Han Jiapeng, Xie Xiaoxue, Zhang Yang, Yu Xiaofen, He Guangyuan, Li Yin, Yang Guangxiao
The Genetic Engineering International Cooperation Base of Chinese Ministry of Science and Technology, Key Laboratory of Molecular Biophysics of Chinese Ministry of Education, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan 430074, China.
Plant Physiol. 2022 Aug 29;190(1):421-440. doi: 10.1093/plphys/kiac286.
Adapting to unfavorable environments is a necessary step in plant terrestrialization and radiation. The dehydration-responsive element-binding (DREB) protein subfamily plays a pivotal role in plant abiotic stress regulation. However, relationships between the origin and expansion of the DREB subfamily and adaptive evolution of land plants are still being elucidated. Here, we constructed the evolutionary history of the DREB subfamily by compiling APETALA2/ethylene-responsive element-binding protein superfamily genes from 169 representative species of green plants. Through extensive phylogenetic analyses and comparative genomic analysis, our results revealed that the DREB subfamily diverged from the ethylene-responsive factor (ERF) subfamily in the common ancestor of Zygnemophyceae and Embryophyta during the colonization of land by plants, followed by expansions to form three different ancient archetypal genes in Zygnemophyceae species, designated as groups archetype-I, archetype-II/III, and archetype-IV. Four large-scale expansions paralleling the evolution of land plants led to the nine-subgroup divergence of group archetype-II/III in angiosperms, and five whole-genome duplications during Brassicaceae and Poaceae radiation shaped the diversity of subgroup IIb-1. We identified a Poaceae-specific gene in subgroup IIb-1, ERF014, remaining in a Poaceae-specific microsynteny block and co-evolving with a small heat shock protein cluster. Expression analyses demonstrated that heat acclimation may have driven the neofunctionalization of ERF014s in Pooideae by engaging in the conserved heat-responsive module in Poaceae. This study provides insights into lineage-specific expansion and neofunctionalization in the DREB subfamily, together with evolutionary information valuable for future functional studies of plant stress biology.
适应不利环境是植物陆地化和辐射的必要步骤。脱水响应元件结合（DREB）蛋白亚家族在植物非生物胁迫调控中起关键作用。然而，DREB亚家族的起源与扩张和陆地植物适应性进化之间的关系仍有待阐明。在此，我们通过汇编来自169种代表性绿色植物的APETALA2/乙烯响应元件结合蛋白超家族基因，构建了DREB亚家族的进化史。通过广泛的系统发育分析和比较基因组分析，我们的结果表明，在植物陆地定殖过程中，DREB亚家族在双星藻纲和胚植物的共同祖先中与乙烯响应因子（ERF）亚家族分化，随后扩张形成双星藻纲物种中的三种不同的古老原型基因，分别命名为原型-I组、原型-II/III组和原型-IV组。与陆地植物进化平行的四次大规模扩张导致被子植物中原型-II/III组的九个亚组分化，十字花科和禾本科辐射期间的五次全基因组复制塑造了IIb-1亚组的多样性。我们在IIb-1亚组中鉴定出一个禾本科特有的基因ERF014，它保留在禾本科特有的微共线性模块中，并与一个小热激蛋白簇共同进化。表达分析表明，热驯化可能通过参与禾本科保守的热响应模块，驱动了早熟禾亚科中ERF014的新功能化。本研究为DREB亚家族的谱系特异性扩张和新功能化提供了见解，同时也为植物胁迫生物学的未来功能研究提供了有价值的进化信息。
