Transcriptome-wide identification of miRNA targets and a TAS3-homologous gene in Populus by degradome sequencing.
Identifieur interne : 000653 ( Main/Exploration ); précédent : 000652; suivant : 000654Transcriptome-wide identification of miRNA targets and a TAS3-homologous gene in Populus by degradome sequencing.
Auteurs : Hai Bao [République populaire de Chine] ; Min Chen [République populaire de Chine] ; Hui Chen [République populaire de Chine] ; Liang Du [République populaire de Chine] ; Yanwei Wang [République populaire de Chine]Source :
- Genes & genomics [ 2092-9293 ] ; 2019.
Descripteurs français
- KwdFr :
- MESH :
- génétique : ARN messager, Populus, Protéines végétales, microARN.
- métabolisme : ARN messager, Protéines végétales, microARN.
- Régulation de l'expression des gènes végétaux, Transcriptome.
English descriptors
- KwdEn :
- MESH :
- chemical , genetics : MicroRNAs, Plant Proteins, RNA, Messenger.
- chemical , metabolism : MicroRNAs, Plant Proteins, RNA, Messenger.
- genetics : Populus.
- Gene Expression Regulation, Plant, Transcriptome.
Abstract
BACKGROUND
Degradome sequencing has been applied to identify miRNA-directed mRNA cleavage and understand the biological function of miRNAs and their target genes in plants defense to stress. miRNAs involved in the response to cold stress have been identified in Populus, however, there are few reports about the validated targets of miRNAs in Populus under cold stress.
OBJECTIVES
The primary objective of this investigation was to globally identify and validate the targets of the miRNAs and regulatory components in Populus under cold stress.
METHODS
Populus plantlets grown in vitro were treated with cold (4 °C for 8 h) and total RNA was extracted using Trizol reagent. Approximately 200 µg total RNA was used for the construction of the degradome library, and degradome sequencing was conducted on an Illumina HiSeq 2000. The sequences were mapped to Populus genome using SOAP 2.0 and then were collected for degradome analysis. Additionally, trans-acting siRNA sequences from transacting siRNA gene 3 sequences and mature miRNAs cleaved from precursor miRNAs of Populus were analyzed. 5' RNA ligase-mediated-RACE (5'-RACE) were further conducted.
RESULTS
80 genes were experimentally determined to be the target of 51 unique miRNAs, including three down-regulated miRNAs (pto-miR156k, pto-miR169i-m, and pto-miR394a-5p/b-5p) and two up-regulated miRNAs (pto-miR167a-d and pto-miR167f/g). The specificity and diversity of cleavage sites of miRNA targets were validated through 5'-RACE experiment and the results were similar with that of degradome sequencing, further supporting the empirical cleavage of miRNAs on targets in vivo in Populus. Interestingly, the TAS-homologous gene pto-TAS3 (EF146176.1) was identified and 11 potential ta-siRNAs [D1(+)-D11(+)] and their possible biogenesis sites within the pto-TAS3 transcript sequence were predicted in Populus. In addition, the biosynthesis of miRNA from precursor miRNA (pre-miRNA) was also validated through the detection of a total of 17 pre-miRNAs.
CONCLUSION
Our investigation expands the application of degradome sequencing for evaluating miRNA regulatory elements and evidence of the miRNA synthesis process, and provides empirical evidence of bona fide cleavage of target genes by miRNAs in Populus, which might be used for the research of miRNA-mediated regulation mechanism and molecular improvement of resistance to cold stress.
DOI: 10.1007/s13258-019-00797-8
PubMed: 30912003
Affiliations:
Links toward previous steps (curation, corpus...)
