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Evolution of small RNA expression following hybridization and allopolyploidization: insights from Spartina species (Poaceae, Chloridoideae)
Key Message Differential expression of mi-RNAs targeting developmental processes and progressive downregulation of repeat-associated siRNAs following genome merger and genome duplication in the context of allopolyploid speciation in Spartina . The role of small RNAs on gene expression regulation and...
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Published in: | Plant molecular biology 2020-01, Vol.102 (1-2), p.55-72 |
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container_title | Plant molecular biology |
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creator | Cavé-Radet, Armand Giraud, Delphine Lima, Oscar El Amrani, Abdelhak Aïnouche, Malika Salmon, Armel |
description | Key Message
Differential expression of mi-RNAs targeting developmental processes and progressive downregulation of repeat-associated siRNAs following genome merger and genome duplication in the context of allopolyploid speciation in
Spartina
.
The role of small RNAs on gene expression regulation and genome stability is arousing increased interest and is being explored in various plant systems. In spite of prominence of reticulate evolution and polyploidy that affects the evolutionary history of all plant lineages, very few studies analysed RNAi mechanisms with this respect. Here, we explored small RNAs diversity and expression in the context of recent allopolyploid speciation, using the
Spartina
system, which offers a unique opportunity to explore the immediate changes following hybridization and genome duplication. Small RNA-Seq analyses were conducted on hexaploid parental species (
S. alterniflora
and
S. maritima
), their F1 hybrid
S. x townsendii
, and the neoallododecaploid
S. anglica
. We identified 594 miRNAs, 2197 miRNA-target genes, and 3730 repeat-associated siRNAs (mostly targeting Class I/
Copia
-
Ivana
-
Copia
-
SIRE
and LINEs elements). For both mi- and ra-siRNAs, we detected differential expression patterns following genome merger and genome duplication. These misregulations include non-additive expression of miRNAs in the F1 hybrid and additional changes in the allopolyploid targeting developmental processes. Expression of repeat-associated siRNAs indicates a strengthen of transposable element repression during the allopolyploidization process. Altogether, these results confirm the central role small RNAs play in shaping regulatory changes in naturally formed recent allopolyploids. |
doi_str_mv | 10.1007/s11103-019-00931-w |
format | article |
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Differential expression of mi-RNAs targeting developmental processes and progressive downregulation of repeat-associated siRNAs following genome merger and genome duplication in the context of allopolyploid speciation in
Spartina
.
The role of small RNAs on gene expression regulation and genome stability is arousing increased interest and is being explored in various plant systems. In spite of prominence of reticulate evolution and polyploidy that affects the evolutionary history of all plant lineages, very few studies analysed RNAi mechanisms with this respect. Here, we explored small RNAs diversity and expression in the context of recent allopolyploid speciation, using the
Spartina
system, which offers a unique opportunity to explore the immediate changes following hybridization and genome duplication. Small RNA-Seq analyses were conducted on hexaploid parental species (
S. alterniflora
and
S. maritima
), their F1 hybrid
S. x townsendii
, and the neoallododecaploid
S. anglica
. We identified 594 miRNAs, 2197 miRNA-target genes, and 3730 repeat-associated siRNAs (mostly targeting Class I/
Copia
-
Ivana
-
Copia
-
SIRE
