PuHox52-mediated hierarchical multilayered gene regulatory network promotes adventitious root formation in Populus ussuriensis.
Identifieur interne : 000166 ( Main/Exploration ); précédent : 000165; suivant : 000167PuHox52-mediated hierarchical multilayered gene regulatory network promotes adventitious root formation in Populus ussuriensis.
Auteurs : Ming Wei [République populaire de Chine] ; Quangang Liu [République populaire de Chine] ; Zhanchao Wang [République populaire de Chine] ; Jingli Yang [République populaire de Chine] ; Wenlong Li [République populaire de Chine] ; Yingxi Chen [République populaire de Chine] ; Han Lu [République populaire de Chine] ; Jinfu Nie [République populaire de Chine] ; Baoguang Liu [République populaire de Chine] ; Kaiwen Lv [République populaire de Chine] ; Xuliang Mao [République populaire de Chine] ; Su Chen [République populaire de Chine] ; Jennifer Sanders [États-Unis] ; Hairong Wei [États-Unis] ; Chenghao Li [République populaire de Chine]Source :
- The New phytologist [ 1469-8137 ] ; 2020.
Abstract
Adventitious root (AR) formation is critically important in vegetative propagation through cuttings in some plants, especially woody species. However, the underlying molecular mechanisms remain elusive. Here, we report the identification of a poplar homeobox gene, PuHox52, which was induced rapidly (within 15 min) at the basal ends of stems upon cutting and played a key regulatory role in adventitious rooting. We demonstrated that overexpression of PuHox52 significantly increased the number of ARs while suppression of PuHox52 had the opposite effect. A multilayered hierarchical gene regulatory network (ML-hGRN) mediated by PuHox52 was reverse-engineered and demonstrated to govern AR formation. PuHox52 regulated AR formation through upregulation of nine hub regulators, including a jasmonate signaling pathway gene, PuMYC2, and an auxin signaling pathway gene, PuAGL12. We also identified coherent type 4 feed-forward loops within this ML-hGRN; PuHox52 repressed PuHDA9, which encodes a histone deacetylase, and led to an increase in acetylation and presumably expression of three hub regulators, PuWRKY51, PuLBD21 and PuIAA7. Our results indicate that the ML-hGRN mediated by PuHox52 governs AR formation at the basal ends of stem cuttings from poplar trees.
DOI: 10.1111/nph.16778
PubMed: 32589766
Affiliations:
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xml:lang="en">PuHox52-mediated hierarchical multilayered gene regulatory network promotes adventitious root formation in Populus ussuriensis.</title><author><name sortKey="Wei, Ming" sort="Wei, Ming" uniqKey="Wei M" first="Ming" last="Wei">Ming Wei</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040</wicri:regionArea><wicri:noRegion>150040</wicri:noRegion></affiliation></author><author><name sortKey="Liu, Quangang" sort="Liu, Quangang" uniqKey="Liu Q" first="Quangang" last="Liu">Quangang Liu</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040</wicri:regionArea><wicri:noRegion>150040</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>College of Forestry, Shenyang Agricultural University, Shenyang, 110866, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>College of Forestry, Shenyang Agricultural University, Shenyang, 110866</wicri:regionArea><wicri:noRegion>110866</wicri:noRegion></affiliation></author><author><name sortKey="Wang, Zhanchao" sort="Wang, Zhanchao" uniqKey="Wang Z" first="Zhanchao" last="Wang">Zhanchao Wang</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040</wicri:regionArea><wicri:noRegion>150040</wicri:noRegion></affiliation></author><author><name sortKey="Yang, Jingli" sort="Yang, Jingli" uniqKey="Yang J" first="Jingli" last="Yang">Jingli Yang</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040</wicri:regionArea><wicri:noRegion>150040</wicri:noRegion></affiliation></author><author><name sortKey="Li, Wenlong" sort="Li, Wenlong" uniqKey="Li W" first="Wenlong" last="Li">Wenlong Li</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040</wicri:regionArea><wicri:noRegion>150040</wicri:noRegion></affiliation></author><author><name sortKey="Chen, Yingxi" sort="Chen, Yingxi" uniqKey="Chen Y" first="Yingxi" last="Chen">Yingxi Chen</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040</wicri:regionArea><wicri:noRegion>150040</wicri:noRegion></affiliation></author><author><name sortKey="Lu, Han" sort="Lu, Han" uniqKey="Lu H" first="Han" last="Lu">Han Lu</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040</wicri:regionArea><wicri:noRegion>150040</wicri:noRegion></affiliation></author><author><name sortKey="Nie, Jinfu" sort="Nie, Jinfu" uniqKey="Nie J" first="Jinfu" last="Nie">Jinfu Nie</name><affiliation wicri:level="1"><nlm:affiliation>Anhui Province Key Laboratory of Medical Physics and Technology, Center of Medical Physics and Technology, Hefei Institutes of Physical Science, Chinese Academy of Sciences, Hefei, 230000, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Anhui Province Key Laboratory of Medical Physics and Technology, Center of Medical Physics and Technology, Hefei Institutes of Physical Science, Chinese Academy of Sciences, Hefei, 230000</wicri:regionArea><wicri:noRegion>230000</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Guangzhou Institute of Biomedicine and Health, Chinese