RNA-seq of eight different poplar clones reveals conserved up-regulation of gene expression in response to insect herbivory.
Identifieur interne : 000743 ( Main/Exploration ); précédent : 000742; suivant : 000744RNA-seq of eight different poplar clones reveals conserved up-regulation of gene expression in response to insect herbivory.
Auteurs : Niels A. Müller [Allemagne] ; Birgit Kersten [Allemagne] ; Matthias Fladung [Allemagne] ; Hilke Schroeder [Allemagne]Source :
- BMC genomics [ 1471-2164 ] ; 2019.
Descripteurs français
- KwdFr :
- Animaux (MeSH), Chitinase (métabolisme), Cyclopentanes (métabolisme), Cytochrome P-450 enzyme system (métabolisme), Facteurs de transcription à motifs basiques hélice-boucle-hélice et à glissière à leucines (métabolisme), Herbivorie (MeSH), Inhibiteurs de protéases (métabolisme), Insectes (physiologie), Oxylipines (métabolisme), Populus (génétique), Populus (métabolisme), Régulation de l'expression des gènes végétaux (MeSH), Régulation positive (MeSH), Séquences d'acides nucléiques régulatrices (génétique), Transcriptome (MeSH), Transduction du signal (MeSH).
- MESH :
- génétique : Populus, Séquences d'acides nucléiques régulatrices.
- métabolisme : Chitinase, Cyclopentanes, Cytochrome P-450 enzyme system, Facteurs de transcription à motifs basiques hélice-boucle-hélice et à glissière à leucines, Inhibiteurs de protéases, Oxylipines, Populus.
- physiologie : Insectes.
- Animaux, Herbivorie, Régulation de l'expression des gènes végétaux, Régulation positive, Transcriptome, Transduction du signal.
English descriptors
- KwdEn :
- Animals (MeSH), Basic Helix-Loop-Helix Leucine Zipper Transcription Factors (metabolism), Chitinases (metabolism), Cyclopentanes (metabolism), Cytochrome P-450 Enzyme System (metabolism), Gene Expression Regulation, Plant (MeSH), Herbivory (MeSH), Insecta (physiology), Oxylipins (metabolism), Populus (genetics), Populus (metabolism), Protease Inhibitors (metabolism), RNA-Seq (MeSH), Regulatory Sequences, Nucleic Acid (genetics), Signal Transduction (MeSH), Transcriptome (MeSH), Up-Regulation (MeSH).
- MESH :
- chemical , metabolism : Basic Helix-Loop-Helix Leucine Zipper Transcription Factors, Chitinases, Cyclopentanes, Cytochrome P-450 Enzyme System, Oxylipins, Protease Inhibitors.
- genetics : Populus, Regulatory Sequences, Nucleic Acid.
- metabolism : Populus.
- physiology : Insecta.
- Animals, Gene Expression Regulation, Plant, Herbivory, RNA-Seq, Signal Transduction, Transcriptome, Up-Regulation.
Abstract
BACKGROUND
Herbivorous insects can have a profound impact on plant growth performance. In some years, canopy damage in poplar plantations exceeds 50% of the total leaf surface, thereby possibly compromising carbon fixation and biomass yield. To assess the transcriptional response of elite poplar clones to insect feeding and to test whether this response varies between different genotypes, we performed an RNA-sequencing experiment. We deeply sequenced the transcriptomes of eight elite clones belonging to three poplar species (Populus trichocarpa, P. nigra and P. maximowiczii), under Phratora vitellinae feeding and control conditions. This allowed us to precisely quantify transcript levels of about 24,000 expressed genes.
RESULTS
Our data reveal a striking overall up-regulation of gene expression under insect attack in all eight poplar clones studied. The up-regulated genes were markedly enriched for the biological process 'regulation of transcription' indicating a highly concerted restructuring of the transcriptome. A search for potential cis-regulatory elements (CREs) that may be involved in this process identified the G-box (CACGTG) as the most significant motif in the promoters of the induced genes. In line with the role of the G-box in jasmonate (JA)-mediated activation of gene expression by MYC2, several genes involved in JA biosynthesis and signaling were up-regulated in our dataset. A co-expression network analysis additionally highlighted WRKY transcription factors. Within the most prominent expression module, WRKYs were strongly overrepresented and occupied several network hubs. Finally, the insect-induced genes comprised several protein families known to be involved in plant defenses, e.g. cytochrome P450s, chitinases and protease inhibitors.
CONCLUSIONS
Our data represent a comprehensive characterization of the transcriptional response of selected elite poplar clones to insect herbivory. Our results suggest that the concerted up-regulation of gene expression is controlled by JA signaling and WRKY transcription factors, and activates several defense mechanisms. Our data highlight potential targets of selection and may thus contribute to breeding insect-resistant poplar clones.