and LINEs elements). For both mi- and ra-siRNAs, we detected differential expression patterns following genome merger and genome duplication. These misregulations include non-additive expression of miRNAs in the F1 hybrid and additional changes in the allopolyploid targeting developmental processes. Expression of repeat-associated siRNAs indicates a strengthen of transposable element repression during the allopolyploidization process. Altogether, these results confirm the central role small RNAs play in shaping regulatory changes in naturally formed recent allopolyploids.</description><identifier>ISSN: 0167-4412</identifier><identifier>EISSN: 1573-5028</identifier><identifier>DOI: 10.1007/s11103-019-00931-w</identifier><identifier>PMID: 31748889</identifier><language>eng</language><publisher>Dordrecht: Springer Netherlands</publisher><subject>Base Sequence ; Biochemistry ; Biodiversity and Ecology ; Biomedical and Life Sciences ; DNA Transposable Elements ; DNA, Plant ; Environmental Sciences ; Evolutionary genetics ; Gene expression ; Gene Expression Regulation, Plant ; Gene regulation ; Genes, Plant - genetics ; Genome, Plant ; Genomes ; Genomic Instability ; Hybridization ; Hybridization, Genetic ; Life Sciences ; MicroRNAs - genetics ; MicroRNAs - metabolism ; miRNA ; Molecular Sequence Annotation ; Plant Pathology ; Plant Sciences ; Poaceae - genetics ; Poaceae - metabolism ; Polyploidy ; RNA, Plant - genetics ; RNA, Plant - metabolism ; RNA-mediated interference ; siRNA ; Spartina ; Speciation ; Transposons</subject><ispartof>Plant molecular biology, 2020-01, Vol.102 (1-2), p.55-72</ispartof><rights>Springer Nature B.V. 2019</rights><rights>Plant Molecular Biology is a copyright of Springer, (2019). All Rights Reserved.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c475t-684931009cdad968bb80a266d726619f4e3f3a0e51e247a6e2765ff68f2ed4b53</citedby><cites>FETCH-LOGICAL-c475t-684931009cdad968bb80a266d726619f4e3f3a0e51e247a6e2765ff68f2ed4b53</cites><orcidid>0000-0003-4479-0801 ; 0000-0001-6078-8379</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,315,786,790,891,27957,27958</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31748889$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://univ-rennes.hal.science/hal-02393952$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Cavé-Radet, Armand</creatorcontrib><creatorcontrib>Giraud, Delphine</creatorcontrib><creatorcontrib>Lima, Oscar</creatorcontrib><creatorcontrib>El Amrani, Abdelhak</creatorcontrib><creatorcontrib>Aïnouche, Malika</creatorcontrib><creatorcontrib>Salmon, Armel</creatorcontrib><title>Evolution of small RNA expression following hybridization and allopolyploidization: insights from Spartina species (Poaceae, Chloridoideae)</title><title>Plant molecular biology</title><addtitle>Plant Mol Biol</addtitle><addtitle>Plant Mol Biol</addtitle><description>Key Message
Differential expression of mi-RNAs targeting developmental processes and progressive downregulation of repeat-associated siRNAs following genome merger and genome duplication in the context of allopolyploid speciation in
Spartina
.
The role of small RNAs on gene expression regulation and genome stability is arousing increased interest and is being explored in various plant systems. In spite of prominence of reticulate evolution and polyploidy that affects the evolutionary history of all plant lineages, very few studies analysed RNAi mechanisms with this respect. Here, we explored small RNAs diversity and expression in the context of recent allopolyploid speciation, using the
Spartina
system, which offers a unique opportunity to explore the immediate changes following hybridization and genome duplication. Small RNA-Seq analyses were conducted on hexaploid parental species (
S. alterniflora
and
S. maritima
), their F1 hybrid
S. x townsendii
, and the neoallododecaploid
S. anglica
. We identified 594 miRNAs, 2197 miRNA-target genes, and 3730 repeat-associated siRNAs (mostly targeting Class I/
Copia
-
Ivana
-
Copia
-
SIRE
and LINEs elements). For both mi- and ra-siRNAs, we detected differential expression patterns following genome merger and genome duplication. These misregulations include non-additive expression of miRNAs in the F1 hybrid and additional changes in the allopolyploid targeting developmental processes. Expression of repeat-associated siRNAs indicates a strengthen of transposable element repression during the allopolyploidization process. Altogether, these results confirm the central role small RNAs play in shaping regulatory changes in naturally formed recent allopolyploids.