Sugarcane mosaic virus mediated changes in cytosine methylation pattern and differentially transcribed fragments in resistance-contrasting sugarcane genotypes
Sugarcane mosaic virus (SCMV) is the causal agent of sugarcane mosaic disease (SMD) in Brazil; it is mainly controlled by using resistant cultivars. Studies on the changes in sugarcane transcriptome provided the first insights about the molecular basis underlying the genetic resistance to SMD; nonet...
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| description | Sugarcane mosaic virus (SCMV) is the causal agent of sugarcane mosaic disease (SMD) in Brazil; it is mainly controlled by using resistant cultivars. Studies on the changes in sugarcane transcriptome provided the first insights about the molecular basis underlying the genetic resistance to SMD; nonetheless, epigenetic modifications such as cytosine methylation is also informative, considering its roles in gene expression regulation. In our previous study, differentially transcribed fragments (DTFs) were obtained using cDNA-amplified fragment length polymorphism by comparing mock- and SCMV-inoculated plants from two sugarcane cultivars with contrasting responses to SMD. In this study, the identification of unexplored DTFs was continued while the same leaf samples were used to evaluate SCMV-mediated changes in the cytosine methylation pattern by using methylation-sensitive amplification polymorphism. This analysis revealed minor changes in cytosine methylation in response to SCMV infection, but distinct changes between the cultivars with contrasting responses to SMD, with higher hypomethylation events 24 and 72 h post-inoculation in the resistant cultivar. The differentially methylated fragments (DMFs) aligned with transcripts, putative promoters, and genomic regions, with a preponderant distribution within CpG islands. The transcripts found were associated with plant immunity and other stress responses, epigenetic changes, and transposable elements. The DTFs aligned with transcripts assigned to stress responses, epigenetic changes, photosynthesis, lipid transport, and oxidoreductases, in which the transcriptional start site is located in proximity with CpG islands and tandem repeats. Real-time quantitative polymerase chain reaction results revealed significant upregulation in the resistant cultivar of aspartyl protease and VQ protein, respectively, selected from DMF and DTF alignments, suggesting their roles in genetic resistance to SMD and supporting the influence of cytosine methylation in gene expression. Thus, we identified new candidate genes for further validation and showed that the changes in cytosine methylation may regulate important mechanisms underlying the genetic resistance to SMD. |
| doi_str_mv | 10.1371/journal.pone.0241493 |
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Studies on the changes in sugarcane transcriptome provided the first insights about the molecular basis underlying the genetic resistance to SMD; nonetheless, epigenetic modifications such as cytosine methylation is also informative, considering its roles in gene expression regulation. In our previous study, differentially transcribed fragments (DTFs) were obtained using cDNA-amplified fragment length polymorphism by comparing mock- and SCMV-inoculated plants from two sugarcane cultivars with contrasting responses to SMD. In this study, the identification of unexplored DTFs was continued while the same leaf samples were used to evaluate SCMV-mediated changes in the cytosine methylation pattern by using methylation-sensitive amplification polymorphism. This analysis revealed minor changes in cytosine methylation in response to SCMV infection, but distinct changes between the cultivars with contrasting responses to SMD, with higher hypomethylation events 24 and 72 h post-inoculation in the resistant cultivar. The differentially methylated fragments (DMFs) aligned with transcripts, putative promoters, and genomic regions, with a preponderant distribution within CpG islands. The transcripts found were associated with plant immunity and other stress responses, epigenetic changes, and transposable elements. The DTFs aligned with transcripts assigned to stress responses, epigenetic changes, photosynthesis, lipid transport, and oxidoreductases, in which the transcriptional start site is located in proximity with CpG islands and tandem repeats. Real-time quantitative polymerase chain reaction results revealed significant upregulation in the resistant cultivar of aspartyl protease and VQ protein, respectively, selected from DMF and DTF alignments, suggesting their roles in genetic resistance to SMD and supporting the influence of cytosine methylation in gene expression. Thus, we identified new candidate genes for further validation and showed that the changes in cytosine methylation may regulate important mechanisms underlying the genetic resistance to SMD.