High-Temperature-Responsive Poplar lncRNAs Modulate Target Gene Expression via RNA Interference and Act as RNA Scaffolds to Enhance Heat Tolerance.
Identifieur interne : 000353 ( Main/Exploration ); précédent : 000352; suivant : 000354High-Temperature-Responsive Poplar lncRNAs Modulate Target Gene Expression via RNA Interference and Act as RNA Scaffolds to Enhance Heat Tolerance.
Auteurs : Yuepeng Song [République populaire de Chine] ; Panfei Chen [République populaire de Chine] ; Peng Liu [République populaire de Chine] ; Chenhao Bu [République populaire de Chine] ; Deqiang Zhang [République populaire de Chine]Source :
- International journal of molecular sciences [ 1422-0067 ] ; 2020.
Abstract
High-temperature stress is a threat to plant development and survival. Long noncoding RNAs (lncRNAs) participate in plant stress responses, but their functions in the complex stress response network remain unknown. Poplar contributes to terrestrial ecological stability. In this study, we identified 204 high-temperature-responsive lncRNAs in an abiotic stress-tolerant poplar (Populus simonii) species using strand-specific RNA sequencing (ssRNA-seq). Mimicking overexpressed and repressed candidate lncRNAs in poplar was used to illuminate their regulation pattern on targets using nano sheet mediation. These lncRNAs were predicted to target 185 genes, of which 100 were cis genes and 119 were trans genes. Gene Ontology enrichment analysis showed that anatomical structure morphogenesis and response to stress and signaling were significantly enriched. Among heat-responsive LncRNAs, TCONS_00202587 binds to upstream sequences via its secondary structure and interferes with target gene transcription. TCONS_00260893 enhances calcium influx in response to high-temperature treatment by interfering with a specific variant/isoform of the target gene. Heterogeneous expression of these two lncRNA targets promoted photosynthetic protection and recovery, inhibited membrane peroxidation, and suppressed DNA damage in Arabidopsis under heat stress. These results showed that lncRNAs can regulate their target genes by acting as potential RNA scaffolds or through the RNA interference pathway.
DOI: 10.3390/ijms21186808
PubMed: 32948072
PubMed Central: PMC7555564
Affiliations:
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Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing Forestry University, 35 Qinghua East Road, Beijing 100083, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing Forestry University, 35 Qinghua East Road, Beijing 100083</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 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Breeding by Molecular Design, Beijing Forestry University, 35 Qinghua East Road, Beijing 100083, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing Forestry University, 35 Qinghua East Road, Beijing 100083</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, 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, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Bu, Chenhao" sort="Bu, Chenhao" uniqKey="Bu C" first="Chenhao" last="Bu">Chenhao Bu</name><affiliation wicri:level="1"><nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing Forestry University, 35 Qinghua East Road, Beijing 100083, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing Forestry University, 35 Qinghua East Road, Beijing 100083</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, 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, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Zhang, Deqiang" sort="Zhang, Deqiang" uniqKey="Zhang D" first="Deqiang" last="Zhang">Deqiang Zhang</name><affiliation wicri:level="1"><nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing Forestry University, 35 Qinghua East Road, Beijing 100083, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing Forestry University, 35 Qinghua East Road, Beijing 100083</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, 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, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author></analytic><series><title level="j">International journal of molecular sciences</title><idno type="eISSN">1422-0067</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">High-temperature stress is a threat to plant development and survival. Long noncoding RNAs (lncRNAs) participate in plant stress responses, but their functions in the complex stress response network remain unknown. Poplar contributes to terrestrial ecological stability. In this study, we identified 204 high-temperature-responsive lncRNAs in an abiotic stress-tolerant poplar (<i>Populus simonii</i>) species using strand-specific RNA sequencing (ssRNA-seq). Mimicking overexpressed and repressed candidate lncRNAs in poplar was used to illuminate their regulation pattern on targets using nano sheet mediation. These lncRNAs were predicted to target 185 genes, of which 100 were <i>cis</i> genes and 119 were <i>trans</i> genes. Gene Ontology enrichment analysis showed that anatomical structure morphogenesis and response to stress and signaling were significantly enriched. Among heat-responsive LncRNAs, TCONS_00202587 binds to upstream sequences via its secondary structure and interferes with target gene transcription. TCONS_00260893 enhances calcium influx in response to high-temperature treatment by interfering with a specific variant/isoform of the target gene. Heterogeneous expression of these two lncRNA targets promoted photosynthetic protection and recovery, inhibited membrane peroxidation, and suppressed DNA damage in <i>Arabidopsis</i> under heat stress. These results showed that lncRNAs can regulate their target genes by acting as potential RNA scaffolds or through the RNA interference pathway.