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Differential alternative polyadenylation of homoeologous genes of allohexaploid wheat ABD subgenomes during drought stress response
SUMMARY Because allohexaploid wheat genome contains ABD subgenomes, how the expression of homoeologous genes is coordinated remains largely unknown, particularly at the co‐transcriptional level. Alternative polyadenylation (APA) is an important part of co‐transcriptional regulation, which is crucial...
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Published in: | The Plant journal : for cell and molecular biology 2023-05, Vol.114 (3), p.499-518 |
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creator | Ma, Hui Lin, Juncheng Mei, Fangming Mao, Hude Li, Qingshun Q. |
description | SUMMARY
Because allohexaploid wheat genome contains ABD subgenomes, how the expression of homoeologous genes is coordinated remains largely unknown, particularly at the co‐transcriptional level. Alternative polyadenylation (APA) is an important part of co‐transcriptional regulation, which is crucial in developmental processes and stress responses. Drought stress is a major threat to the stable yield of wheat. Focusing on APA, we used poly(A) tag sequencing to track poly(A) site dynamics in wheat under drought stress. The results showed that drought stress led to extensive APA involving 37–47% of differentially expressed genes in wheat. Significant poly(A) site switching was found in stress‐responsive genes. Interestingly, homoeologous genes exhibit unequal numbers of poly(A) sites, divergent APA patterns with tissue specificity and time‐course dynamics, and distinct 3′‐UTR length changes. Moreover, differentially expressed transcripts in leaves and roots used different poly(A) signals, the up‐ and downregulated isoforms had distinct preferences for non‐canonical poly(A) sites. Genes that encode key polyadenylation factors showed differential expression patterns under drought stress. In summary, poly(A) signals and the changes in core poly(A) factors may widely affect the selection of poly(A) sites and gene expression levels during the response to drought stress, and divergent APA patterns among homoeologous genes add extensive plasticity to this responsive network. These results not only reveal the significant role of APA in drought stress response, but also provide a fresh perspective on how homoeologous genes contribute to adaptability through transcriptome diversity. In addition, this work provides information about the ends of transcripts for a better annotation of the wheat genome.
Significance Statement
The functional conservation and divergence in a polyploidy genome across the subgenomes of wheat have always been intriguing. From the angle of APA, this work not only reveals the widespread occurrence of APA in the allohexaploid wheat and the important role it plays, but also broadens the knowledge of how homoeologous genes contribute to the adaptability and transcriptional plasticity in a polyploidy genome through RNA processing. |
doi_str_mv | 10.1111/tpj.16150 |
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Because allohexaploid wheat genome contains ABD subgenomes, how the expression of homoeologous genes is coordinated remains largely unknown, particularly at the co‐transcriptional level. Alternative polyadenylation (APA) is an important part of co‐transcriptional regulation, which is crucial in developmental processes and stress responses. Drought stress is a major threat to the stable yield of wheat. Focusing on APA, we used poly(A) tag sequencing to track poly(A) site dynamics in wheat under drought stress. The results showed that drought stress led to extensive APA involving 37–47% of differentially expressed genes in wheat. Significant poly(A) site switching was found in stress‐responsive genes. Interestingly, homoeologous genes exhibit unequal numbers of poly(A) sites, divergent APA patterns with tissue specificity and time‐course dynamics, and distinct 3′‐UTR length changes. Moreover, differentially expressed transcripts in leaves and roots used different poly(A) signals, the up‐ and downregulated isoforms had distinct preferences for non‐canonical poly(A) sites. Genes that encode key polyadenylation factors showed differential expression patterns under drought stress. In summary, poly(A) signals and the changes in core poly(A) factors may widely affect the selection of poly(A) sites and gene expression levels during the response to drought stress, and divergent APA patterns among homoeologous genes add extensive plasticity to this responsive network. These results not only reveal the significant role of APA in drought stress response, but also provide a fresh perspective on how homoeologous genes contribute to adaptability through transcriptome diversity. In addition, this work provides information about the ends of transcripts for a better annotation of the wheat genome.
