Poplar miR472a targeting NBS-LRRs is involved in effective defence against the necrotrophic fungus Cytospora chrysosperma.
Identifieur interne : 000C98 ( Main/Corpus ); précédent : 000C97; suivant : 000C99Poplar miR472a targeting NBS-LRRs is involved in effective defence against the necrotrophic fungus Cytospora chrysosperma.
Auteurs : Yanyan Su ; Hui-Guang Li ; Yonglin Wang ; Shuang Li ; Hou-Ling Wang ; Lu Yu ; Fang He ; Yanli Yang ; Cong-Hua Feng ; Peng Shuai ; Chao Liu ; Weilun Yin ; Xinli XiaSource :
- Journal of experimental botany [ 1460-2431 ] ; 2018.
English descriptors
- KwdEn :
- Colletotrichum (physiology), Disease Resistance (genetics), MicroRNAs (genetics), MicroRNAs (metabolism), Plant Diseases (immunology), Plant Diseases (microbiology), Plant Immunity (genetics), Plant Proteins (genetics), Plant Proteins (metabolism), Populus (genetics), Populus (immunology), Populus (microbiology), Species Specificity (MeSH).
- MESH :
- chemical , genetics : MicroRNAs, Plant Proteins.
- genetics : Disease Resistance, Plant Immunity, Populus.
- immunology : Plant Diseases, Populus.
- chemical , metabolism : MicroRNAs, Plant Proteins.
- microbiology : Plant Diseases, Populus.
- physiology : Colletotrichum.
- Species Specificity.
Abstract
The hemibiotroph Colletotrichum gloeosporioides and the necrotroph Cytospora chrysosperma cause poplar foliage and stem disease, respectively, resulting in substantial economic losses. In this study, Populus trichocarpa ptc-miR472a was down-regulated in leaves treated with salicylic acid, jasmonic acid (JA) or bacterial flagellin (flg22). Here, ptc-miR472a and a short tandem target mimic (STTM) of miR472a were overexpressed in P. alba × P. glandulosa, and overexpression lines of miR472a and silenced lines of STTM472a were generated. Compared with the STTM472a and wild type lines, lower reactive oxygen species accumulation was detected in miR472a overexpressing plants treated with flg22, C. gloeosporioides or C. chrysosperma. In addition, the miR472a overexpressing lines exhibited the highest susceptibility to the hemibiotroph, C. gloeosporioides, but the highest effective defence response to the necrotroph, C. chrysosperma. The JA/ethylene marker gene ERF1 was rapidly up-regulated in miR472a overexpressing plants. Furthermore, five phased, secondary, small interfering RNAs (phasiRNAs) were confirmed in the miR472a overexpressing and STTM472a lines, triggering phasiRNAs predicted to enhance NBS-LRR silencing. Taken together, our results revealed that ptc-miR472a exerts a key role in plant immunity to C. gloeosporioides and C. chrysosperma by targeting NBS-LRR transcripts. This study provides a new strategy and method in plant breeding to improve plant disease resistance.
DOI: 10.1093/jxb/ery304
PubMed: 30124931
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pubmed:30124931Le document en format XML
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China.</nlm:affiliation></affiliation></author><author><name sortKey="Wang, Yonglin" sort="Wang, Yonglin" uniqKey="Wang Y" first="Yonglin" last="Wang">Yonglin Wang</name><affiliation><nlm:affiliation>College of Forestry, Beijing Forestry University, Beijing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Li, Shuang" sort="Li, Shuang" uniqKey="Li S" first="Shuang" last="Li">Shuang Li</name><affiliation><nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, National Engineering Laboratory of Tree Breeding, Beijing Forestry University, Beijing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Wang, Hou Ling" sort="Wang, Hou Ling" uniqKey="Wang H" first="Hou-Ling" last="Wang">Hou-Ling Wang</name><affiliation><nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, National Engineering Laboratory of Tree Breeding, Beijing Forestry University, Beijing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Yu, Lu" sort="Yu, Lu" uniqKey="Yu L" first="Lu" last="Yu">Lu Yu</name><affiliation><nlm:affiliation>College of Forestry, Beijing Forestry University, Beijing, China.</nlm:affiliation></affiliation></author><author><name sortKey="He, Fang" sort="He, Fang" uniqKey="He F" first="Fang" last="He">Fang He</name><affiliation><nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, National Engineering Laboratory of Tree Breeding, Beijing Forestry University, Beijing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Yang, Yanli" sort="Yang, Yanli" uniqKey="Yang Y" first="Yanli" last="Yang">Yanli Yang</name><affiliation><nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, National Engineering Laboratory of Tree Breeding, Beijing Forestry University, Beijing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Feng, Cong Hua" sort="Feng, Cong Hua" uniqKey="Feng C" first="Cong-Hua" last="Feng">Cong-Hua Feng</name><affiliation><nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, National Engineering Laboratory of Tree Breeding, Beijing Forestry University, Beijing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Shuai, Peng" sort="Shuai, Peng" uniqKey="Shuai P" first="Peng" last="Shuai">Peng Shuai</name><affiliation><nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, National