</description><subject>Base Sequence</subject><subject>Biochemistry</subject><subject>Biodiversity and Ecology</subject><subject>Biomedical and Life Sciences</subject><subject>DNA Transposable Elements</subject><subject>DNA, Plant</subject><subject>Environmental Sciences</subject><subject>Evolutionary genetics</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Plant</subject><subject>Gene regulation</subject><subject>Genes, Plant - genetics</subject><subject>Genome, Plant</subject><subject>Genomes</subject><subject>Genomic Instability</subject><subject>Hybridization</subject><subject>Hybridization, Genetic</subject><subject>Life Sciences</subject><subject>MicroRNAs - genetics</subject><subject>MicroRNAs - metabolism</subject><subject>miRNA</subject><subject>Molecular Sequence Annotation</subject><subject>Plant Pathology</subject><subject>Plant Sciences</subject><subject>Poaceae - genetics</subject><subject>Poaceae - metabolism</subject><subject>Polyploidy</subject><subject>RNA, Plant - genetics</subject><subject>RNA, Plant - metabolism</subject><subject>RNA-mediated interference</subject><subject>siRNA</subject><subject>Spartina</subject><subject>Speciation</subject><subject>Transposons</subject><issn>0167-4412</issn><issn>1573-5028</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><recordid>eNp9kc1u1DAUhS0EokPhBVggS2xaiYD_kjjsRqOWIo0A8bO2nMSeceXEqZ10GF6hL82dpgwSCza2fP2d43t9EHpJyVtKSPkuUUoJzwitMkIqTrPdI7SgecmznDD5GC0ILcpMCMpO0LOUrgkBGS-eohNOSyGlrBbo7uI2-Gl0ocfB4tRp7_HXT0tsfg7RpHSo2-B92Ll-g7f7OrrW_dL3vO5bDHgYgt8PPhwv3mPXJ7fZjgnbGDr8bdBxdL3GaTCNMwmffQm6Mdq8wautD-AIWjieP0dPrPbJvHjYT9GPy4vvq6ts_fnDx9VynTWizMeskAKGhYmbVrdVIetaEs2Koi1hoZUVhluuicmpYaLUhWFlkVtbSMtMK-qcn6Lz2XervRqi63Tcq6Cdulqu1aFGGK94lbNbCuzZzA4x3EwmjapzqTHe696EKSnG4Y8lr5gE9PU_6HWYYg-TACU4h1ZLDhSbqSaGlKKxxw4oUYdY1RyrgljVfaxqB6JXD9ZT3Zn2KPmTIwB8BhJc9RsT_779H9vfXbevAg</recordid><startdate>20200101</startdate><enddate>20200101</enddate><creator>Cavé-Radet, Armand</creator><creator>Giraud, Delphine</creator><creator>Lima, Oscar</creator><creator>El Amrani, Abdelhak</creator><creator>Aïnouche, Malika</creator><creator>Salmon, Armel</creator><general>Springer Netherlands</general><general>Springer Nature B.V</general><general>Springer Verlag (Germany)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7TM</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2O</scope><scope>M7P</scope><scope>MBDVC</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>RC3</scope><scope>7X8</scope><scope>1XC</scope><orcidid>https://orcid.org/0000-0003-4479-0801</orcidid><orcidid>https://orcid.org/0000-0001-6078-8379</orcidid></search><sort><creationdate>20200101</creationdate><title>Evolution of small RNA expression following hybridization and allopolyploidization: insights from Spartina species (Poaceae, Chloridoideae)</title><author>Cavé-Radet, Armand ; Giraud, Delphine ; Lima, Oscar ; El Amrani, Abdelhak ; Aïnouche, Malika ; Salmon, Armel</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c475t-684931009cdad968bb80a266d726619f4e3f3a0e51e247a6e2765ff68f2ed4b53</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Base Sequence</topic><topic>Biochemistry</topic><topic>Biodiversity and Ecology</topic><topic>Biomedical and Life Sciences</topic><topic>DNA Transposable Elements</topic><topic>DNA, Plant</topic><topic>Environmental Sciences</topic><topic>Evolutionary genetics</topic><topic>Gene expression</topic><topic>Gene Expression Regulation, Plant</topic><topic>Gene regulation</topic><topic>Genes, Plant - genetics</topic><topic>Genome, Plant</topic><topic>Genomes</topic><topic>Genomic Instability</topic><topic>Hybridization</topic><topic>Hybridization, Genetic</topic><topic>Life Sciences</topic><topic>MicroRNAs - genetics</topic><topic>MicroRNAs - metabolism</topic><topic>miRNA</topic><topic>Molecular Sequence Annotation</topic><topic>Plant Pathology</topic><topic>Plant Sciences</topic><topic>Poaceae - genetics</topic><topic>Poaceae - metabolism</topic><topic>Polyploidy</topic><topic>RNA, Plant - genetics</topic><topic>RNA, Plant - metabolism</topic><topic>RNA-mediated interference</topic><topic>siRNA</topic><topic>Spartina</topic><topic>Speciation</topic><topic>Transposons</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Cavé-Radet, Armand</creatorcontrib><creatorcontrib>Giraud, Delphine</creatorcontrib><creatorcontrib>Lima, Oscar</creatorcontrib><creatorcontrib>El Amrani, Abdelhak</creatorcontrib><creatorcontrib>Aïnouche, Malika</creatorcontrib><creatorcontrib>Salmon, Armel</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Nucleic Acids Abstracts</collection><collection>ProQuest_Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Research Library (Alumni