Transcriptome-wide identification of novel circular RNAs in soybean in response to low-phosphorus stress
Low-phosphorus (LP) stress is a major factor limiting the growth and yield of soybean. Circular RNAs (circRNAs) are novel noncoding RNAs that play a crucial role in plant responses to abiotic stress. However, how LP stress mediates the biogenesis of circRNAs in soybean remains unclear. Here, to expl...
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| description | Low-phosphorus (LP) stress is a major factor limiting the growth and yield of soybean. Circular RNAs (circRNAs) are novel noncoding RNAs that play a crucial role in plant responses to abiotic stress. However, how LP stress mediates the biogenesis of circRNAs in soybean remains unclear. Here, to explore the response mechanisms of circRNAs to LP stress, the roots of two representative soybean genotypes with different P-use efficiency, Bogao (a LP-sensitive genotype) and Nannong 94156 (a LP-tolerant genotype), were used for the construction of RNA sequencing (RNA-seq) libraries and circRNA identification. In total, 371 novel circRNA candidates, including 120 significantly differentially expressed (DE) circRNAs, were identified across different P levels and genotypes. More DE circRNAs were significantly regulated by LP stress in Bogao than in NN94156, suggesting that the tolerant genotype was less affected by LP stress than the sensitive genotype was; in other words, NN94156 may have a better ability to maintain P homeostasis under LP stress. Moreover, a positive correlation was observed between the expression patterns of P stress-induced circRNAs and their circRNA-host genes. Gene Ontology (GO) enrichment analysis of these circRNA-host genes and microRNA (miRNA)-targeted genes indicated that these DE circRNAs were involved mainly in defense responses, ADP binding, nucleoside binding, organic substance catabolic processes, oxidoreductase activity, and signal transduction. Together, our results revealed that LP stress can significantly alter the genome-wide profiles of circRNAs and indicated that the regulation of circRNAs was both genotype and environment specific in response to LP stress. LP-induced circRNAs might provide a rich resource for LP-responsive circRNA candidates for future studies. |
| doi_str_mv | 10.1371/journal.pone.0227243 |
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Circular RNAs (circRNAs) are novel noncoding RNAs that play a crucial role in plant responses to abiotic stress. However, how LP stress mediates the biogenesis of circRNAs in soybean remains unclear. Here, to explore the response mechanisms of circRNAs to LP stress, the roots of two representative soybean genotypes with different P-use efficiency, Bogao (a LP-sensitive genotype) and Nannong 94156 (a LP-tolerant genotype), were used for the construction of RNA sequencing (RNA-seq) libraries and circRNA identification. In total, 371 novel circRNA candidates, including 120 significantly differentially expressed (DE) circRNAs, were identified across different P levels and genotypes. More DE circRNAs were significantly regulated by LP stress in Bogao than in NN94156, suggesting that the tolerant genotype was less affected by LP stress than the sensitive genotype was; in other words, NN94156 may have a better ability to maintain P homeostasis under LP stress. Moreover, a positive correlation was observed between the expression patterns of P stress-induced circRNAs and their circRNA-host genes. Gene Ontology (GO) enrichment analysis of these circRNA-host genes and microRNA (miRNA)-targeted genes indicated that these DE circRNAs were involved mainly in defense responses, ADP binding, nucleoside binding, organic substance catabolic processes, oxidoreductase activity, and signal transduction. Together, our results revealed that LP stress can significantly alter the genome-wide profiles of circRNAs and indicated that the regulation of circRNAs was both genotype and environment specific in response to LP stress. LP-induced circRNAs might provide a rich resource for LP-responsive circRNA candidates for future studies.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0227243</identifier><identifier>PMID: 31961887</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Abiotic stress ; Adaptation ; Adenosine diphosphate ; Agronomy ; Analysis ; Binding ; Biology and Life Sciences ; Biosynthesis ; Cellular signal transduction ; Collaboration ; Crop yield ; Crops ; Deoxyribonucleic acid ; DNA ; Ecology and Environmental Sciences ; Future predictions ; Gene expression ; Gene Expression Regulation, Plant ; Gene Ontology ; Gene sequencing ; Genes ; Genetic aspects ; Genomes ; Genomics ; Genotype & phenotype ; Genotypes ; Glycine max - genetics ; Glycine max - metabolism ; Homeostasis ; MicroRNA ; MicroRNAs ; miRNA ; Novels ; Nucleosides ; Oxidoreductase ; Phosphorus ; Phosphorus - metabolism ; Physical Sciences ; Plant Roots - genetics ; Plant Roots - metabolism ; Research and analysis methods ; Ribonucleic acid ; RNA ; RNA sequencing ; RNA, Circular - genetics ; RNA, Plant - genetics ; Seeds ; Signal processing ; Signal transduction ; Soybeans ; Stress ; Stress, Physiological ; Transcriptome</subject><ispartof>PloS one, 2020-01, Vol.15 (1), p.e0227243-e0227243</ispartof><rights>COPYRIGHT 2020 Public Library of Science</rights><rights>2020 Lv 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 Lv et al 2020 Lv et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-5e582b8dc809e00ad4cb7fae9cb15128d853e6cb1a64ddc8506203da84cf0a9b3</citedby><cites>FETCH-LOGICAL-c692t-5e582b8dc809e00ad4cb7fae9cb15128d853e6cb1a64ddc8506203da84cf0a9b3</cites><orcidid>0000-0001-6119-9533</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/PMC6974154/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6974154/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79342,79343</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31961887$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Lv, Lingling</creatorcontrib><creatorcontrib>Yu, Kaiye</creatorcontrib><creatorcontrib>Lü, Haiyan</creatorcontrib><creatorcontrib>Zhang, Xiangqian</creatorcontrib><creatorcontrib>Liu, Xiaoqian</creatorcontrib><creatorcontrib>Sun, Chongyuan</creatorcontrib><creatorcontrib>Xu, Huanqing</creatorcontrib><creatorcontrib>Zhang, Jinyu</creatorcontrib><creatorcontrib>He, Xiaohui</creatorcontrib><creatorcontrib>Zhang, Dan</creatorcontrib><title>Transcriptome-wide identification of novel circular RNAs in soybean in response to low-phosphorus stress</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Low-phosphorus (LP) stress is a major factor limiting the growth and yield of soybean. Circular RNAs (circRNAs) are novel noncoding RNAs that play a crucial role in plant responses to abiotic stress. However, how LP stress mediates the biogenesis of circRNAs in soybean remains unclear. Here, to explore the response mechanisms of circRNAs to LP stress, the roots of two representative soybean genotypes with different P-use efficiency, Bogao (a LP-sensitive genotype) and Nannong 94156 (a LP-tolerant genotype), were used for the construction of RNA sequencing (RNA-seq) libraries and circRNA identification. In total, 371 novel circRNA candidates, including 120 significantly differentially expressed (DE) circRNAs, were identified across different P levels and genotypes. More DE circRNAs were significantly regulated by LP stress in Bogao than in NN94156, suggesting that the tolerant genotype was less affected by LP stress than the sensitive genotype was; in other words, NN94156 may have a better ability to maintain P homeostasis under LP stress. Moreover, a positive correlation was observed between the expression patterns of P stress-induced circRNAs and their circRNA-host genes. Gene Ontology (GO) enrichment analysis of these circRNA-host genes and microRNA (miRNA)-targeted genes indicated that these DE circRNAs were involved mainly in defense responses, ADP binding, nucleoside binding, organic substance catabolic processes, oxidoreductase activity, and signal transduction. Together, our results revealed that LP stress can significantly alter the genome-wide profiles of circRNAs and indicated that the regulation of circRNAs was both genotype and environment specific in response to LP stress. LP-induced circRNAs might provide a rich resource for LP-responsive circRNA candidates for future studies.</description><subject>Abiotic stress</subject><subject>Adaptation</subject><subject>Adenosine diphosphate</subject><subject>Agronomy</subject><subject>Analysis</subject><subject>Binding</subject><subject>Biology and Life Sciences</subject><subject>Biosynthesis</subject><subject>Cellular signal transduction</subject><subject>Collaboration</subject><subject>Crop yield</subject><subject>Crops</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>Ecology and Environmental Sciences</subject><subject>Future predictions</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Plant</subject><subject>Gene Ontology</subject><subject>Gene sequencing</subject><subject>Genes</subject><subject>Genetic aspects</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Genotype & phenotype</subject><subject>Genotypes</subject><subject>Glycine max - genetics</subject><subject>Glycine max - metabolism</subject><subject>Homeostasis</subject><subject>MicroRNA</subject><subject>MicroRNAs</subject><subject>miRNA</subject><subject>Novels</subject><subject>Nucleosides</subject><subject>Oxidoreductase</subject><subject>Phosphorus</subject><subject>Phosphorus - metabolism</subject><subject>Physical Sciences</subject><subject>Plant Roots - genetics</subject><subject>Plant Roots - metabolism</subject><subject>Research and analysis methods</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>RNA sequencing</subject><subject>RNA, Circular - genetics</subject><subject>RNA, Plant - genetics</subject><subject>Seeds</subject><subject>Signal processing</subject><subject>Signal transduction</subject><subject>Soybeans</subject><subject>Stress</subject><subject>Stress, 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identification