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.

中文翻译：

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绿色植物中脱水反应性元素结合蛋白亚家族的进化。

适应不利环境是植物陆化辐射的必要步骤。脱水反应元件结合 (DREB) 蛋白亚家族在植物非生物胁迫调控中起着关键作用。然而，DREB 亚科的起源和扩展与陆生植物适应性进化之间的关系仍在阐明中。在这里，我们通过编译来自 169 种绿色植物代表性物种的 APETALA2/乙烯反应元件结合蛋白超家族基因，构建了 DREB 亚科的进化史。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，DREB 亚科在植物在陆地上的定殖过程中与 Zygnemophyceae 和 Embryophyta 的共同祖先中的乙烯反应因子 (ERF) 亚科分离开来，随后在 Zygnemophyceae 物种中扩展以形成三个不同的古代原型基因，指定为 archetype-I、archetype-II/III 和 archetype-IV 组。平行于陆生植物进化的四次大规模扩张导致被子植物原型 II/III 的九个亚群分化，十字花科和禾本科辐射期间的五次全基因组复制形成了 IIb-1 亚群的多样性。我们在 IIb-1 亚组 ERF014 中发现了一个禾本科特有基因，该基因保留在禾本科特有的微同步块中，并与一个小的热休克蛋白簇共同进化。表达分析表明，热驯化可能通过参与禾本科中的保守热响应模块来驱动禾本科中 ERF014 的新功能化。