><Month>Apr</Month><Day>08</Day></PubDate></JournalIssue><Title>BMC plant biology</Title><ISOAbbreviation>BMC Plant Biol</ISOAbbreviation></Journal><ArticleTitle>Overexpression of an apple LysM-containing protein gene, MdCERK1-2, confers improved resistance to the pathogenic fungus, Alternaria alternata, in Nicotiana benthamiana.</ArticleTitle><Pagination><MedlinePgn>146</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1186/s12870-020-02361-z</ELocationID><Abstract><AbstractText Label="BACKGROUND" NlmCategory="BACKGROUND">Lysin motif (LysM)-containing proteins are involved in the recognition of fungal and bacterial pathogens. However, few studies have reported on their roles in the defense responses of woody plants against pathogens. A previous study reported that the apple MdCERK1 gene was induced by chitin and Rhizoctonia solani, and its protein can bind to chitin. However, its effect on defense responses has not been investigated.</AbstractText><AbstractText Label="RESULTS" NlmCategory="RESULTS">In this study, a new apple CERK gene, designated as MdCERK1-2, was identified. It encodes a protein that shares high sequence identity with the previously reported MdCERK1 and AtCERK1. Its chitin binding ability and subcellular location are similar to MdCERK1 and AtCERK1, suggesting that MdCERK1-2 may play a role in apple immune defense responses as a pattern recognition receptor (PRR). MdCERK1-2 expression in apple was induced by 2 fungal pathogens, Botryosphaeria dothidea and Glomerella cingulate, but not by the bacterial pathogen, Erwinia amylovora, indicating that MdCERK1-2 is involved in apple anti-fungal defense responses. Further functional analysis by heterologous overexpression (OE) in Nicotiana benthamiana (Nb) demonstrated that MdCERK1-2 OE improved Nb resistance to the pathogenic fungus, Alternaria alternata. H<sub>2</sub>O<sub>2</sub> accumulation and callose deposition increased after A. alternata infection in MdCERK1-2 OE plants compared to wild type (WT) and empty vector (EV)-transformed plants. The induced expression of NbPAL4 by A. alternata significantly (p < 0.01, n = 4) increased in MdCERK1-2 OE plants. Other tested genes, including NbNPR1, NbPR1a, NbERF1, and NbLOX1, did not exhibit significant changes after A. alternata infection in OE plants compared to EV or WT plants. OE plants also accumulated more polyphenols after A. alternata infection.</AbstractText><AbstractText Label="CONCLUSIONS" NlmCategory="CONCLUSIONS">Heterologous MdCERK1-2 OE affects multiple defense responses in Nb plants and increased their resistance to fungal pathogens. This result also suggests that MdCERK1-2 is involved in apple defense responses against pathogenic fungi.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Chen</LastName><ForeName>Qiming</ForeName><Initials>Q</Initials><AffiliationInfo><Affiliation>College of Life Sciences, Key Laboratory of Plant Biotechnology of Shandong Province, Qingdao Agricultural University, 700 Changcheng Road, Qingdao, 266109, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Qingdao Key Laboratory of Genetic Improvement and Breeding in Horticultural Plants, Qingdao Agricultural University, Qingdao, 266109, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Shandong Province Key Laboratory of Applied Mycology, Qingdao, 266109, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Dong</LastName><ForeName>Chaohua</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>College of Life Sciences, Key Laboratory of Plant Biotechnology of Shandong Province, Qingdao Agricultural University, 700 Changcheng Road, Qingdao, 266109, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Qingdao Key Laboratory of Genetic Improvement and Breeding in Horticultural Plants, Qingdao Agricultural University, Qingdao, 266109, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Shandong Province Key Laboratory of Applied Mycology, Qingdao, 266109, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Sun</LastName><ForeName>Xiaohong</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>College of Life Sciences, Key Laboratory of Plant Biotechnology of Shandong Province, Qingdao Agricultural University, 700 Changcheng Road, Qingdao, 266109, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Qingdao Key Laboratory of Genetic Improvement and Breeding in Horticultural Plants, Qingdao Agricultural University, Qingdao, 266109, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhang</LastName><ForeName>Yugang</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>Qingdao Key Laboratory of Genetic Improvement and Breeding in Horticultural Plants, Qingdao Agricultural University, Qingdao, 266109, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>College of Horticulture, Qingdao Agricultural University, Qingdao, 266109, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Dai</LastName><ForeName>Hongyi</ForeName><Initials>H</Initials><AffiliationInfo><Affiliation>Qingdao Key Laboratory of Genetic Improvement and Breeding in Horticultural Plants, Qingdao Agricultural University, Qingdao, 266109, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>College of Horticulture, Qingdao Agricultural University, Qingdao, 266109, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Bai</LastName><ForeName>Suhua</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>College of Life Sciences, Key Laboratory of Plant Biotechnology of Shandong Province, Qingdao Agricultural University, 700 Changcheng Road, Qingdao, 266109, China. shbai0402@126.com.