The heat shock factor GhHSFA4a positively regulates cotton resistance to Verticillium dahliae

Heat shock factors (HSFs) play a crucial role in the environmental stress responses of numerous plant species, including defense responses to pathogens; however, their role in cotton resistance to Verticillium dahliae remains unclear. We have previously identified several differentially expressed ge...

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Main Authors: Lu Liu, Di Wang, Chao Zhang, Haiyang Liu, Huiming Guo, Hongmei Cheng, Enliang Liu, Xiaofeng Su
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-11-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2022.1050216/full
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author Lu Liu
Di Wang
Chao Zhang
Haiyang Liu
Huiming Guo
Huiming Guo
Hongmei Cheng
Hongmei Cheng
Enliang Liu
Xiaofeng Su
Xiaofeng Su
author_facet Lu Liu
Di Wang
Chao Zhang
Haiyang Liu
Huiming Guo
Huiming Guo
Hongmei Cheng
Hongmei Cheng
Enliang Liu
Xiaofeng Su
Xiaofeng Su
author_sort Lu Liu
collection DOAJ
description Heat shock factors (HSFs) play a crucial role in the environmental stress responses of numerous plant species, including defense responses to pathogens; however, their role in cotton resistance to Verticillium dahliae remains unclear. We have previously identified several differentially expressed genes (DEGs) in Arabidopsis thaliana after inoculation with V. dahliae. Here, we discovered that GhHSFA4a in Gossypium hirsutum (cotton) after inoculation with V. dahliae shares a high identity with a DEG in A. thaliana in response to V. dahliae infection. Quantitative real-time PCR (qRT-PCR) analysis indicated that GhHSFA4a expression was rapidly induced by V. dahliae and ubiquitous in cotton roots, stems, and leaves. In a localization analysis using transient expression, GhHSFA4a was shown to be localized to the nucleus. Virus-induced gene silencing (VIGS) revealed that downregulation of GhHSFA4a significantly increased cotton susceptibility to V. dahliae. To investigate GhHSFA4a-mediated defense, 814 DEGs were identified between GhHSFA4a-silenced plants and controls using comparative RNA-seq analysis. The Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis showed that DEGs were enriched in “flavonoid biosynthesis”, “sesquiterpenoid and triterpenoid biosynthesis”, “linoleic acid metabolism” and “alpha-linolenic acid metabolism”. The expression levels of marker genes for these four pathways were triggered after inoculation with V. dahliae. Moreover, GhHSFA4a-overexpressing lines of A. thaliana displayed enhanced resistance against V. dahliae compared to that of the wild type. These results indicate that GhHSFA4a is involved in the synthesis of secondary metabolites and signal transduction, which are indispensable for innate immunity against V. dahliae in cotton.
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spelling doaj.art-030eb169781e4148a2b5a77b9209575b2022-12-22T03:29:52ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-11-011310.3389/fpls.2022.10502161050216The heat shock factor GhHSFA4a positively regulates cotton resistance to Verticillium dahliaeLu Liu0Di Wang1Chao Zhang2Haiyang Liu3Huiming Guo4Huiming Guo5Hongmei Cheng6Hongmei Cheng7Enliang Liu8Xiaofeng Su9Xiaofeng Su10Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing, ChinaCenter for Advanced Measurement Science, National Institute of Metrology, Beijing, ChinaState Key Laboratory of North China Crop Improvement and Regulation, College of Life Science, Hebei Agricultural University, Baoding, ChinaInstitute of Plant Protection, Xinjiang Academy of Agricultural Sciences, Urumqi, ChinaBiotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing, ChinaHainan Yazhou Bay Seed Lab, Sanya, ChinaBiotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing, ChinaHainan Yazhou Bay Seed Lab, Sanya, ChinaInstitute of Grain Crops, Xinjiang Academy of Agricultural ScienceS, Urumqi, ChinaBiotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing, ChinaHainan Yazhou Bay Seed Lab, Sanya, ChinaHeat shock factors (HSFs) play a crucial role in the environmental stress responses of numerous plant species, including defense responses to pathogens; however, their role in cotton resistance to Verticillium dahliae remains unclear. We have previously identified several differentially expressed genes (DEGs) in Arabidopsis thaliana after inoculation with V. dahliae. Here, we discovered that GhHSFA4a in Gossypium hirsutum (cotton) after inoculation with V. dahliae shares a high identity with a DEG in A. thaliana in response to V. dahliae infection. Quantitative real-time PCR (qRT-PCR) analysis indicated that GhHSFA4a expression was rapidly induced by V. dahliae and ubiquitous in cotton roots, stems, and leaves. In a localization analysis using transient expression, GhHSFA4a was shown to be localized to the nucleus. Virus-induced gene silencing (VIGS) revealed that downregulation of GhHSFA4a significantly increased cotton susceptibility to V. dahliae. To investigate GhHSFA4a-mediated defense, 814 DEGs were identified between GhHSFA4a-silenced plants and controls using comparative RNA-seq analysis. The Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis showed that DEGs were enriched in “flavonoid biosynthesis”, “sesquiterpenoid and triterpenoid biosynthesis”, “linoleic acid metabolism” and “alpha-linolenic acid metabolism”. The expression levels of marker genes for these four pathways were triggered after inoculation with V. dahliae. Moreover, GhHSFA4a-overexpressing lines of A. thaliana displayed enhanced resistance against V. dahliae compared to that of the wild type. These results indicate that GhHSFA4a is involved in the synthesis of secondary metabolites and signal transduction, which are indispensable for innate immunity against V. dahliae in cotton.https://www.frontiersin.org/articles/10.3389/fpls.2022.1050216/fullcottonVerticillium wiltVerticillium dahliaeheat shock factorsGhHSFA4a
spellingShingle Lu Liu
Di Wang
Chao Zhang
Haiyang Liu
Huiming Guo
Huiming Guo
Hongmei Cheng
Hongmei Cheng
Enliang Liu
Xiaofeng Su
Xiaofeng Su
The heat shock factor GhHSFA4a positively regulates cotton resistance to Verticillium dahliae
Frontiers in Plant Science
cotton
Verticillium wilt
Verticillium dahliae
heat shock factors
GhHSFA4a
title The heat shock factor GhHSFA4a positively regulates cotton resistance to Verticillium dahliae
title_full The heat shock factor GhHSFA4a positively regulates cotton resistance to Verticillium dahliae
title_fullStr The heat shock factor GhHSFA4a positively regulates cotton resistance to Verticillium dahliae
title_full_unstemmed The heat shock factor GhHSFA4a positively regulates cotton resistance to Verticillium dahliae
title_short The heat shock factor GhHSFA4a positively regulates cotton resistance to Verticillium dahliae
title_sort heat shock factor ghhsfa4a positively regulates cotton resistance to verticillium dahliae
topic cotton
Verticillium wilt
Verticillium dahliae
heat shock factors
GhHSFA4a
url https://www.frontiersin.org/articles/10.3389/fpls.2022.1050216/full
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