Engineering Laboratory of Tree Breeding, Beijing Forestry University, Beijing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Liu, Chao" sort="Liu, Chao" uniqKey="Liu C" first="Chao" last="Liu">Chao Liu</name><affiliation><nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, National Engineering Laboratory of Tree Breeding, Beijing Forestry University, Beijing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Yin, Weilun" sort="Yin, Weilun" uniqKey="Yin W" first="Weilun" last="Yin">Weilun Yin</name><affiliation><nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, National Engineering Laboratory of Tree Breeding, Beijing Forestry University, Beijing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Xia, Xinli" sort="Xia, Xinli" uniqKey="Xia X" first="Xinli" last="Xia">Xinli Xia</name><affiliation><nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, National Engineering Laboratory of Tree Breeding, Beijing Forestry University, Beijing, China.</nlm:affiliation></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2018">2018</date><idno type="RBID">pubmed:30124931</idno><idno type="pmid">30124931</idno><idno type="doi">10.1093/jxb/ery304</idno><idno type="wicri:Area/Main/Corpus">000C98</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Corpus" wicri:corpus="PubMed">000C98</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">Poplar miR472a targeting NBS-LRRs is involved in effective defence against the necrotrophic fungus Cytospora chrysosperma.</title><author><name sortKey="Su, Yanyan" sort="Su, Yanyan" uniqKey="Su Y" first="Yanyan" last="Su">Yanyan Su</name><affiliation><nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, National Engineering Laboratory of Tree Breeding, Beijing Forestry University, Beijing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Li, Hui Guang" sort="Li, Hui Guang" uniqKey="Li H" first="Hui-Guang" last="Li">Hui-Guang Li</name><affiliation><nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, National Engineering Laboratory of Tree Breeding, Beijing Forestry University, Beijing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Wang, Yonglin" sort="Wang, Yonglin" uniqKey="Wang Y" first="Yonglin" last="Wang">Yonglin Wang</name><affiliation><nlm:affiliation>College of Forestry, Beijing Forestry University, Beijing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Li, Shuang" sort="Li, Shuang" uniqKey="Li S" first="Shuang" last="Li">Shuang Li</name><affiliation><nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, National Engineering Laboratory of Tree Breeding, Beijing Forestry University, Beijing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Wang, Hou Ling" sort="Wang, Hou Ling" uniqKey="Wang H" first="Hou-Ling" last="Wang">Hou-Ling Wang</name><affiliation><nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, National Engineering Laboratory of Tree Breeding, Beijing Forestry University, Beijing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Yu, Lu" sort="Yu, Lu" uniqKey="Yu L" first="Lu" last="Yu">Lu Yu</name><affiliation><nlm:affiliation>College of Forestry, Beijing Forestry University, Beijing, China.</nlm:affiliation></affiliation></author><author><name sortKey="He, Fang" sort="He, Fang" uniqKey="He F" first="Fang" last="He">Fang He</name><affiliation><nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, National Engineering Laboratory of Tree Breeding, Beijing Forestry University, Beijing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Yang, Yanli" sort="Yang, Yanli" uniqKey="Yang Y" first="Yanli" last="Yang">Yanli Yang</name><affiliation><nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, National Engineering Laboratory of Tree Breeding, Beijing Forestry University, Beijing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Feng, Cong Hua" sort="Feng, Cong Hua" uniqKey="Feng C" first="Cong-Hua" last="Feng">Cong-Hua Feng</name><affiliation><nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, National Engineering Laboratory of Tree Breeding, Beijing Forestry University, Beijing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Shuai, Peng" sort="Shuai, Peng" uniqKey="Shuai P" first="Peng" last="Shuai">Peng Shuai</name><affiliation><nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, National Engineering Laboratory of Tree Breeding, Beijing Forestry University, Beijing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Liu, Chao" sort="Liu, Chao" uniqKey="Liu C" first="Chao" last="Liu">Chao Liu</name><affiliation><nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, National Engineering Laboratory of Tree Breeding, Beijing Forestry University, Beijing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Yin, Weilun" sort="Yin, Weilun" uniqKey="Yin W" first="Weilun" last="Yin">Weilun Yin</name><affiliation><nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, National Engineering Laboratory of Tree Breeding, Beijing Forestry University, Beijing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Xia, Xinli" sort="Xia, Xinli" uniqKey="Xia X" first="Xinli" last="Xia">Xinli Xia</name><affiliation><nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, National Engineering Laboratory of Tree Breeding, Beijing Forestry University, Beijing, China.