Cargando…

Allelic variation in transcription factor PtoWRKY68 contributes to drought tolerance in Populus

Drought stress limits woody species productivity and influences tree distribution. However, dissecting the molecular mechanisms that underpin drought responses in forest trees can be challenging due to trait complexity. Here, using a panel of 300 Chinese white poplar (Populus tomentosa) accessions c...

Descripción completa

Detalles Bibliográficos
Autores principales: Fang, Yuanyuan, Wang, Dan, Xiao, Liang, Quan, Mingyang, Qi, Weina, Song, Fangyuan, Zhou, Jiaxuan, Liu, Xin, Qin, Shitong, Du, Qingzhang, Liu, Qing, El-Kassaby, Yousry A, Zhang, Deqiang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10469405/
https://www.ncbi.nlm.nih.gov/pubmed/37247391
http://dx.doi.org/10.1093/plphys/kiad315
_version_ 1785099432760442880
author Fang, Yuanyuan
Wang, Dan
Xiao, Liang
Quan, Mingyang
Qi, Weina
Song, Fangyuan
Zhou, Jiaxuan
Liu, Xin
Qin, Shitong
Du, Qingzhang
Liu, Qing
El-Kassaby, Yousry A
Zhang, Deqiang
author_facet Fang, Yuanyuan
Wang, Dan
Xiao, Liang
Quan, Mingyang
Qi, Weina
Song, Fangyuan
Zhou, Jiaxuan
Liu, Xin
Qin, Shitong
Du, Qingzhang
Liu, Qing
El-Kassaby, Yousry A
Zhang, Deqiang
author_sort Fang, Yuanyuan
collection PubMed
description Drought stress limits woody species productivity and influences tree distribution. However, dissecting the molecular mechanisms that underpin drought responses in forest trees can be challenging due to trait complexity. Here, using a panel of 300 Chinese white poplar (Populus tomentosa) accessions collected from different geographical climatic regions in China, we performed a genome-wide association study (GWAS) on seven drought-related traits and identified PtoWRKY68 as a candidate gene involved in the response to drought stress. A 12-bp insertion and/or deletion and three nonsynonymous variants in the PtoWRKY68 coding sequence categorized natural populations of P. tomentosa into two haplotype groups, PtoWRKY68(hap1) and PtoWRKY68(hap2). The allelic variation in these two PtoWRKY68 haplotypes conferred differential transcriptional regulatory activities and binding to the promoters of downstream abscisic acid (ABA) efflux and signaling genes. Overexpression of PtoWRKY68(hap1) and PtoWRKY68(hap2) in Arabidopsis (Arabidopsis thaliana) ameliorated the drought tolerance of two transgenic lines and increased ABA content by 42.7% and 14.3% compared to wild-type plants, respectively. Notably, PtoWRKY68(hap1) (associated with drought tolerance) is ubiquitous in accessions in water-deficient environments, whereas the drought-sensitive allele PtoWRKY68(hap2) is widely distributed in well-watered regions, consistent with the trends in local precipitation, suggesting that these alleles correspond to geographical adaptation in Populus. Moreover, quantitative trait loci analysis and an electrophoretic mobility shift assay showed that SHORT VEGETATIVE PHASE (PtoSVP.3) positively regulates the expression of PtoWRKY68 under drought stress. We propose a drought tolerance regulatory module in which PtoWRKY68 modulates ABA signaling and accumulation, providing insight into the genetic basis of drought tolerance in trees. Our findings will facilitate molecular breeding to improve the drought tolerance of forest trees.
format Online
Article
Text
id pubmed-10469405
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Oxford University Press
record_format MEDLINE/PubMed
spelling pubmed-104694052023-09-01 Allelic variation in transcription factor PtoWRKY68 contributes to drought tolerance in Populus Fang, Yuanyuan Wang, Dan Xiao, Liang Quan, Mingyang Qi, Weina Song, Fangyuan Zhou, Jiaxuan Liu, Xin Qin, Shitong Du, Qingzhang Liu, Qing El-Kassaby, Yousry A Zhang, Deqiang Plant Physiol Research Article Drought stress limits woody species productivity and influences tree distribution. However, dissecting the molecular mechanisms that underpin drought responses in forest trees can be challenging due to trait complexity. Here, using a panel of 300 Chinese white poplar (Populus tomentosa) accessions collected from different geographical climatic regions in China, we performed a genome-wide association study (GWAS) on seven drought-related traits and identified PtoWRKY68 as a candidate gene involved in the response to drought stress. A 12-bp insertion and/or deletion and three nonsynonymous variants in