Edition)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>AUTh Library subscriptions: ProQuest Central</collection><collection>ProQuest Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>Research Library Prep</collection><collection>SciTech Premium Collection (Proquest) (PQ_SDU_P3)</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biological Sciences</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>PML(ProQuest Medical Library)</collection><collection>ProQuest research library</collection><collection>Biological Science Database</collection><collection>Research Library (Corporate)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>ProQuest Central Basic</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><jtitle>Plant molecular biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Cavé-Radet, Armand</au><au>Giraud, Delphine</au><au>Lima, Oscar</au><au>El Amrani, Abdelhak</au><au>Aïnouche, Malika</au><au>Salmon, Armel</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Evolution of small RNA expression following hybridization and allopolyploidization: insights from Spartina species (Poaceae, Chloridoideae)</atitle><jtitle>Plant molecular biology</jtitle><stitle>Plant Mol Biol</stitle><addtitle>Plant Mol Biol</addtitle><date>2020-01-01</date><risdate>2020</risdate><volume>102</volume><issue>1-2</issue><spage>55</spage><epage>72</epage><pages>55-72</pages><issn>0167-4412</issn><eissn>1573-5028</eissn><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-2</notes><notes>content type line 23</notes><abstract>Key Message
Differential expression of mi-RNAs targeting developmental processes and progressive downregulation of repeat-associated siRNAs following genome merger and genome duplication in the context of allopolyploid speciation in
Spartina
.
The role of small RNAs on gene expression regulation and genome stability is arousing increased interest and is being explored in various plant systems. In spite of prominence of reticulate evolution and polyploidy that affects the evolutionary history of all plant lineages, very few studies analysed RNAi mechanisms with this respect. Here, we explored small RNAs diversity and expression in the context of recent allopolyploid speciation, using the
Spartina
system, which offers a unique opportunity to explore the immediate changes following hybridization and genome duplication. Small RNA-Seq analyses were conducted on hexaploid parental species (
S. alterniflora
and
S. maritima
), their F1 hybrid
S. x townsendii
, and the neoallododecaploid
S. anglica
. We identified 594 miRNAs, 2197 miRNA-target genes, and 3730 repeat-associated siRNAs (mostly targeting Class I/
Copia
-
Ivana
-
Copia
-
SIRE
and LINEs elements). For both mi- and ra-siRNAs, we detected differential expression patterns following genome merger and genome duplication. These misregulations include non-additive expression of miRNAs in the F1 hybrid and additional changes in the allopolyploid targeting developmental processes. Expression of repeat-associated siRNAs indicates a strengthen of transposable element repression during the allopolyploidization process. Altogether, these results confirm the central role small RNAs play in shaping regulatory changes in naturally formed recent allopolyploids.</abstract><cop>Dordrecht</cop><pub>Springer Netherlands</pub><pmid>31748889</pmid><doi>10.1007/s11103-019-00931-w</doi><tpages>18</tpages><orcidid>https://orcid.org/0000-0003-4479-0801</orcidid><orcidid>https://orcid.org/0000-0001-6078-8379</orcidid></addata></record> |
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subjects | Base Sequence Biochemistry Biodiversity and Ecology Biomedical and Life Sciences DNA Transposable Elements DNA, Plant Environmental Sciences Evolutionary genetics Gene expression Gene Expression Regulation, Plant Gene regulation Genes, Plant - genetics Genome, Plant Genomes Genomic Instability Hybridization Hybridization, Genetic Life Sciences MicroRNAs - genetics MicroRNAs - metabolism miRNA Molecular Sequence Annotation Plant Pathology Plant Sciences Poaceae - genetics Poaceae - metabolism Polyploidy RNA, Plant - genetics RNA, Plant - metabolism RNA-mediated interference siRNA Spartina Speciation Transposons |
title | Evolution of small RNA expression following hybridization and allopolyploidization: insights from Spartina species (Poaceae, Chloridoideae) |
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