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0241493</identifier><identifier>PMID: 33166323</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Amplification ; Amplified fragment length polymorphism ; Aspartic endopeptidase ; Biology and life sciences ; CpG islands ; Crop diseases ; Cultivars ; Cytosine ; Cytosine - metabolism ; Deoxyribonucleic acid ; Disease resistance ; Disease resistance (Plants) ; Disease Resistance - genetics ; Diseases and pests ; DNA ; DNA methylation ; DNA Methylation - genetics ; Epigenetics ; Fragments ; Gene expression ; Gene Expression Regulation, Plant ; Gene polymorphism ; Gene regulation ; Genetic aspects ; Genomes ; Genomics ; Genotype ; Genotypes ; Influence ; Inoculation ; Islands ; Lipids ; Methylation ; Mosaic disease ; Photosynthesis ; Physical Sciences ; Physiological aspects ; Plant Diseases - genetics ; Plant Diseases - virology ; Plant immunity ; Plant virus diseases ; Plant viruses ; Polymerase chain reaction ; Polymorphism ; Potyvirus - physiology ; Principal Component Analysis ; Research and Analysis Methods ; RNA, Messenger - genetics ; RNA, Messenger - metabolism ; Saccharum - genetics ; Saccharum - virology ; Silicon carbide ; Sorghum ; Sugarcane ; Transcription ; Transcription, Genetic ; Viruses</subject><ispartof>PloS one, 2020-11, Vol.15 (11), p.e0241493-e0241493</ispartof><rights>COPYRIGHT 2020 Public Library of Science</rights><rights>2020 da Silva et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2020 da Silva et al 2020 da Silva et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-baea212af57151c15a685bd4a0d10da18f481f8af6b8fc94b4e45df9f74159ea3</citedby><cites>FETCH-LOGICAL-c692t-baea212af57151c15a685bd4a0d10da18f481f8af6b8fc94b4e45df9f74159ea3</cites><orcidid>0000-0002-7369-7609 ; 0000-0002-9923-7459</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7652275/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7652275/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793,79600,79601</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33166323$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Mondal, Tapan Kumar</contributor><creatorcontrib>da Silva, Marcel Fernando</creatorcontrib><creatorcontrib>Gonçalves, Marcos Cesar</creatorcontrib><creatorcontrib>Brito, Michael Dos Santos</creatorcontrib><creatorcontrib>Medeiros, Cibele Nataliane</creatorcontrib><creatorcontrib>Harakava, Ricardo</creatorcontrib><creatorcontrib>Landell, Marcos Guimarães de Andrade</creatorcontrib><creatorcontrib>Pinto, Luciana Rossini</creatorcontrib><title>Sugarcane mosaic virus mediated changes in cytosine methylation pattern and differentially transcribed fragments in resistance-contrasting sugarcane genotypes</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Sugarcane mosaic virus (SCMV) is the causal agent of sugarcane mosaic disease (SMD) in Brazil; it is mainly controlled by using resistant cultivars. Studies on the changes in sugarcane transcriptome provided the first insights about the molecular basis underlying the genetic resistance to SMD; nonetheless, epigenetic modifications such as cytosine methylation is also informative, considering its roles in gene expression regulation. In our previous study, differentially transcribed fragments (DTFs) were obtained using cDNA-amplified fragment length polymorphism by comparing mock- and SCMV-inoculated plants from two sugarcane cultivars with contrasting responses to SMD. In this study, the identification of unexplored DTFs was continued while the same leaf samples were used to evaluate SCMV-mediated changes in the cytosine methylation pattern by using methylation-sensitive amplification polymorphism. This analysis revealed minor changes in cytosine methylation in response to SCMV infection, but distinct changes between the cultivars with contrasting responses to SMD, with higher hypomethylation events 24 and 72 h post-inoculation in the resistant cultivar. The differentially methylated fragments (DMFs) aligned with transcripts, putative