DOI: 10.1186/s12864-019-6048-8
PubMed: 31455224
PubMed Central: PMC6712675
Affiliations:
Links toward previous steps (curation, corpus...)
Le document en format XML
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Müller</name><affiliation wicri:level="1"><nlm:affiliation>Thünen Institute of Forest Genetics, Sieker Landstraße 2, 22927, Grosshansdorf, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Thünen Institute of Forest Genetics, Sieker Landstraße 2, 22927, Grosshansdorf</wicri:regionArea><wicri:noRegion>22927, Grosshansdorf</wicri:noRegion><wicri:noRegion>22927, Grosshansdorf</wicri:noRegion><wicri:noRegion>Grosshansdorf</wicri:noRegion></affiliation></author><author><name sortKey="Kersten, Birgit" sort="Kersten, Birgit" uniqKey="Kersten B" first="Birgit" last="Kersten">Birgit Kersten</name><affiliation wicri:level="1"><nlm:affiliation>Thünen Institute of Forest Genetics, Sieker Landstraße 2, 22927, Grosshansdorf, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Thünen Institute of Forest Genetics, Sieker Landstraße 2, 22927, Grosshansdorf</wicri:regionArea><wicri:noRegion>22927, Grosshansdorf</wicri:noRegion><wicri:noRegion>22927, Grosshansdorf</wicri:noRegion><wicri:noRegion>Grosshansdorf</wicri:noRegion></affiliation></author><author><name sortKey="Fladung, Matthias" sort="Fladung, Matthias" uniqKey="Fladung M" first="Matthias" last="Fladung">Matthias Fladung</name><affiliation wicri:level="1"><nlm:affiliation>Thünen Institute of Forest Genetics, Sieker Landstraße 2, 22927, Grosshansdorf, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Thünen Institute of Forest Genetics, Sieker Landstraße 2, 22927, Grosshansdorf</wicri:regionArea><wicri:noRegion>22927, Grosshansdorf</wicri:noRegion><wicri:noRegion>22927, Grosshansdorf</wicri:noRegion><wicri:noRegion>Grosshansdorf</wicri:noRegion></affiliation></author><author><name sortKey="Schroeder, Hilke" sort="Schroeder, Hilke" uniqKey="Schroeder H" first="Hilke" last="Schroeder">Hilke Schroeder</name><affiliation wicri:level="1"><nlm:affiliation>Thünen Institute of Forest Genetics, Sieker Landstraße 2, 22927, Grosshansdorf, Germany. hilke.schroeder@thuenen.de.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Thünen Institute of Forest Genetics, Sieker Landstraße 2, 22927, Grosshansdorf</wicri:regionArea><wicri:noRegion>22927, Grosshansdorf</wicri:noRegion><wicri:noRegion>22927, Grosshansdorf</wicri:noRegion><wicri:noRegion>Grosshansdorf</wicri:noRegion></affiliation></author></analytic><series><title level="j">BMC genomics</title><idno type="eISSN">1471-2164</idno><imprint><date when="2019" type="published">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Animals (MeSH)</term><term>Basic Helix-Loop-Helix Leucine Zipper Transcription Factors (metabolism)</term><term>Chitinases (metabolism)</term><term>Cyclopentanes (metabolism)</term><term>Cytochrome P-450 Enzyme System (metabolism)</term><term>Gene Expression Regulation, Plant (MeSH)</term><term>Herbivory (MeSH)</term><term>Insecta (physiology)</term><term>Oxylipins (metabolism)</term><term>Populus (genetics)</term><term>Populus (metabolism)</term><term>Protease Inhibitors (metabolism)</term><term>RNA-Seq (MeSH)</term><term>Regulatory Sequences, Nucleic Acid (genetics)</term><term>Signal Transduction (MeSH)</term><term>Transcriptome (MeSH)</term><term>Up-Regulation (MeSH)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Animaux (MeSH)</term><term>Chitinase (métabolisme)</term><term>Cyclopentanes (métabolisme)</term><term>Cytochrome P-450 enzyme system (métabolisme)</term><term>Facteurs de transcription à motifs basiques hélice-boucle-hélice et à glissière à leucines (métabolisme)</term><term>Herbivorie (MeSH)</term><term>Inhibiteurs de protéases (métabolisme)</term><term>Insectes (physiologie)</term><term>Oxylipines (métabolisme)</term><term>Populus (génétique)</term><term>Populus (métabolisme)</term><term>Régulation de l'expression des gènes végétaux (MeSH)</term><term>Régulation positive (MeSH)</term><term>Séquences d'acides nucléiques régulatrices (génétique)</term><term>Transcriptome (MeSH)</term><term>Transduction du signal (MeSH)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Basic Helix-Loop-Helix Leucine Zipper Transcription Factors</term><term>Chitinases</term><term>Cyclopentanes</term><term>Cytochrome P-450 Enzyme System</term><term>Oxylipins</term><term>Protease Inhibitors</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Populus</term><term>Regulatory Sequences, Nucleic Acid</term></keywords><keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>Populus</term><term>Séquences d'acides nucléiques régulatrices</term></keywords><keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Populus</term></keywords><keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Chitinase</term><term>Cyclopentanes</term><term>Cytochrome P-450 enzyme system</term><term>Facteurs de transcription à motifs basiques hélice-boucle-hélice et à glissière à leucines</term><term>Inhibiteurs de protéases</term><term>Oxylipines</term><term>Populus</term></keywords><keywords