Significance Statement
The functional conservation and divergence in a polyploidy genome across the subgenomes of wheat have always been intriguing. From the angle of APA, this work not only reveals the widespread occurrence of APA in the allohexaploid wheat and the important role it plays, but also broadens the knowledge of how homoeologous genes contribute to the adaptability and transcriptional plasticity in a polyploidy genome through RNA processing.</description><identifier>ISSN: 0960-7412</identifier><identifier>EISSN: 1365-313X</identifier><identifier>DOI: 10.1111/tpj.16150</identifier><identifier>PMID: 36786697</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>3' Untranslated regions ; Adaptability ; allohexaploid ; alternative polyadenylation ; Annotations ; Crop yield ; Divergence ; Drought ; drought stress ; Droughts ; Gene expression ; Gene Expression Regulation ; Gene Expression Regulation, Plant - genetics ; Gene regulation ; Genes ; Genomes ; homoeologous genes ; Isoforms ; Polyadenylation ; Polyadenylation - genetics ; Transcriptome - genetics ; Transcriptomes ; Triticum - genetics ; Triticum - metabolism ; Triticum aestivum ; Wheat</subject><ispartof>The Plant journal : for cell and molecular biology, 2023-05, Vol.114 (3), p.499-518</ispartof><rights>2023 The Authors. published by Society for Experimental Biology and John Wiley & Sons Ltd.</rights><rights>2023 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.</rights><rights>2023. This article is published under http://creativecommons.org/licenses/by-nc/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3880-b75f4b6d50440fa279842207ed9cc9cd304c7bc2b55be492e4da66f8a6c47fe73</citedby><cites>FETCH-LOGICAL-c3880-b75f4b6d50440fa279842207ed9cc9cd304c7bc2b55be492e4da66f8a6c47fe73</cites><orcidid>0000-0002-2484-9952 ; 0000-0003-4737-8978 ; 0000-0002-5795-1099 ; 0000-0003-4105-1480 ; 0000-0002-1413-3627</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36786697$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Ma, Hui</creatorcontrib><creatorcontrib>Lin, Juncheng</creatorcontrib><creatorcontrib>Mei, Fangming</creatorcontrib><creatorcontrib>Mao, Hude</creatorcontrib><creatorcontrib>Li, Qingshun Q.</creatorcontrib><title>Differential alternative polyadenylation of homoeologous genes of allohexaploid wheat ABD subgenomes during drought stress response</title><title>The Plant journal : for cell and molecular biology</title><addtitle>Plant J</addtitle><description>SUMMARY
Because allohexaploid wheat genome contains ABD subgenomes, how the expression of homoeologous genes is coordinated remains largely unknown, particularly at the co‐transcriptional level. Alternative polyadenylation (APA) is an important part of co‐transcriptional regulation, which is crucial in developmental processes and stress responses. Drought stress is a major threat to the stable yield of wheat. Focusing on APA, we used poly(A) tag sequencing to track poly(A) site dynamics in wheat under drought stress. The results showed that drought stress led to extensive APA involving 37–47% of differentially expressed genes in wheat. Significant poly(A) site switching was found in stress‐responsive genes. Interestingly, homoeologous genes exhibit unequal numbers of poly(A) sites, divergent APA patterns with tissue specificity and time‐course dynamics, and distinct 3′‐UTR length changes. Moreover, differentially expressed transcripts in leaves and roots used different poly(A) signals, the up‐ and downregulated isoforms had distinct preferences for non‐canonical poly(A) sites. Genes that encode key polyadenylation factors showed differential expression patterns under drought stress. In summary, poly(A) signals and the changes in core poly(A) factors may widely affect the selection of poly(A) sites and gene expression levels during the response to drought stress, and divergent APA patterns among homoeologous genes add extensive plasticity to this responsive network. These results not only reveal the significant role of APA in drought stress response, but also provide a fresh perspective on how homoeologous genes contribute to adaptability through transcriptome diversity. In addition, this work provides information about the ends of transcripts for a better annotation of the wheat genome.