</nlm:affiliation></affiliation></author></analytic><series><title level="j">Journal of experimental botany</title><idno type="eISSN">1460-2431</idno><imprint><date when="2018" type="published">2018</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Colletotrichum (physiology)</term><term>Disease Resistance (genetics)</term><term>MicroRNAs (genetics)</term><term>MicroRNAs (metabolism)</term><term>Plant Diseases (immunology)</term><term>Plant Diseases (microbiology)</term><term>Plant Immunity (genetics)</term><term>Plant Proteins (genetics)</term><term>Plant Proteins (metabolism)</term><term>Populus (genetics)</term><term>Populus (immunology)</term><term>Populus (microbiology)</term><term>Species Specificity (MeSH)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>MicroRNAs</term><term>Plant Proteins</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Disease Resistance</term><term>Plant Immunity</term><term>Populus</term></keywords><keywords scheme="MESH" qualifier="immunology" xml:lang="en"><term>Plant Diseases</term><term>Populus</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>MicroRNAs</term><term>Plant Proteins</term></keywords><keywords scheme="MESH" qualifier="microbiology" xml:lang="en"><term>Plant Diseases</term><term>Populus</term></keywords><keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Colletotrichum</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Species Specificity</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">The hemibiotroph Colletotrichum gloeosporioides and the necrotroph Cytospora chrysosperma cause poplar foliage and stem disease, respectively, resulting in substantial economic losses. In this study, Populus trichocarpa ptc-miR472a was down-regulated in leaves treated with salicylic acid, jasmonic acid (JA) or bacterial flagellin (flg22). Here, ptc-miR472a and a short tandem target mimic (STTM) of miR472a were overexpressed in P. alba × P. glandulosa, and overexpression lines of miR472a and silenced lines of STTM472a were generated. Compared with the STTM472a and wild type lines, lower reactive oxygen species accumulation was detected in miR472a overexpressing plants treated with flg22, C. gloeosporioides or C. chrysosperma. In addition, the miR472a overexpressing lines exhibited the highest susceptibility to the hemibiotroph, C. gloeosporioides, but the highest effective defence response to the necrotroph, C. chrysosperma. The JA/ethylene marker gene ERF1 was rapidly up-regulated in miR472a overexpressing plants. Furthermore, five phased, secondary, small interfering RNAs (phasiRNAs) were confirmed in the miR472a overexpressing and STTM472a lines, triggering phasiRNAs predicted to enhance NBS-LRR silencing. Taken together, our results revealed that ptc-miR472a exerts a key role in plant immunity to C. gloeosporioides and C. chrysosperma by targeting NBS-LRR transcripts. This study provides a new strategy and method in plant breeding to improve plant disease resistance.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">30124931</PMID><DateCompleted><Year>2019</Year><Month>10</Month><Day>15</Day></DateCompleted><DateRevised><Year>2019</Year><Month>10</Month><Day>15</Day></DateRevised><Article PubModel="Print"><Journal><ISSN IssnType="Electronic">1460-2431</ISSN><JournalIssue CitedMedium="Internet"><Volume>69</Volume><Issue>22</Issue><PubDate><Year>2018</Year><Month>11</Month><Day>26</Day></PubDate></JournalIssue><Title>Journal of experimental botany</Title><ISOAbbreviation>J Exp Bot</ISOAbbreviation></Journal><ArticleTitle>Poplar miR472a targeting NBS-LRRs is involved in effective defence against the necrotrophic fungus Cytospora chrysosperma.</ArticleTitle><Pagination><MedlinePgn>5519-5530</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1093/jxb/ery304</ELocationID><Abstract><AbstractText>The hemibiotroph Colletotrichum gloeosporioides and the necrotroph Cytospora chrysosperma cause poplar foliage and stem disease, respectively, resulting in substantial economic losses. In this study, Populus trichocarpa ptc-miR472a was down-regulated in leaves treated with salicylic acid, jasmonic acid (JA) or bacterial flagellin (flg22). Here, ptc-miR472a and a short tandem target mimic (STTM) of miR472a were overexpressed in P. alba × P. glandulosa, and overexpression lines of miR472a and silenced lines of STTM472a were generated. Compared with the STTM472a and wild type lines, lower reactive oxygen species accumulation was detected in miR472a overexpressing plants treated with flg22, C. gloeosporioides or C. chrysosperma. In addition, the miR472a overexpressing lines exhibited the highest susceptibility to the hemibiotroph, C. gloeosporioides, but the highest effective defence response to the necrotroph, C. chrysosperma. The JA/ethylene marker gene ERF1 was rapidly up-regulated in miR472a overexpressing plants. Furthermore, five phased, secondary, small interfering RNAs (phasiRNAs) were confirmed in the miR472a overexpressing and STTM472a lines, triggering phasiRNAs predicted to enhance NBS-LRR silencing. Taken together, our results revealed that ptc-miR472a exerts a key role in plant immunity to C. gloeosporioides and C. chrysosperma by targeting NBS-LRR transcripts. This study provides a new strategy and method in plant breeding to improve plant disease resistance.