scheme="MESH" qualifier="physiologie" xml:lang="fr"><term>Insectes</term></keywords><keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Insecta</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Animals</term><term>Gene Expression Regulation, Plant</term><term>Herbivory</term><term>RNA-Seq</term><term>Signal Transduction</term><term>Transcriptome</term><term>Up-Regulation</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Animaux</term><term>Herbivorie</term><term>Régulation de l'expression des gènes végétaux</term><term>Régulation positive</term><term>Transcriptome</term><term>Transduction du signal</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p><b>BACKGROUND</b></p><p>Herbivorous insects can have a profound impact on plant growth performance. In some years, canopy damage in poplar plantations exceeds 50% of the total leaf surface, thereby possibly compromising carbon fixation and biomass yield. To assess the transcriptional response of elite poplar clones to insect feeding and to test whether this response varies between different genotypes, we performed an RNA-sequencing experiment. We deeply sequenced the transcriptomes of eight elite clones belonging to three poplar species (Populus trichocarpa, P. nigra and P. maximowiczii), under Phratora vitellinae feeding and control conditions. This allowed us to precisely quantify transcript levels of about 24,000 expressed genes.</p></div><div type="abstract" xml:lang="en"><p><b>RESULTS</b></p><p>Our data reveal a striking overall up-regulation of gene expression under insect attack in all eight poplar clones studied. The up-regulated genes were markedly enriched for the biological process 'regulation of transcription' indicating a highly concerted restructuring of the transcriptome. A search for potential cis-regulatory elements (CREs) that may be involved in this process identified the G-box (CACGTG) as the most significant motif in the promoters of the induced genes. In line with the role of the G-box in jasmonate (JA)-mediated activation of gene expression by MYC2, several genes involved in JA biosynthesis and signaling were up-regulated in our dataset. A co-expression network analysis additionally highlighted WRKY transcription factors. Within the most prominent expression module, WRKYs were strongly overrepresented and occupied several network hubs. Finally, the insect-induced genes comprised several protein families known to be involved in plant defenses, e.g. cytochrome P450s, chitinases and protease inhibitors.</p></div><div type="abstract" xml:lang="en"><p><b>CONCLUSIONS</b></p><p>Our data represent a comprehensive characterization of the transcriptional response of selected elite poplar clones to insect herbivory. Our results suggest that the concerted up-regulation of gene expression is controlled by JA signaling and WRKY transcription factors, and activates several defense mechanisms. Our data highlight potential targets of selection and may thus contribute to breeding insect-resistant poplar clones.</p></div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">31455224</PMID><DateCompleted><Year>2020</Year><Month>01</Month><Day>08</Day></DateCompleted><DateRevised><Year>2020</Year><Month>02</Month><Day>25</Day></DateRevised><Article PubModel="Electronic"><Journal><ISSN IssnType="Electronic">1471-2164</ISSN><JournalIssue CitedMedium="Internet"><Volume>20</Volume><Issue>1</Issue><PubDate><Year>2019</Year><Month>Aug</Month><Day>28</Day></PubDate></JournalIssue><Title>BMC genomics</Title><ISOAbbreviation>BMC Genomics</ISOAbbreviation></Journal><ArticleTitle>RNA-seq of eight different poplar clones reveals conserved up-regulation of gene expression in response to insect herbivory.</ArticleTitle><Pagination><MedlinePgn>673</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1186/s12864-019-6048-8</ELocationID><Abstract><AbstractText Label="BACKGROUND" NlmCategory="BACKGROUND">Herbivorous insects can have a profound impact on plant growth performance. In some years, canopy damage in poplar plantations exceeds 50% of the total leaf surface, thereby possibly compromising carbon fixation and biomass yield. To assess the transcriptional response of elite poplar clones to insect feeding and to test whether this response varies between different genotypes, we performed an RNA-sequencing experiment. We deeply sequenced the transcriptomes of eight elite clones belonging to three poplar species (Populus trichocarpa, P. nigra and P. maximowiczii), under Phratora vitellinae feeding and control conditions. This allowed us to precisely quantify transcript levels of about 24,000 expressed genes.</AbstractText><AbstractText Label="RESULTS" NlmCategory="RESULTS">Our data reveal a striking overall up-regulation of gene expression under insect attack in all eight poplar clones studied. The up-regulated genes were markedly enriched for the biological process 'regulation of transcription' indicating a highly concerted restructuring of the transcriptome. A search for potential cis-regulatory elements (CREs) that may be involved in this process identified the G-box (CACGTG) as the most significant motif in the promoters of the induced genes. In line with the role of the G-box in jasmonate (JA)-mediated activation of gene expression by MYC2, several genes involved in JA biosynthesis and signaling were up-regulated in our dataset. A co-expression network analysis additionally highlighted WRKY transcription factors. Within the most prominent expression module, WRKYs were strongly overrepresented and occupied several network hubs. Finally, the insect-induced genes comprised several protein families known to be involved in plant defenses, e.g. cytochrome P450s, chitinases and protease inhibitors.