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Qingdao Key Laboratory of Genetic Improvement and Breeding in Horticultural Plants, Qingdao Agricultural University, Qingdao, 266109, China. shbai0402@126.com.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Shandong Province Key Laboratory of Applied Mycology, Qingdao, 266109, China. shbai0402@126.com.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>31471853</GrantID><Agency>National Natural Science Foundation of China</Agency><Country></Country></Grant><Grant><GrantID>CARS-27</GrantID><Agency>Agriculture Research System of China</Agency><Country></Country></Grant><Grant><GrantID>631436</GrantID><Agency>Advanced Talents Foundation of Qingdao Agricultural University</Agency><Country></Country></Grant><Grant><GrantID>No. 12-1-4-5-(1)-jch</GrantID><Agency>Qingdao Science and Technology Program</Agency><Country></Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>04</Month><Day>08</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>BMC Plant Biol</MedlineTA><NlmUniqueID>100967807</NlmUniqueID><ISSNLinking>1471-2229</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Fungal pathogen</Keyword><Keyword MajorTopicYN="N">LysM-containing protein</Keyword><Keyword MajorTopicYN="N">Malus × domestica</Keyword><Keyword MajorTopicYN="N">Nicotiana benthamiana</Keyword><Keyword MajorTopicYN="N">Plant immunity</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2019</Year><Month>08</Month><Day>01</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>03</Month><Day>24</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>4</Month><Day>10</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>4</Month><Day>10</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>4</Month><Day>10</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>epublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">32268888</ArticleId><ArticleId IdType="doi">10.1186/s12870-020-02361-z</ArticleId><ArticleId IdType="pii">10.1186/s12870-020-02361-z</ArticleId><ArticleId 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IdType="pubmed">24395781</ArticleId></ArticleIdList></Reference></ReferenceList></PubmedData></pubmed><affiliations><list><country><li>République populaire de Chine</li></country></list><tree><country name="République populaire de Chine"><noRegion><name sortKey="Chen, Qiming" sort="Chen, Qiming" uniqKey="Chen Q" first="Qiming" last="Chen">Qiming Chen</name></noRegion><name sortKey="Bai, Suhua" sort="Bai, Suhua" uniqKey="Bai S" first="Suhua" last="Bai">Suhua Bai</name><name sortKey="Bai, Suhua" sort="Bai, Suhua" uniqKey="Bai S" first="Suhua" last="Bai">Suhua Bai</name><name sortKey="Bai, Suhua" sort="Bai, Suhua" uniqKey="Bai S" first="Suhua" last="Bai">Suhua Bai</name><name sortKey="Chen, Qiming" sort="Chen, Qiming" uniqKey="Chen Q" first="Qiming" last="Chen">Qiming Chen</name><name sortKey="Chen, Qiming" sort="Chen, Qiming" uniqKey="Chen Q" first="Qiming" last="Chen">Qiming Chen</name><name sortKey="Dai, Hongyi" sort="Dai, Hongyi" uniqKey="Dai H" first="Hongyi" last="Dai">Hongyi Dai</name><name sortKey="Dai, Hongyi" sort="Dai, Hongyi" uniqKey="Dai H" first="Hongyi" last="Dai">Hongyi Dai</name><name sortKey="Dong, Chaohua" sort="Dong, Chaohua" uniqKey="Dong C" first="Chaohua" last="Dong">Chaohua Dong</name><name sortKey="Dong, Chaohua" sort="Dong, Chaohua" uniqKey="Dong C" first="Chaohua" last="Dong">Chaohua Dong</name><name sortKey="Dong, Chaohua" sort="Dong, Chaohua" uniqKey="Dong C" first="Chaohua" last="Dong">Chaohua Dong</name><name sortKey="Sun, Xiaohong" sort="Sun, Xiaohong" uniqKey="Sun X" first="Xiaohong" last="Sun">Xiaohong Sun</name><name sortKey="Sun, Xiaohong" sort="Sun, Xiaohong" uniqKey="Sun X" first="Xiaohong" last="Sun">Xiaohong Sun</name><name sortKey="Zhang, Yugang" sort="Zhang, Yugang" uniqKey="Zhang Y" first="Yugang" last="Zhang">Yugang Zhang</name><name sortKey="Zhang, Yugang" sort="Zhang, Yugang" uniqKey="Zhang Y" first="Yugang" last="Zhang">Yugang Zhang</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix 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