promoters, and genomic regions, with a preponderant distribution within CpG islands. The transcripts found were associated with plant immunity and other stress responses, epigenetic changes, and transposable elements. The DTFs aligned with transcripts assigned to stress responses, epigenetic changes, photosynthesis, lipid transport, and oxidoreductases, in which the transcriptional start site is located in proximity with CpG islands and tandem repeats. Real-time quantitative polymerase chain reaction results revealed significant upregulation in the resistant cultivar of aspartyl protease and VQ protein, respectively, selected from DMF and DTF alignments, suggesting their roles in genetic resistance to SMD and supporting the influence of cytosine methylation in gene expression. Thus, we identified new candidate genes for further validation and showed that the changes in cytosine methylation may regulate important mechanisms underlying the genetic resistance to SMD.</description><subject>Amplification</subject><subject>Amplified fragment length polymorphism</subject><subject>Aspartic endopeptidase</subject><subject>Biology and life sciences</subject><subject>CpG islands</subject><subject>Crop diseases</subject><subject>Cultivars</subject><subject>Cytosine</subject><subject>Cytosine - metabolism</subject><subject>Deoxyribonucleic acid</subject><subject>Disease resistance</subject><subject>Disease resistance (Plants)</subject><subject>Disease Resistance - genetics</subject><subject>Diseases and pests</subject><subject>DNA</subject><subject>DNA methylation</subject><subject>DNA Methylation - genetics</subject><subject>Epigenetics</subject><subject>Fragments</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Plant</subject><subject>Gene polymorphism</subject><subject>Gene regulation</subject><subject>Genetic aspects</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Genotype</subject><subject>Genotypes</subject><subject>Influence</subject><subject>Inoculation</subject><subject>Islands</subject><subject>Lipids</subject><subject>Methylation</subject><subject>Mosaic disease</subject><subject>Photosynthesis</subject><subject>Physical Sciences</subject><subject>Physiological aspects</subject><subject>Plant Diseases - 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metabolism</topic><topic>Deoxyribonucleic acid</topic><topic>Disease resistance</topic><topic>Disease resistance (Plants)</topic><topic>Disease Resistance - genetics</topic><topic>Diseases and pests</topic><topic>DNA</topic><topic>DNA methylation</topic><topic>DNA Methylation - genetics</topic><topic>Epigenetics</topic><topic>Fragments</topic><topic>Gene expression</topic><topic>Gene Expression Regulation, Plant</topic><topic>Gene polymorphism</topic><topic>Gene regulation</topic><topic>Genetic aspects</topic><topic>Genomes</topic><topic>Genomics</topic><topic>Genotype</topic><topic>Genotypes</topic><topic>Influence</topic><topic>Inoculation</topic><topic>Islands</topic><topic>Lipids</topic><topic>Methylation</topic><topic>Mosaic disease</topic><topic>Photosynthesis</topic><topic>Physical Sciences</topic><topic>Physiological aspects</topic><topic>Plant Diseases - genetics</topic><topic>Plant Diseases - virology</topic><topic>Plant immunity</topic><topic>Plant virus diseases</topic><topic>Plant viruses</topic><topic>Polymerase chain reaction</topic><topic>Polymorphism</topic><topic>Potyvirus - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>da Silva, Marcel Fernando</au><au>Gonçalves, Marcos Cesar</au><au>Brito, Michael Dos Santos</au><au>Medeiros, Cibele Nataliane</au><au>Harakava, Ricardo</au><au>Landell, Marcos Guimarães de Andrade</au><au>Pinto, Luciana Rossini</au><au>Mondal, Tapan Kumar</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Sugarcane mosaic virus mediated changes in cytosine methylation pattern and differentially transcribed fragments in resistance-contrasting sugarcane genotypes</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2020-11-09</date><risdate>2020</risdate><volume>15</volume><issue>11</issue><spage>e0241493</spage><epage>e0241493</epage><pages>e0241493-e0241493</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Sugarcane mosaic virus (SCMV) is the causal agent of sugarcane mosaic disease (SMD) in Brazil; it is mainly controlled by using resistant cultivars. Studies on the changes in sugarcane transcriptome provided the first insights about the molecular basis underlying the genetic resistance