Significance Statement
The functional conservation and divergence in a polyploidy genome across the subgenomes of wheat have always been intriguing. From the angle of APA, this work not only reveals the widespread occurrence of APA in the allohexaploid wheat and the important role it plays, but also broadens the knowledge of how homoeologous genes contribute to the adaptability and transcriptional plasticity in a polyploidy genome through RNA processing.</description><subject>3' Untranslated regions</subject><subject>Adaptability</subject><subject>allohexaploid</subject><subject>alternative polyadenylation</subject><subject>Annotations</subject><subject>Crop yield</subject><subject>Divergence</subject><subject>Drought</subject><subject>drought stress</subject><subject>Droughts</subject><subject>Gene expression</subject><subject>Gene Expression Regulation</subject><subject>Gene Expression Regulation, Plant - genetics</subject><subject>Gene regulation</subject><subject>Genes</subject><subject>Genomes</subject><subject>homoeologous genes</subject><subject>Isoforms</subject><subject>Polyadenylation</subject><subject>Polyadenylation - genetics</subject><subject>Transcriptome - genetics</subject><subject>Transcriptomes</subject><subject>Triticum - genetics</subject><subject>Triticum - metabolism</subject><subject>Triticum aestivum</subject><subject>Wheat</subject><issn>0960-7412</issn><issn>1365-313X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><recordid>eNp10ctO3DAUBmCrApVh2kVfAFliUxYBO_ElWcLQchFSu6BSd5FjH89k5MTBTkpn3RfH0wEWSHhhy9anXzr-EfpCySlN62wc1qdUUE4-oBktBM8KWvzeQzNSCZJJRvMDdBjjmhAqC8E-ooNCyFKISs7Qv8vWWgjQj61yWLkRQq_G9g_gwbuNMtBvXLr7HnuLV77z4J1f-iniJfQQt6_KOb-Cv2pwvjX4cQVqxOcXlzhOTTK-S8pMoe2X2AQ_LVcjjmOAGHHaBt9H-IT2rXIRPj-fc_Tr-7f7xXV29-PqZnF-l-miLEnWSG5ZIwwnjBGrclmVLM-JBFNpXWlTEKZlo_OG8wZYlQMzSghbKqGZtCCLOfq6yx2Cf5ggjnXXRg3OqR7SRHUupeC04owmevyGrv2UfsYlVRLJCM8FS-pkp3TwMQaw9RDaToVNTUm9baZOzdT_m0n26Dlxajowr_KligTOduCxdbB5P6m-_3m7i3wCdHmbGg</recordid><startdate>202305</startdate><enddate>202305</enddate><creator>Ma, Hui</creator><creator>Lin, Juncheng</creator><creator>Mei, Fangming</creator><creator>Mao, Hude</creator><creator>Li, Qingshun Q.</creator><general>Blackwell Publishing Ltd</general><scope>24P</scope><scope>WIN</scope><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>7QO</scope><scope>7QP</scope><scope>7QR</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-2484-9952</orcidid><orcidid>https://orcid.org/0000-0003-4737-8978</orcidid><orcidid>https://orcid.org/0000-0002-5795-1099</orcidid><orcidid>https://orcid.org/0000-0003-4105-1480</orcidid><orcidid>https://orcid.org/0000-0002-1413-3627</orcidid></search><sort><creationdate>202305</creationdate><title>Differential alternative polyadenylation of homoeologous genes of allohexaploid wheat ABD subgenomes during drought stress response</title><author>Ma, Hui ; Lin, Juncheng ; Mei, Fangming ; Mao, Hude ; Li, Qingshun Q.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3880-b75f4b6d50440fa279842207ed9cc9cd304c7bc2b55be492e4da66f8a6c47fe73</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>3' Untranslated regions</topic><topic>Adaptability</topic><topic>allohexaploid</topic><topic>alternative polyadenylation</topic><topic>Annotations</topic><topic>Crop yield</topic><topic>Divergence</topic><topic>Drought</topic><topic>drought stress</topic><topic>Droughts</topic><topic>Gene expression</topic><topic>Gene Expression Regulation</topic><topic>Gene Expression Regulation, Plant - genetics</topic><topic>Gene regulation</topic><topic>Genes</topic><topic>Genomes</topic><topic>homoeologous genes</topic><topic>Isoforms</topic><topic>Polyadenylation</topic><topic>Polyadenylation - genetics</topic><topic>Transcriptome - genetics</topic><topic>Transcriptomes</topic><topic>Triticum - genetics</topic><topic>Triticum - metabolism</topic><topic>Triticum aestivum</topic><topic>Wheat</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ma, Hui</creatorcontrib><creatorcontrib>Lin, Juncheng</creatorcontrib><creatorcontrib>Mei, Fangming</creatorcontrib><creatorcontrib>Mao, Hude</creatorcontrib><creatorcontrib>Li, Qingshun Q.