</AbstractText><AbstractText Label="CONCLUSIONS" NlmCategory="CONCLUSIONS">Our data represent a comprehensive characterization of the transcriptional response of selected elite poplar clones to insect herbivory. Our results suggest that the concerted up-regulation of gene expression is controlled by JA signaling and WRKY transcription factors, and activates several defense mechanisms. Our data highlight potential targets of selection and may thus contribute to breeding insect-resistant poplar clones.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Müller</LastName><ForeName>Niels A</ForeName><Initials>NA</Initials><AffiliationInfo><Affiliation>Thünen Institute of Forest Genetics, Sieker Landstraße 2, 22927, Grosshansdorf, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kersten</LastName><ForeName>Birgit</ForeName><Initials>B</Initials><AffiliationInfo><Affiliation>Thünen Institute of Forest Genetics, Sieker Landstraße 2, 22927, Grosshansdorf, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Fladung</LastName><ForeName>Matthias</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Thünen Institute of Forest Genetics, Sieker Landstraße 2, 22927, Grosshansdorf, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Schroeder</LastName><ForeName>Hilke</ForeName><Initials>H</Initials><Identifier Source="ORCID">http://orcid.org/0000-0002-0908-3397</Identifier><AffiliationInfo><Affiliation>Thünen Institute of Forest Genetics, Sieker Landstraße 2, 22927, Grosshansdorf, Germany. hilke.schroeder@thuenen.de.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>22000514</GrantID><Agency>Fachagentur Nachwachsende Rohstoffe</Agency><Country></Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2019</Year><Month>08</Month><Day>28</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>BMC Genomics</MedlineTA><NlmUniqueID>100965258</NlmUniqueID><ISSNLinking>1471-2164</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D051778">Basic Helix-Loop-Helix Leucine Zipper Transcription Factors</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D003517">Cyclopentanes</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D054883">Oxylipins</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D011480">Protease Inhibitors</NameOfSubstance></Chemical><Chemical><RegistryNumber>6RI5N05OWW</RegistryNumber><NameOfSubstance UI="C011006">jasmonic acid</NameOfSubstance></Chemical><Chemical><RegistryNumber>9035-51-2</RegistryNumber><NameOfSubstance UI="D003577">Cytochrome P-450 Enzyme System</NameOfSubstance></Chemical><Chemical><RegistryNumber>EC 3.2.1.14</RegistryNumber><NameOfSubstance UI="D002688">Chitinases</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D000818" MajorTopicYN="N">Animals</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D051778" MajorTopicYN="N">Basic Helix-Loop-Helix Leucine Zipper Transcription Factors</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D002688" MajorTopicYN="N">Chitinases</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D003517" MajorTopicYN="N">Cyclopentanes</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D003577" MajorTopicYN="N">Cytochrome P-450 Enzyme System</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D018506" MajorTopicYN="Y">Gene Expression Regulation, Plant</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D060434" MajorTopicYN="Y">Herbivory</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D007313" MajorTopicYN="N">Insecta</DescriptorName><QualifierName UI="Q000502" MajorTopicYN="N">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D054883" MajorTopicYN="N">Oxylipins</DescriptorName><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="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D011480" MajorTopicYN="N">Protease Inhibitors</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D000081246" MajorTopicYN="N">RNA-Seq</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D012045" MajorTopicYN="N">Regulatory Sequences, Nucleic Acid</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D015398" MajorTopicYN="N">Signal Transduction</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D059467" MajorTopicYN="N">Transcriptome</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D015854" MajorTopicYN="N">Up-Regulation</DescriptorName></MeshHeading></MeshHeadingList><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Co-expression network</Keyword><Keyword MajorTopicYN="N">G-box</Keyword><Keyword MajorTopicYN="N">Insect herbivory</Keyword><Keyword MajorTopicYN="N">Jasmonate (JA) signaling</Keyword><Keyword MajorTopicYN="N">Phratora vitellinae</Keyword><Keyword MajorTopicYN="N">Populus</Keyword><Keyword MajorTopicYN="N">WRKY transcription 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