to SMD; nonetheless, epigenetic modifications such as cytosine methylation is also informative, considering its roles in gene expression regulation. In our previous study, differentially transcribed fragments (DTFs) were obtained using cDNA-amplified fragment length polymorphism by comparing mock- and SCMV-inoculated plants from two sugarcane cultivars with contrasting responses to SMD. In this study, the identification of unexplored DTFs was continued while the same leaf samples were used to evaluate SCMV-mediated changes in the cytosine methylation pattern by using methylation-sensitive amplification polymorphism. This analysis revealed minor changes in cytosine methylation in response to SCMV infection, but distinct changes between the cultivars with contrasting responses to SMD, with higher hypomethylation events 24 and 72 h post-inoculation in the resistant cultivar. The differentially methylated fragments (DMFs) aligned with transcripts, putative promoters, and genomic regions, with a preponderant distribution within CpG islands. The transcripts found were associated with plant immunity and other stress responses, epigenetic changes, and transposable elements. The DTFs aligned with transcripts assigned to stress responses, epigenetic changes, photosynthesis, lipid transport, and oxidoreductases, in which the transcriptional start site is located in proximity with CpG islands and tandem repeats. Real-time quantitative polymerase chain reaction results revealed significant upregulation in the resistant cultivar of aspartyl protease and VQ protein, respectively, selected from DMF and DTF alignments, suggesting their roles in genetic resistance to SMD and supporting the influence of cytosine methylation in gene expression. Thus, we identified new candidate genes for further validation and showed that the changes in cytosine methylation may regulate important mechanisms underlying the genetic resistance to SMD.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>33166323</pmid><doi>10.1371/journal.pone.0241493</doi><tpages>e0241493</tpages><orcidid>https://orcid.org/0000-0002-7369-7609</orcidid><orcidid>https://orcid.org/0000-0002-9923-7459</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2020-11, Vol.15 (11), p.e0241493-e0241493 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_2458949797 |
| source | MEDLINE; Public Library of Science; PubMed Central; Directory of Open Access Journals; Free Full-Text Journals in Chemistry; EZB Electronic Journals Library |
| subjects | Amplification Amplified fragment length polymorphism Aspartic endopeptidase Biology and life sciences CpG islands Crop diseases Cultivars Cytosine Cytosine - metabolism Deoxyribonucleic acid Disease resistance Disease resistance (Plants) Disease Resistance - genetics Diseases and pests DNA DNA methylation DNA Methylation - genetics Epigenetics Fragments Gene expression Gene Expression Regulation, Plant Gene polymorphism Gene regulation Genetic aspects Genomes Genomics Genotype Genotypes Influence Inoculation Islands Lipids Methylation Mosaic disease Photosynthesis Physical Sciences Physiological aspects Plant Diseases - genetics Plant Diseases - virology Plant immunity Plant virus diseases Plant viruses Polymerase chain reaction Polymorphism Potyvirus - physiology Principal Component Analysis Research and Analysis Methods RNA, Messenger - genetics RNA, Messenger - metabolism Saccharum - genetics Saccharum - virology Silicon carbide Sorghum Sugarcane Transcription Transcription, Genetic Viruses |
| title | Sugarcane mosaic virus mediated changes in cytosine methylation pattern and differentially transcribed fragments in resistance-contrasting sugarcane genotypes |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-01T11%3A30%3A32IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Sugarcane%20mosaic%20virus%20mediated%20changes%20in%20cytosine%20methylation%20pattern%20and%20differentially%20transcribed%20fragments%20in%20resistance-contrasting%20sugarcane%20genotypes&rft.jtitle=PloS%20one&rft.au=da%20Silva,%20Marcel%20Fernando&rft.date=2020-11-09&rft.volume=15&rft.issue=11&rft.spage=e0241493&rft.epage=e0241493&rft.pages=e0241493-e0241493&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0241493&rft_dat=%3Cgale_plos_%3EA641043226%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2458949797&rft_id=info:pmid/33166323&rft_galeid=A641043226&rft_doaj_id=oai_doaj_org_article_5cf0ad76374d4e629c455519f49dce34&rfr_iscdi=true |