</creatorcontrib><collection>Wiley-Blackwell Open Access Collection</collection><collection>Wiley Free Archive</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Biotechnology Research Abstracts</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>The Plant journal : for cell and molecular biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ma, Hui</au><au>Lin, Juncheng</au><au>Mei, Fangming</au><au>Mao, Hude</au><au>Li, Qingshun Q.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Differential alternative polyadenylation of homoeologous genes of allohexaploid wheat ABD subgenomes during drought stress response</atitle><jtitle>The Plant journal : for cell and molecular biology</jtitle><addtitle>Plant J</addtitle><date>2023-05</date><risdate>2023</risdate><volume>114</volume><issue>3</issue><spage>499</spage><epage>518</epage><pages>499-518</pages><issn>0960-7412</issn><eissn>1365-313X</eissn><abstract>SUMMARY
Because allohexaploid wheat genome contains ABD subgenomes, how the expression of homoeologous genes is coordinated remains largely unknown, particularly at the co‐transcriptional level. Alternative polyadenylation (APA) is an important part of co‐transcriptional regulation, which is crucial in developmental processes and stress responses. Drought stress is a major threat to the stable yield of wheat. Focusing on APA, we used poly(A) tag sequencing to track poly(A) site dynamics in wheat under drought stress. The results showed that drought stress led to extensive APA involving 37–47% of differentially expressed genes in wheat. Significant poly(A) site switching was found in stress‐responsive genes. Interestingly, homoeologous genes exhibit unequal numbers of poly(A) sites, divergent APA patterns with tissue specificity and time‐course dynamics, and distinct 3′‐UTR length changes. Moreover, differentially expressed transcripts in leaves and roots used different poly(A) signals, the up‐ and downregulated isoforms had distinct preferences for non‐canonical poly(A) sites. Genes that encode key polyadenylation factors showed differential expression patterns under drought stress. In summary, poly(A) signals and the changes in core poly(A) factors may widely affect the selection of poly(A) sites and gene expression levels during the response to drought stress, and divergent APA patterns among homoeologous genes add extensive plasticity to this responsive network. These results not only reveal the significant role of APA in drought stress response, but also provide a fresh perspective on how homoeologous genes contribute to adaptability through transcriptome diversity. In addition, this work provides information about the ends of transcripts for a better annotation of the wheat genome.
Significance Statement
The functional conservation and divergence in a polyploidy genome across the subgenomes of wheat have always been intriguing. From the angle of APA, this work not only reveals the widespread occurrence of APA in the allohexaploid wheat and the important role it plays, but also broadens the knowledge of how homoeologous genes contribute to the adaptability and transcriptional plasticity in a polyploidy genome through RNA processing.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>36786697</pmid><doi>10.1111/tpj.16150</doi><tpages>518</tpages><orcidid>https://orcid.org/0000-0002-2484-9952</orcidid><orcidid>https://orcid.org/0000-0003-4737-8978</orcidid><orcidid>https://orcid.org/0000-0002-5795-1099</orcidid><orcidid>https://orcid.org/0000-0003-4105-1480</orcidid><orcidid>https://orcid.org/0000-0002-1413-3627</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | 3' Untranslated regions Adaptability allohexaploid alternative polyadenylation Annotations Crop yield Divergence Drought drought stress Droughts Gene expression Gene Expression Regulation Gene Expression Regulation, Plant - genetics Gene regulation Genes Genomes homoeologous genes Isoforms Polyadenylation Polyadenylation - genetics Transcriptome - genetics Transcriptomes Triticum - genetics Triticum - metabolism Triticum aestivum Wheat |
title | Differential alternative polyadenylation of homoeologous genes of allohexaploid wheat ABD subgenomes during drought stress response |
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