Academy of Sciences, Guangzhou, 510000, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Guangzhou Institute of Biomedicine and Health, Chinese Academy of Sciences, Guangzhou, 510000</wicri:regionArea><wicri:noRegion>510000</wicri:noRegion></affiliation></author><author><name sortKey="Liu, Baoguang" sort="Liu, Baoguang" uniqKey="Liu B" first="Baoguang" last="Liu">Baoguang Liu</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040</wicri:regionArea><wicri:noRegion>150040</wicri:noRegion></affiliation></author><author><name sortKey="Lv, Kaiwen" sort="Lv, Kaiwen" uniqKey="Lv K" first="Kaiwen" last="Lv">Kaiwen Lv</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040</wicri:regionArea><wicri:noRegion>150040</wicri:noRegion></affiliation></author><author><name sortKey="Mao, Xuliang" sort="Mao, Xuliang" uniqKey="Mao X" first="Xuliang" last="Mao">Xuliang Mao</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040</wicri:regionArea><wicri:noRegion>150040</wicri:noRegion></affiliation></author><author><name sortKey="Chen, Su" sort="Chen, Su" uniqKey="Chen S" first="Su" last="Chen">Su Chen</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040</wicri:regionArea><wicri:noRegion>150040</wicri:noRegion></affiliation></author><author><name sortKey="Sanders, Jennifer" sort="Sanders, Jennifer" uniqKey="Sanders J" first="Jennifer" last="Sanders">Jennifer Sanders</name><affiliation wicri:level="1"><nlm:affiliation>College of Forest Resources and Environmental Science, Michigan Technological University, Houghton, MI, 49931, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>College of Forest Resources and Environmental Science, Michigan Technological University, Houghton, MI, 49931</wicri:regionArea><wicri:noRegion>49931</wicri:noRegion></affiliation></author><author><name sortKey="Wei, Hairong" sort="Wei, Hairong" uniqKey="Wei H" first="Hairong" last="Wei">Hairong Wei</name><affiliation wicri:level="1"><nlm:affiliation>College of Forest Resources and Environmental Science, Michigan Technological University, Houghton, MI, 49931, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>College of Forest Resources and Environmental Science, Michigan Technological University, Houghton, MI, 49931</wicri:regionArea><wicri:noRegion>49931</wicri:noRegion></affiliation></author><author><name sortKey="Li, Chenghao" sort="Li, Chenghao" uniqKey="Li C" first="Chenghao" last="Li">Chenghao Li</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040</wicri:regionArea><wicri:noRegion>150040</wicri:noRegion></affiliation></author></analytic><series><title level="j">The New phytologist</title><idno type="eISSN">1469-8137</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">Adventitious root (AR) formation is critically important in vegetative propagation through cuttings in some plants, especially woody species. However, the underlying molecular mechanisms remain elusive. Here, we report the identification of a poplar homeobox gene, PuHox52, which was induced rapidly (within 15 min) at the basal ends of stems upon cutting and played a key regulatory role in adventitious rooting. We demonstrated that overexpression of PuHox52 significantly increased the number of ARs while suppression of PuHox52 had the opposite effect. A multilayered hierarchical gene regulatory network (ML-hGRN) mediated by PuHox52 was reverse-engineered and demonstrated to govern AR formation. PuHox52 regulated AR formation through upregulation of nine hub regulators, including a jasmonate signaling pathway gene, PuMYC2, and an auxin signaling pathway gene, PuAGL12. We also identified coherent type 4 feed-forward loops within this ML-hGRN; PuHox52 repressed PuHDA9, which encodes a histone deacetylase, and led to an increase in acetylation and presumably expression of three hub regulators, PuWRKY51, PuLBD21 and PuIAA7. Our results indicate that the ML-hGRN mediated by PuHox52 governs AR formation at the basal ends of stem cuttings from poplar trees.</div></front></TEI><pubmed><MedlineCitation Status="Publisher" Owner="NLM"><PMID Version="1">32589766</PMID><DateRevised><Year>2020</Year><Month>09</Month><Day>30</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1469-8137</ISSN><JournalIssue CitedMedium="Internet"><PubDate><Year>2020</Year><Month>Jun</Month><Day>26</Day></PubDate></JournalIssue><Title>The New phytologist</Title><ISOAbbreviation>New Phytol</ISOAbbreviation></Journal><ArticleTitle>PuHox52-mediated hierarchical multilayered gene regulatory network promotes adventitious root formation in Populus ussuriensis.</ArticleTitle><ELocationID EIdType="doi" ValidYN="Y">10.1111/nph.16778</ELocationID><Abstract><AbstractText>Adventitious root (AR) formation is critically important in vegetative propagation through cuttings in some plants, especially woody species. However, the underlying molecular mechanisms remain elusive. Here, we report the identification of a poplar homeobox gene, PuHox52, which was induced rapidly (within 15 min) at the basal ends of stems upon cutting and played a key regulatory role in adventitious rooting. We demonstrated that overexpression of PuHox52 significantly increased the number of ARs while suppression of PuHox52 had the opposite effect. A multilayered hierarchical gene regulatory network (ML-hGRN) mediated by PuHox52 was reverse-engineered and demonstrated to govern AR formation. PuHox52 regulated AR formation through upregulation of nine hub regulators, including a jasmonate signaling pathway gene, PuMYC2, and an auxin signaling pathway gene, PuAGL12. We also identified coherent type 4 feed-forward loops within this ML-hGRN; PuHox52 repressed PuHDA9, which encodes a histone deacetylase, and led to an increase in acetylation and presumably expression of three hub regulators, PuWRKY51, PuLBD21 and PuIAA7. Our results indicate that the ML-hGRN mediated by PuHox52 governs AR formation at the basal ends of stem cuttings from poplar trees.