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xml:lang="fr">République populaire de Chine</country><wicri:regionArea>National Engineering Laboratory for Tree Breeding, Beijing Forestry University, Beijing, 100083</wicri:regionArea><wicri:noRegion>100083</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, Beijing Forestry University, Beijing, 100083, People's Republic of China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, Beijing Forestry University, Beijing, 100083</wicri:regionArea><wicri:noRegion>100083</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>College of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing, 100083, People's Republic of China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>College of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing, 100083</wicri:regionArea><wicri:noRegion>100083</wicri:noRegion></affiliation></author><author><name sortKey="Chen, Min" sort="Chen, Min" uniqKey="Chen M" first="Min" last="Chen">Min Chen</name><affiliation wicri:level="1"><nlm:affiliation>National Engineering Laboratory for Tree Breeding, Beijing Forestry University, Beijing, 100083, People's Republic of China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>National Engineering Laboratory for Tree Breeding, Beijing Forestry University, Beijing, 100083</wicri:regionArea><wicri:noRegion>100083</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, Beijing Forestry University, Beijing, 100083, People's Republic of China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, Beijing Forestry University, Beijing, 100083</wicri:regionArea><wicri:noRegion>100083</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>College of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing, 100083, People's Republic of China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>College of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing, 100083</wicri:regionArea><wicri:noRegion>100083</wicri:noRegion></affiliation></author><author><name sortKey="Chen, Hui" sort="Chen, Hui" uniqKey="Chen H" first="Hui" last="Chen">Hui Chen</name><affiliation wicri:level="1"><nlm:affiliation>National Engineering Laboratory for Tree Breeding, Beijing Forestry University, Beijing, 100083, People's Republic of China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>National Engineering Laboratory for Tree Breeding, Beijing Forestry University, Beijing, 100083</wicri:regionArea><wicri:noRegion>100083</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, Beijing Forestry University, Beijing, 100083, People's Republic of China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, Beijing Forestry University, Beijing, 100083</wicri:regionArea><wicri:noRegion>100083</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>College of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing, 100083, People's Republic of China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>College of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing, 100083</wicri:regionArea><wicri:noRegion>100083</wicri:noRegion></affiliation></author><author><name sortKey="Du, Liang" sort="Du, Liang" uniqKey="Du L" first="Liang" last="Du">Liang Du</name><affiliation wicri:level="1"><nlm:affiliation>National Engineering Laboratory for Tree Breeding, Beijing Forestry University, Beijing, 100083, People's Republic of China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>National Engineering Laboratory for Tree Breeding, Beijing Forestry University, Beijing, 100083</wicri:regionArea><wicri:noRegion>100083</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, Beijing Forestry University, Beijing, 100083, People's Republic of China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, Beijing Forestry University, Beijing, 100083</wicri:regionArea><wicri:noRegion>100083</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>College of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing, 100083, People's Republic of China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>College of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing, 100083</wicri:regionArea><wicri:noRegion>100083</wicri:noRegion></affiliation></author><author><name sortKey="Wang, Yanwei" sort="Wang, Yanwei" uniqKey="Wang Y" first="Yanwei" last="Wang">Yanwei Wang</name><affiliation wicri:level="1"><nlm:affiliation>National Engineering Laboratory for Tree Breeding, Beijing Forestry University, Beijing, 100083, People's Republic of China. ywwang@bjfu.edu.cn.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>National Engineering Laboratory for Tree Breeding, Beijing Forestry University, Beijing, 100083</wicri:regionArea><wicri:noRegion>100083</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, Beijing Forestry University, Beijing, 100083, People's Republic of China. ywwang@bjfu.edu.cn.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, Beijing Forestry University, Beijing, 100083</wicri:regionArea><wicri:noRegion>100083</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>College of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing, 100083, People's Republic of China. ywwang@bjfu.edu.cn.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>College of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing, 100083</wicri:regionArea><wicri:noRegion>100083</wicri:noRegion></affiliation></author></analytic><series><title level="j">Genes & genomics</title><idno type="eISSN">2092-9293</idno><imprint><date when="2019" type="published">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Gene Expression Regulation, Plant (MeSH)</term><term>MicroRNAs (genetics)</term><term>MicroRNAs (metabolism)</term><term>Plant Proteins (genetics)</term><term>Plant Proteins (metabolism)</term><term>Populus (genetics)</term><term>RNA, Messenger (genetics)</term><term>RNA, Messenger (metabolism)</term><term>Transcriptome (MeSH)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>ARN messager (génétique)</term><term>ARN messager (métabolisme)</term><term>Populus (génétique)</term><term>Protéines végétales (génétique)</term><term>Protéines végétales (métabolisme)</term><term>Régulation de l'expression des gènes végétaux (MeSH)</term><term>Transcriptome (MeSH)</term><term>microARN (génétique)</term><term>microARN (métabolisme)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>MicroRNAs</term><term>Plant Proteins</term><term>RNA, Messenger</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>MicroRNAs</term><term>Plant Proteins</term><term>RNA, Messenger</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Populus</term></keywords><keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>ARN messager</term><term>Populus</term><term>Protéines végétales</term><term>microARN</term></keywords><keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>ARN messager</term><term>Protéines végétales</term><term>microARN</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Gene Expression Regulation, Plant</term><term>Transcriptome</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Régulation de l'expression des gènes végétaux</term><term>Transcriptome</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p><b>BACKGROUND</b></p><p>Degradome sequencing has been applied to identify miRNA-directed mRNA cleavage and understand the biological function of miRNAs and their target genes in plants defense to stress. miRNAs involved in the response to cold stress have been identified in Populus, however, there are few reports about the validated targets of miRNAs in Populus under cold stress.</p></div><div type="abstract" xml:lang="en"><p><b>OBJECTIVES</b></p><p>The primary objective of this investigation was to globally identify and validate the targets of the miRNAs and regulatory components in Populus under cold stress.</p></div><div type="abstract" xml:lang="en"><p><b>METHODS</b></p><p>Populus plantlets grown in vitro were treated with cold (4 °C for 8 h) and total RNA was extracted using Trizol reagent. Approximately 200 µg total RNA was used for the construction of the degradome library, and degradome sequencing was conducted on an Illumina HiSeq 2000. The sequences were mapped to Populus genome using SOAP 2.0 and then were collected for degradome analysis. Additionally, trans-acting siRNA sequences from transacting siRNA gene 3 sequences and mature miRNAs cleaved from precursor miRNAs of Populus were analyzed. 5' RNA ligase-mediated-RACE (5'-RACE) were further conducted.</p></div><div type="abstract" xml:lang="en"><p><b>RESULTS</b></p><p>80 genes were experimentally determined to be the target of 51 unique miRNAs, including three down-regulated miRNAs (pto-miR156k, pto-miR169i-m, and pto-miR394a-5p/b-5p) and two up-regulated miRNAs (pto-miR167a-d and pto-miR167f/g). The specificity and diversity of cleavage sites of miRNA targets were validated through 5'-RACE experiment and the results were similar with that of degradome sequencing, further supporting the empirical cleavage of miRNAs on targets in vivo in Populus. Interestingly, the TAS-homologous gene pto-TAS3 (EF146176.1) was identified and 11 potential ta-siRNAs [D1(+)-D11(+)] and their possible biogenesis sites within the pto-TAS3 transcript sequence were predicted in Populus. In addition, the biosynthesis of miRNA from precursor miRNA (pre-miRNA) was also validated through the detection of a total of 17 pre-miRNAs.</p></div><div type="abstract" xml:lang="en"><p><b>CONCLUSION</b></p><p>Our investigation expands the application of degradome sequencing for evaluating miRNA regulatory elements and evidence of the miRNA synthesis process, and provides empirical evidence of bona fide cleavage of target genes by miRNAs in Populus, which might be used for the research of miRNA-mediated regulation mechanism and molecular improvement of resistance to cold stress.</p></div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">30912003</PMID><DateCompleted><Year>2019</Year><Month>12</Month><Day>31</Day></DateCompleted><DateRevised><Year>2020</Year><Month>03</Month><Day>09</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">2092-9293</ISSN><JournalIssue CitedMedium="Internet"><Volume>41</Volume><Issue>7</Issue><PubDate><Year>2019</Year><Month>07</Month></PubDate></JournalIssue><Title>Genes & genomics</Title><ISOAbbreviation>Genes Genomics</ISOAbbreviation></Journal><ArticleTitle>Transcriptome-wide identification of miRNA targets and a TAS3-homologous gene in Populus by degradome sequencing.</ArticleTitle><Pagination><MedlinePgn>849-861</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1007/s13258-019-00797-8</ELocationID><Abstract><AbstractText Label="BACKGROUND">Degradome sequencing has been applied to identify miRNA-directed mRNA cleavage and understand the biological function of miRNAs and their target genes in plants defense to stress. miRNAs involved in the response to cold stress have been identified in Populus, however, there are few reports about the validated targets of miRNAs in Populus under cold stress.</AbstractText><AbstractText Label="OBJECTIVES">The primary objective of this investigation was to globally identify and validate the targets of the miRNAs and regulatory components in Populus under cold stress.</AbstractText><AbstractText Label="METHODS">Populus plantlets grown in vitro were treated with cold (4 °C for 8 h) and total RNA was extracted using Trizol reagent. Approximately 200 µg total RNA was used for the construction of the degradome library, and degradome sequencing was conducted on an Illumina HiSeq 2000. The sequences were mapped to Populus genome using SOAP 2.0 and then were collected for degradome analysis. Additionally, trans-acting siRNA sequences from transacting siRNA gene 3 sequences and mature miRNAs cleaved from precursor miRNAs of Populus were analyzed. 5' RNA ligase-mediated-RACE (5'-RACE) were further conducted.</AbstractText><AbstractText Label="RESULTS">80 genes were experimentally determined to be the target of 51 unique miRNAs, including three down-regulated miRNAs (pto-miR156k, pto-miR169i-m, and pto-miR394a-5p/b-5p) and two up-regulated miRNAs (pto-miR167a-d and pto-miR167f/g). The specificity and diversity of cleavage sites of miRNA targets were validated through 5'-RACE experiment and the results were similar with that of degradome sequencing, further supporting the empirical cleavage of miRNAs on targets in vivo in Populus. Interestingly, the TAS-homologous gene pto-TAS3 (EF146176.1) was identified and 11 potential ta-siRNAs [D1(+)-D11(+)] and their possible biogenesis sites within the pto-TAS3 transcript sequence were predicted in Populus. In addition, the biosynthesis of miRNA from precursor miRNA (pre-miRNA) was also validated through the detection of a total of 17 pre-miRNAs.