</div></front></TEI><pubmed><MedlineCitation Status="In-Process" Owner="NLM"><PMID Version="1">32948072</PMID><DateRevised><Year>2020</Year><Month>10</Month><Day>20</Day></DateRevised><Article PubModel="Electronic"><Journal><ISSN IssnType="Electronic">1422-0067</ISSN><JournalIssue CitedMedium="Internet"><Volume>21</Volume><Issue>18</Issue><PubDate><Year>2020</Year><Month>Sep</Month><Day>16</Day></PubDate></JournalIssue><Title>International journal of molecular sciences</Title><ISOAbbreviation>Int J Mol Sci</ISOAbbreviation></Journal><ArticleTitle>High-Temperature-Responsive Poplar lncRNAs Modulate Target Gene Expression via RNA Interference and Act as RNA Scaffolds to Enhance Heat Tolerance.</ArticleTitle><ELocationID EIdType="pii" ValidYN="Y">E6808</ELocationID><ELocationID EIdType="doi" ValidYN="Y">10.3390/ijms21186808</ELocationID><Abstract><AbstractText>High-temperature stress is a threat to plant development and survival. Long noncoding RNAs (lncRNAs) participate in plant stress responses, but their functions in the complex stress response network remain unknown. Poplar contributes to terrestrial ecological stability. In this study, we identified 204 high-temperature-responsive lncRNAs in an abiotic stress-tolerant poplar (<i>Populus simonii</i>) species using strand-specific RNA sequencing (ssRNA-seq). Mimicking overexpressed and repressed candidate lncRNAs in poplar was used to illuminate their regulation pattern on targets using nano sheet mediation. These lncRNAs were predicted to target 185 genes, of which 100 were <i>cis</i> genes and 119 were <i>trans</i> genes. Gene Ontology enrichment analysis showed that anatomical structure morphogenesis and response to stress and signaling were significantly enriched. Among heat-responsive LncRNAs, TCONS_00202587 binds to upstream sequences via its secondary structure and interferes with target gene transcription. TCONS_00260893 enhances calcium influx in response to high-temperature treatment by interfering with a specific variant/isoform of the target gene. Heterogeneous expression of these two lncRNA targets promoted photosynthetic protection and recovery, inhibited membrane peroxidation, and suppressed DNA damage in <i>Arabidopsis</i> under heat stress. These results showed that lncRNAs can regulate their target genes by acting as potential RNA scaffolds or through the RNA interference pathway.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Song</LastName><ForeName>Yuepeng</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing Forestry University, 35 Qinghua East Road, Beijing 100083, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Chen</LastName><ForeName>Panfei</ForeName><Initials>P</Initials><AffiliationInfo><Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing Forestry University, 35 Qinghua East Road, Beijing 100083, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Liu</LastName><ForeName>Peng</ForeName><Initials>P</Initials><AffiliationInfo><Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing Forestry University, 35 Qinghua East Road, Beijing 100083, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Bu</LastName><ForeName>Chenhao</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing Forestry University, 35 Qinghua East Road, Beijing 100083, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhang</LastName><ForeName>Deqiang</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing Forestry University, 35 Qinghua East Road, Beijing 100083, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, China.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>2017ZY04</GrantID><Agency>the Fundamental Research Funds for the Central Universities</Agency><Country></Country></Grant><Grant><GrantID>31400553, 31670333 and 31770707</GrantID><Agency>the Project of the National Natural Science Foundation of China</Agency><Country></Country></Grant><Grant><GrantID>B20050</GrantID><Agency>the 111 Project</Agency><Country></Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>09</Month><Day>16</Day></ArticleDate></Article><MedlineJournalInfo><Country>Switzerland</Country><MedlineTA>Int J Mol Sci</MedlineTA><NlmUniqueID>101092791</NlmUniqueID><ISSNLinking>1422-0067</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Populus simonii</Keyword><Keyword MajorTopicYN="N">RNA structure</Keyword><Keyword MajorTopicYN="N">high temperature</Keyword><Keyword MajorTopicYN="N">layered double hydroxide nanosheets</Keyword><Keyword MajorTopicYN="N">long noncoding RNAs</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2020</Year><Month>07</Month><Day>29</Day></PubMedPubDate><PubMedPubDate 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uniqKey="Chen P" first="Panfei" last="Chen">Panfei Chen</name><name sortKey="Liu, Peng" sort="Liu, Peng" uniqKey="Liu P" first="Peng" last="Liu">Peng Liu</name><name sortKey="Liu, Peng" sort="Liu, Peng" uniqKey="Liu P" first="Peng" last="Liu">Peng Liu</name><name sortKey="Liu, Peng" sort="Liu, Peng" uniqKey="Liu P" first="Peng" last="Liu">Peng Liu</name><name sortKey="Song, Yuepeng" sort="Song, Yuepeng" uniqKey="Song Y" first="Yuepeng" last="Song">Yuepeng Song</name><name sortKey="Song, Yuepeng" sort="Song, Yuepeng" uniqKey="Song Y" first="Yuepeng" last="Song">Yuepeng Song</name><name sortKey="Zhang, Deqiang" sort="Zhang, Deqiang" uniqKey="Zhang D" first="Deqiang" last="Zhang">Deqiang Zhang</name><name sortKey="Zhang, Deqiang" sort="Zhang, Deqiang" uniqKey="Zhang D" first="Deqiang" last="Zhang">Deqiang Zhang</name><name sortKey="Zhang, Deqiang" sort="Zhang, Deqiang" uniqKey="Zhang D" first="Deqiang" last="Zhang">Deqiang Zhang</name></country></tree></affiliations></record>Pour 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