</AbstractText><CopyrightInformation>© 2020 The Authors. New Phytologist © 2020 New Phytologist Trust.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Wei</LastName><ForeName>Ming</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Liu</LastName><ForeName>Quangang</ForeName><Initials>Q</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>College of Forestry, Shenyang Agricultural University, Shenyang, 110866, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Zhanchao</ForeName><Initials>Z</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Yang</LastName><ForeName>Jingli</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Li</LastName><ForeName>Wenlong</ForeName><Initials>W</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Chen</LastName><ForeName>Yingxi</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lu</LastName><ForeName>Han</ForeName><Initials>H</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Nie</LastName><ForeName>Jinfu</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Anhui Province Key Laboratory of Medical Physics and Technology, Center of Medical Physics and Technology, Hefei Institutes of Physical Science, Chinese Academy of Sciences, Hefei, 230000, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Guangzhou Institute of Biomedicine and Health, Chinese Academy of Sciences, Guangzhou, 510000, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Liu</LastName><ForeName>Baoguang</ForeName><Initials>B</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lv</LastName><ForeName>Kaiwen</ForeName><Initials>K</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Mao</LastName><ForeName>Xuliang</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Chen</LastName><ForeName>Su</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Sanders</LastName><ForeName>Jennifer</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>College of Forest Resources and Environmental Science, Michigan Technological University, Houghton, MI, 49931, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wei</LastName><ForeName>Hairong</ForeName><Initials>H</Initials><Identifier Source="ORCID">https://orcid.org/0000-0002-3551-4998</Identifier><AffiliationInfo><Affiliation>College of Forest Resources and Environmental Science, Michigan Technological University, Houghton, MI, 49931, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Li</LastName><ForeName>Chenghao</ForeName><Initials>C</Initials><Identifier Source="ORCID">https://orcid.org/0000-0003-0916-0409</Identifier><AffiliationInfo><Affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040, China.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>31670668</GrantID><Agency>National Natural Science Foundation of China</Agency><Country></Country></Grant><Grant><Agency>Heilongjiang Touyan Innovation Team Program (Tree Genetics and Breeding Innovation Team)</Agency><Country></Country></Grant><Grant><GrantID>2572018AA14</GrantID><Agency>The Fundamental Research Funds for the Central Universities of China</Agency><Country></Country></Grant><Grant><GrantID>2572018CL04</GrantID><Agency>The Fundamental Research Funds for the Central Universities of China</Agency><Country></Country></Grant><Grant><GrantID>2020A02</GrantID><Agency>The Innovation Project of State Key Laboratory of Tree Genetics and Breeding</Agency><Country></Country></Grant><Grant><GrantID>B16010</GrantID><Agency>111 Project</Agency><Country></Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>06</Month><Day>26</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>New Phytol</MedlineTA><NlmUniqueID>9882884</NlmUniqueID><ISSNLinking>0028-646X</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Populus ussuriensis
</Keyword><Keyword MajorTopicYN="N">PuHox52</Keyword><Keyword MajorTopicYN="N">adventitious root</Keyword><Keyword MajorTopicYN="N">cutting</Keyword><Keyword MajorTopicYN="N">histone acetylation</Keyword><Keyword MajorTopicYN="N">multilayered hierarchical gene regulatory network</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2020</Year><Month>04</Month><Day>21</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>06</Month><Day>15</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>6</Month><Day>27</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>6</Month><Day>27</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>6</Month><Day>27</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>aheadofprint</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">32589766</ArticleId><ArticleId IdType="doi">10.1111/nph.16778</ArticleId></ArticleIdList><ReferenceList><Title>References</Title><Reference><Citation>Ades SE, Sauer RT. 1994. 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