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Su</LastName><ForeName>Yanyan</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, National Engineering Laboratory of Tree Breeding, Beijing Forestry University, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Li</LastName><ForeName>Hui-Guang</ForeName><Initials>HG</Initials><AffiliationInfo><Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, National Engineering Laboratory of Tree Breeding, Beijing Forestry University, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Yonglin</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>College of Forestry, Beijing Forestry University, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Li</LastName><ForeName>Shuang</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, National Engineering Laboratory of Tree Breeding, Beijing Forestry University, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Hou-Ling</ForeName><Initials>HL</Initials><AffiliationInfo><Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, National Engineering Laboratory of Tree Breeding, Beijing Forestry University, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Yu</LastName><ForeName>Lu</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>College of Forestry, Beijing Forestry University, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>He</LastName><ForeName>Fang</ForeName><Initials>F</Initials><AffiliationInfo><Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, National Engineering Laboratory of Tree Breeding, Beijing Forestry University, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Yang</LastName><ForeName>Yanli</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, National Engineering Laboratory of Tree Breeding, Beijing Forestry University, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Feng</LastName><ForeName>Cong-Hua</ForeName><Initials>CH</Initials><AffiliationInfo><Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, National Engineering Laboratory of Tree Breeding, Beijing Forestry University, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Shuai</LastName><ForeName>Peng</ForeName><Initials>P</Initials><AffiliationInfo><Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, National Engineering Laboratory of Tree Breeding, Beijing Forestry University, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Liu</LastName><ForeName>Chao</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, National Engineering Laboratory of Tree Breeding, Beijing Forestry University, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Yin</LastName><ForeName>Weilun</ForeName><Initials>W</Initials><AffiliationInfo><Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, National Engineering Laboratory of Tree Breeding, Beijing Forestry University, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Xia</LastName><ForeName>Xinli</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, National Engineering Laboratory of Tree Breeding, Beijing Forestry University, Beijing, China.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>J Exp Bot</MedlineTA><NlmUniqueID>9882906</NlmUniqueID><ISSNLinking>0022-0957</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D035683">MicroRNAs</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D010940">Plant Proteins</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D020231" MajorTopicYN="N">Colletotrichum</DescriptorName><QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D060467" MajorTopicYN="N">Disease Resistance</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D035683" MajorTopicYN="N">MicroRNAs</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D010935" MajorTopicYN="N">Plant Diseases</DescriptorName><QualifierName UI="Q000276" MajorTopicYN="Y">immunology</QualifierName><QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D057865" MajorTopicYN="N">Plant Immunity</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D010940" MajorTopicYN="N">Plant Proteins</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D032107" MajorTopicYN="N">Populus</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName><QualifierName UI="Q000276" MajorTopicYN="Y">immunology</QualifierName><QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D013045" MajorTopicYN="N">Species Specificity</DescriptorName></MeshHeading></MeshHeadingList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2018</Year><Month>02</Month><Day>07</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2018</Year><Month>08</Month><Day>09</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2018</Year><Month>8</Month><Day>21</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2019</Year><Month>10</Month><Day>16</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate 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