</AbstractText><AbstractText Label="CONCLUSION">Our investigation expands the application of degradome sequencing for evaluating miRNA regulatory elements and evidence of the miRNA synthesis process, and provides empirical evidence of bona fide cleavage of target genes by miRNAs in Populus, which might be used for the research of miRNA-mediated regulation mechanism and molecular improvement of resistance to cold stress.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Bao</LastName><ForeName>Hai</ForeName><Initials>H</Initials><AffiliationInfo><Affiliation>National Engineering Laboratory for Tree Breeding, Beijing Forestry University, Beijing, 100083, People's Republic of China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, Beijing Forestry University, Beijing, 100083, People's Republic of China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>College of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing, 100083, People's Republic of China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Chen</LastName><ForeName>Min</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>National Engineering Laboratory for Tree Breeding, Beijing Forestry University, Beijing, 100083, People's Republic of China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, Beijing Forestry University, Beijing, 100083, People's Republic of China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>College of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing, 100083, People's Republic of China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Chen</LastName><ForeName>Hui</ForeName><Initials>H</Initials><AffiliationInfo><Affiliation>National Engineering Laboratory for Tree Breeding, Beijing Forestry University, Beijing, 100083, People's Republic of China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, Beijing Forestry University, Beijing, 100083, People's Republic of China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>College of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing, 100083, People's Republic of China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Du</LastName><ForeName>Liang</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>National Engineering Laboratory for Tree Breeding, Beijing Forestry University, Beijing, 100083, People's Republic of China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, Beijing Forestry University, Beijing, 100083, People's Republic of China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>College of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing, 100083, People's Republic of China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Yanwei</ForeName><Initials>Y</Initials><Identifier Source="ORCID">0000-0002-4111-4843</Identifier><AffiliationInfo><Affiliation>National Engineering Laboratory for Tree Breeding, Beijing Forestry University, Beijing, 100083, People's Republic of China. ywwang@bjfu.edu.cn.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, Beijing Forestry University, Beijing, 100083, People's Republic of China. ywwang@bjfu.edu.cn.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>College of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing, 100083, People's Republic of China. ywwang@bjfu.edu.cn.</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><ArticleDate DateType="Electronic"><Year>2019</Year><Month>03</Month><Day>25</Day></ArticleDate></Article><MedlineJournalInfo><Country>Korea (South)</Country><MedlineTA>Genes Genomics</MedlineTA><NlmUniqueID>101481027</NlmUniqueID><ISSNLinking>1976-9571</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D035683">MicroRNAs</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D010940">Plant Proteins</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D012333">RNA, Messenger</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D018506" MajorTopicYN="Y">Gene Expression Regulation, Plant</DescriptorName></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="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></MeshHeading><MeshHeading><DescriptorName UI="D012333" MajorTopicYN="N">RNA, Messenger</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D059467" MajorTopicYN="Y">Transcriptome</DescriptorName></MeshHeading></MeshHeadingList><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="Y">Cold stress</Keyword><Keyword MajorTopicYN="Y">Degradome sequencing</Keyword><Keyword MajorTopicYN="Y">Populus</Keyword><Keyword MajorTopicYN="Y">Targets</Keyword><Keyword MajorTopicYN="Y">miRNA</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2017</Year><Month>10</Month><Day>10</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2019</Year><Month>02</Month><Day>19</Day></PubMedPubDate><PubMedPubDate 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last="Chen">Hui Chen</name><name sortKey="Chen, Min" sort="Chen, Min" uniqKey="Chen M" first="Min" last="Chen">Min Chen</name><name sortKey="Chen, Min" sort="Chen, Min" uniqKey="Chen M" first="Min" last="Chen">Min Chen</name><name sortKey="Chen, Min" sort="Chen, Min" uniqKey="Chen M" first="Min" last="Chen">Min Chen</name><name sortKey="Du, Liang" sort="Du, Liang" uniqKey="Du L" first="Liang" last="Du">Liang Du</name><name sortKey="Du, Liang" sort="Du, Liang" uniqKey="Du L" first="Liang" last="Du">Liang Du</name><name sortKey="Du, Liang" sort="Du, Liang" uniqKey="Du L" first="Liang" last="Du">Liang Du</name><name sortKey="Wang, Yanwei" sort="Wang, Yanwei" uniqKey="Wang Y" first="Yanwei" last="Wang">Yanwei Wang</name><name sortKey="Wang, Yanwei" sort="Wang, Yanwei" uniqKey="Wang Y" first="Yanwei" last="Wang">Yanwei Wang</name><name sortKey="Wang, Yanwei" sort="Wang, Yanwei" uniqKey="Wang Y" first="Yanwei" last="Wang">Yanwei Wang</name></country></tree></affiliations></record>Pour 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