the PtoWRKY68 coding sequence categorized natural populations of P. tomentosa into two haplotype groups, PtoWRKY68(hap1) and PtoWRKY68(hap2). The allelic variation in these two PtoWRKY68 haplotypes conferred differential transcriptional regulatory activities and binding to the promoters of downstream abscisic acid (ABA) efflux and signaling genes. Overexpression of PtoWRKY68(hap1) and PtoWRKY68(hap2) in Arabidopsis (Arabidopsis thaliana) ameliorated the drought tolerance of two transgenic lines and increased ABA content by 42.7% and 14.3% compared to wild-type plants, respectively. Notably, PtoWRKY68(hap1) (associated with drought tolerance) is ubiquitous in accessions in water-deficient environments, whereas the drought-sensitive allele PtoWRKY68(hap2) is widely distributed in well-watered regions, consistent with the trends in local precipitation, suggesting that these alleles correspond to geographical adaptation in Populus. Moreover, quantitative trait loci analysis and an electrophoretic mobility shift assay showed that SHORT VEGETATIVE PHASE (PtoSVP.3) positively regulates the expression of PtoWRKY68 under drought stress. We propose a drought tolerance regulatory module in which PtoWRKY68 modulates ABA signaling and accumulation, providing insight into the genetic basis of drought tolerance in trees. Our findings will facilitate molecular breeding to improve the drought tolerance of forest trees. Oxford University Press 2023-05-29 /pmc/articles/PMC10469405/ /pubmed/37247391 http://dx.doi.org/10.1093/plphys/kiad315 Text en © The Author(s) 2023. Published by Oxford University Press on behalf of American Society of Plant Biologists. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs licence (https://creativecommons.org/licenses/by-nc-nd/4.0/), which permits non-commercial reproduction and distribution of the work, in any medium, provided the original work is not altered or transformed in any way, and that the work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Research Article
Fang, Yuanyuan
Wang, Dan
Xiao, Liang
Quan, Mingyang
Qi, Weina
Song, Fangyuan
Zhou, Jiaxuan
Liu, Xin
Qin, Shitong
Du, Qingzhang
Liu, Qing
El-Kassaby, Yousry A
Zhang, Deqiang
Allelic variation in transcription factor PtoWRKY68 contributes to drought tolerance in Populus
title Allelic variation in transcription factor PtoWRKY68 contributes to drought tolerance in Populus
title_full Allelic variation in transcription factor PtoWRKY68 contributes to drought tolerance in Populus
title_fullStr Allelic variation in transcription factor PtoWRKY68 contributes to drought tolerance in Populus
title_full_unstemmed Allelic variation in transcription factor PtoWRKY68 contributes to drought tolerance in Populus
title_short Allelic variation in transcription factor PtoWRKY68 contributes to drought tolerance in Populus
title_sort allelic variation in transcription factor ptowrky68 contributes to drought tolerance in populus
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10469405/
https://www.ncbi.nlm.nih.gov/pubmed/37247391
http://dx.doi.org/10.1093/plphys/kiad315
work_keys_str_mv AT fangyuanyuan allelicvariationintranscriptionfactorptowrky68contributestodroughttoleranceinpopulus
AT wangdan allelicvariationintranscriptionfactorptowrky68contributestodroughttoleranceinpopulus
AT xiaoliang allelicvariationintranscriptionfactorptowrky68contributestodroughttoleranceinpopulus
AT quanmingyang allelicvariationintranscriptionfactorptowrky68contributestodroughttoleranceinpopulus
AT qiweina allelicvariationintranscriptionfactorptowrky68contributestodroughttoleranceinpopulus
AT songfangyuan allelicvariationintranscriptionfactorptowrky68contributestodroughttoleranceinpopulus
AT zhoujiaxuan allelicvariationintranscriptionfactorptowrky68contributestodroughttoleranceinpopulus
AT liuxin allelicvariationintranscriptionfactorptowrky68contributestodroughttoleranceinpopulus
AT qinshitong allelicvariationintranscriptionfactorptowrky68contributestodroughttoleranceinpopulus
AT duqingzhang allelicvariationintranscriptionfactorptowrky68contributestodroughttoleranceinpopulus
AT liuqing allelicvariationintranscriptionfactorptowrky68contributestodroughttoleranceinpopulus
AT elkassabyyousrya allelicvariationintranscriptionfactorptowrky68contributestodroughttoleranceinpopulus
AT zhangdeqiang allelicvariationintranscriptionfactorptowrky68contributestodroughttoleranceinpopulus