of novel circular RNAs in soybean in response to low-phosphorus stress</title><author>Lv, Lingling ; Yu, Kaiye ; Lü, Haiyan ; Zhang, Xiangqian ; Liu, Xiaoqian ; Sun, Chongyuan ; Xu, Huanqing ; Zhang, Jinyu ; He, Xiaohui ; Zhang, Dan</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-5e582b8dc809e00ad4cb7fae9cb15128d853e6cb1a64ddc8506203da84cf0a9b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Abiotic stress</topic><topic>Adaptation</topic><topic>Adenosine diphosphate</topic><topic>Agronomy</topic><topic>Analysis</topic><topic>Binding</topic><topic>Biology and Life Sciences</topic><topic>Biosynthesis</topic><topic>Cellular signal transduction</topic><topic>Collaboration</topic><topic>Crop yield</topic><topic>Crops</topic><topic>Deoxyribonucleic acid</topic><topic>DNA</topic><topic>Ecology and Environmental Sciences</topic><topic>Future 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One</addtitle><date>2020-01-21</date><risdate>2020</risdate><volume>15</volume><issue>1</issue><spage>e0227243</spage><epage>e0227243</epage><pages>e0227243-e0227243</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Low-phosphorus (LP) stress is a major factor limiting the growth and yield of soybean. Circular RNAs (circRNAs) are novel noncoding RNAs that play a crucial role in plant responses to abiotic stress. However, how LP stress mediates the biogenesis of circRNAs in soybean remains unclear. Here, to explore the response mechanisms of circRNAs to LP stress, the roots of two representative soybean genotypes with different P-use efficiency, Bogao (a LP-sensitive genotype) and Nannong 94156 (a LP-tolerant genotype), were used for the construction of RNA sequencing (RNA-seq) libraries and circRNA identification. In total, 371 novel circRNA candidates, including 120 significantly differentially expressed (DE) circRNAs, were identified across different P levels and genotypes. More DE circRNAs were significantly regulated by LP stress in Bogao than in NN94156, suggesting that the tolerant genotype was less affected by LP stress than the sensitive genotype was; in other words, NN94156 may have a better ability to maintain P homeostasis under LP stress. Moreover, a positive correlation was observed between the expression patterns of P stress-induced circRNAs and their circRNA-host genes. Gene Ontology (GO) enrichment analysis of these circRNA-host genes and microRNA (miRNA)-targeted genes indicated that these DE circRNAs were involved mainly in defense responses, ADP binding, nucleoside binding, organic substance catabolic processes, oxidoreductase activity, and signal transduction. Together, our results revealed that LP stress can significantly alter the genome-wide profiles of circRNAs and indicated that the regulation of circRNAs was both genotype and environment specific in response to LP stress. LP-induced circRNAs might provide a rich resource for LP-responsive circRNA candidates for future studies.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>31961887</pmid><doi>10.1371/journal.pone.0227243</doi><tpages>e0227243</tpages><orcidid>https://orcid.org/0000-0001-6119-9533</orcidid><oa>free_for_read</oa></addata></record> |
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| recordid | cdi_plos_journals_2343021316 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Free Full-Text Journals in Chemistry; Public Library of Science (PLoS) |
| subjects | Abiotic stress Adaptation Adenosine diphosphate Agronomy Analysis Binding Biology and Life Sciences Biosynthesis Cellular signal transduction Collaboration Crop yield Crops Deoxyribonucleic acid DNA Ecology and Environmental Sciences Future predictions Gene expression Gene Expression Regulation, Plant Gene Ontology Gene sequencing Genes Genetic aspects Genomes Genomics Genotype & phenotype Genotypes Glycine max - genetics Glycine max - metabolism Homeostasis MicroRNA MicroRNAs miRNA Novels Nucleosides Oxidoreductase Phosphorus Phosphorus - metabolism Physical Sciences Plant Roots - genetics Plant Roots - metabolism Research and analysis methods Ribonucleic acid RNA RNA sequencing RNA, Circular - genetics RNA, Plant - genetics Seeds Signal processing Signal transduction Soybeans Stress Stress, Physiological Transcriptome |
| title | Transcriptome-wide identification of novel circular RNAs in soybean in response to low-phosphorus stress |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-06T19%3A20%3A55IST&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=Transcriptome-wide%20identification%20of%20novel%20circular%20RNAs%20in%20soybean%20in%20response%20to%20low-phosphorus%20stress&rft.jtitle=PloS%20one&rft.au=Lv,%20Lingling&rft.date=2020-01-21&rft.volume=15&rft.issue=1&rft.spage=e0227243&rft.epage=e0227243&rft.pages=e0227243-e0227243&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0227243&rft_dat=%3Cgale_plos_%3EA611897788%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=2343021316&rft_id=info:pmid/31961887&rft_galeid=A611897788&rft_doaj_id=oai_doaj_org_article_0bcc4112dce04b849056aeb081750f23&rfr_iscdi=true |