Evolutionary Origin, Gradual Accumulation and Functional Divergence of Heat Shock Factor Gene Family with Plant Evolution

Plants, as sessile organisms, evolved a complex and functionally diverse heat shock factor (HSF) gene family to cope with various environmental stresses. However, the limited evolution studies of the HSF gene family have hindered our understanding of environmental adaptations in plants. In this stud...

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Main Authors: Xiaoming Wang, Xue Shi, Siyuan Chen, Chuang Ma, Shengbao Xu
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-02-01
Series:Frontiers in Plant Science
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fpls.2018.00071/full
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spelling doaj-db32918fa3ed49979514437ce208ff4a2020-11-25T01:28:57ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2018-02-01910.3389/fpls.2018.00071328452Evolutionary Origin, Gradual Accumulation and Functional Divergence of Heat Shock Factor Gene Family with Plant EvolutionXiaoming Wang0Xue Shi1Siyuan Chen2Siyuan Chen3Chuang Ma4Chuang Ma5Shengbao Xu6State Key Laboratory of Crop Stress Biology for Arid Areas, College of Agronomy, Northwest A&F University, Yangling, ChinaState Key Laboratory of Crop Stress Biology for Arid Areas, College of Agronomy, Northwest A&F University, Yangling, ChinaState Key Laboratory of Crop Stress Biology for Arid Areas, College of Life Sciences, Northwest A&F University, Yangling, ChinaCenter of Bioinformatics, College of Life Sciences, Northwest A&F University, Yangling, ChinaState Key Laboratory of Crop Stress Biology for Arid Areas, College of Life Sciences, Northwest A&F University, Yangling, ChinaCenter of Bioinformatics, College of Life Sciences, Northwest A&F University, Yangling, ChinaState Key Laboratory of Crop Stress Biology for Arid Areas, College of Agronomy, Northwest A&F University, Yangling, ChinaPlants, as sessile organisms, evolved a complex and functionally diverse heat shock factor (HSF) gene family to cope with various environmental stresses. However, the limited evolution studies of the HSF gene family have hindered our understanding of environmental adaptations in plants. In this study, a comprehensive evolution analysis on the HSF gene family was performed in 51 representative plant species. Our results demonstrated that the HSFB group which lacks a typical AHA activation domain, was the most ancient, and is under stronger purifying selection pressure in the subsequent evolutionary processes. While, dramatic gene expansion and functional divergence occurred at evolution timescales corresponding to plant land inhabit, which contribute to the emergence and diversification of the HSFA and HSFC groups in land plants. During the plant evolution, the ancestral functions of HSFs were maintained by strong purifying pressure that acted on the DNA binding domain, while the variable oligomerization domain and motif organization of HSFs underwent functional divergence and generated novel subfamilies. At the same time, variations were further accumulated with plant evolution, and this resulted in remarkable functional diversification among higher plant lineages, including distinct HSF numbers and selection pressures of several HSF subfamilies between monocots and eudicots, highlighting the fundamental differences in different plant lineages in response to environmental stresses. Taken together, our study provides novel insights into the evolutionary origin, pattern and selection pressure of plant HSFs and delineates critical clues that aid our understanding of the adaptation processes of plants to terrestrial environments.http://journal.frontiersin.org/article/10.3389/fpls.2018.00071/fullHeat shock factors (HSFs)heat stressabiotic stressevolutionary originsequence diversificationfunctional divergence
collection DOAJ
language English
format Article
sources DOAJ
author Xiaoming Wang
Xue Shi
Siyuan Chen
Siyuan Chen
Chuang Ma
Chuang Ma
Shengbao Xu
spellingShingle Xiaoming Wang
Xue Shi
Siyuan Chen
Siyuan Chen
Chuang Ma
Chuang Ma
Shengbao Xu
Evolutionary Origin, Gradual Accumulation and Functional Divergence of Heat Shock Factor Gene Family with Plant Evolution
Frontiers in Plant Science
Heat shock factors (HSFs)
heat stress
abiotic stress
evolutionary origin
sequence diversification
functional divergence
author_facet Xiaoming Wang
Xue Shi
Siyuan Chen
Siyuan Chen
Chuang Ma
Chuang Ma
Shengbao Xu
author_sort Xiaoming Wang
title Evolutionary Origin, Gradual Accumulation and Functional Divergence of Heat Shock Factor Gene Family with Plant Evolution
title_short Evolutionary Origin, Gradual Accumulation and Functional Divergence of Heat Shock Factor Gene Family with Plant Evolution
title_full Evolutionary Origin, Gradual Accumulation and Functional Divergence of Heat Shock Factor Gene Family with Plant Evolution
title_fullStr Evolutionary Origin, Gradual Accumulation and Functional Divergence of Heat Shock Factor Gene Family with Plant Evolution
title_full_unstemmed Evolutionary Origin, Gradual Accumulation and Functional Divergence of Heat Shock Factor Gene Family with Plant Evolution
title_sort evolutionary origin, gradual accumulation and functional divergence of heat shock factor gene family with plant evolution
publisher Frontiers Media S.A.
series Frontiers in Plant Science
issn 1664-462X
publishDate 2018-02-01
description Plants, as sessile organisms, evolved a complex and functionally diverse heat shock factor (HSF) gene family to cope with various environmental stresses. However, the limited evolution studies of the HSF gene family have hindered our understanding of environmental adaptations in plants. In this study, a comprehensive evolution analysis on the HSF gene family was performed in 51 representative plant species. Our results demonstrated that the HSFB group which lacks a typical AHA activation domain, was the most ancient, and is under stronger purifying selection pressure in the subsequent evolutionary processes. While, dramatic gene expansion and functional divergence occurred at evolution timescales corresponding to plant land inhabit, which contribute to the emergence and diversification of the HSFA and HSFC groups in land plants. During the plant evolution, the ancestral functions of HSFs were maintained by strong purifying pressure that acted on the DNA binding domain, while the variable oligomerization domain and motif organization of HSFs underwent functional divergence and generated novel subfamilies. At the same time, variations were further accumulated with plant evolution, and this resulted in remarkable functional diversification among higher plant lineages, including distinct HSF numbers and selection pressures of several HSF subfamilies between monocots and eudicots, highlighting the fundamental differences in different plant lineages in response to environmental stresses. Taken together, our study provides novel insights into the evolutionary origin, pattern and selection pressure of plant HSFs and delineates critical clues that aid our understanding of the adaptation processes of plants to terrestrial environments.
topic Heat shock factors (HSFs)
heat stress
abiotic stress
evolutionary origin
sequence diversification
functional divergence
url http://journal.frontiersin.org/article/10.3389/fpls.2018.00071/full
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