Loading…

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...

Full description

Saved in:
Bibliographic Details
Published in:The Plant journal : for cell and molecular biology 2023-05, Vol.114 (3), p.499-518
Main Authors: Ma, Hui, Lin, Juncheng, Mei, Fangming, Mao, Hude, Li, Qingshun Q.
Format: Article
Language:English
Subjects:
Citations: Items that this one cites
Items that cite this one
Online Access:Get full text
Tags: Add Tag
No Tags, Be the first to tag this record!
cited_by cdi_FETCH-LOGICAL-c3880-b75f4b6d50440fa279842207ed9cc9cd304c7bc2b55be492e4da66f8a6c47fe73
cites cdi_FETCH-LOGICAL-c3880-b75f4b6d50440fa279842207ed9cc9cd304c7bc2b55be492e4da66f8a6c47fe73
container_end_page 518
container_issue 3
container_start_page 499
container_title The Plant journal : for cell and molecular biology
container_volume 114
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
format article
fullrecord <record><control><sourceid>proquest_cross</sourceid><recordid>TN_cdi_proquest_miscellaneous_2776519541</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2807405264</sourcerecordid><originalsourceid>FETCH-LOGICAL-c3880-b75f4b6d50440fa279842207ed9cc9cd304c7bc2b55be492e4da66f8a6c47fe73</originalsourceid><addsrcrecordid>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</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2807405264</pqid></control><display><type>article</type><title>Differential alternative polyadenylation of homoeologous genes of allohexaploid wheat ABD subgenomes during drought stress response</title><source>Wiley</source><source>EZB Electronic Journals Library</source><creator>Ma, Hui ; Lin, Juncheng ; Mei, Fangming ; Mao, Hude ; Li, Qingshun Q.</creator><creatorcontrib>Ma, Hui ; Lin, Juncheng ; Mei, Fangming ; Mao, Hude ; Li, Qingshun Q.</creatorcontrib><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><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 &amp; Sons Ltd.</rights><rights>2023 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley &amp; 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 &amp; 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>
fulltext fulltext
identifier ISSN: 0960-7412
ispartof The Plant journal : for cell and molecular biology, 2023-05, Vol.114 (3), p.499-518
issn 0960-7412
1365-313X
language eng
recordid cdi_proquest_miscellaneous_2776519541
source Wiley; EZB Electronic Journals Library
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
url http://sfxeu10.hosted.exlibrisgroup.com/loughborough?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-05T00%3A36%3A13IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_cross&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Differential%20alternative%20polyadenylation%20of%20homoeologous%20genes%20of%20allohexaploid%20wheat%20ABD%20subgenomes%20during%20drought%20stress%20response&rft.jtitle=The%20Plant%20journal%20:%20for%20cell%20and%20molecular%20biology&rft.au=Ma,%20Hui&rft.date=2023-05&rft.volume=114&rft.issue=3&rft.spage=499&rft.epage=518&rft.pages=499-518&rft.issn=0960-7412&rft.eissn=1365-313X&rft_id=info:doi/10.1111/tpj.16150&rft_dat=%3Cproquest_cross%3E2807405264%3C/proquest_cross%3E%3Cgrp_id%3Ecdi_FETCH-LOGICAL-c3880-b75f4b6d50440fa279842207ed9cc9cd304c7bc2b55be492e4da66f8a6c47fe73%3C/grp_id%3E%3Coa%3E%3C/oa%3E%3Curl%3E%3C/url%3E&rft_id=info:oai/&rft_pqid=2807405264&rft_id=info:pmid/36786697&rfr_iscdi=true