UV RESISTANCE LOCUS 8 (UVR8) mediates photomorphogenic responses and acclimation to UV-B radiation by regulating the transcription of a series of transcription factors (TFs). However, the origin and evolution of UVR8-mediated signaling pathways remain largely unknown. In this study, we investigated the origin and evolution of the major components of the UVR8-mediated signaling pathway (UVR8, REPRESSOR OF UV-B PHOTOMORPHOGENESIS [RUP], BRI1-EMS-SUPPRESSOR1 [BES1], BES1-INTERACTING MYC-LIKE 1 (BIM1), WRKY DNA-BINDING PROTEIN 36 (WRKY36), MYB DOMAIN PROTEIN 73/77/13 [MYB73/MYB77/MYB13], and PHYTOCHROME INTERACTING FACTOR 4/5 [PIF4 and PIF5]) using comparative genomics and phylogenetic approaches. We showed that the central regulator UVR8 presented a conservative evolutionary route during plant evolution, and the evolutionary history of downstream negative regulators and TFs was different from that of green plant phylogeny. The canonical UVR8-CONSTITUTIVELY PHOTOMORPHOGENIC 1(COP1)/SUPPRESSOR OF PHYA-105 (SPA)-ELONGATED HYPOCOTYL 5 (HY5)-RUP signaling pathway originated in chlorophytes and conferred green algae the additional ability to cope with UV-B radiation. Moreover, the emergence of multiple UVR8-mediated signaling pathways in charophytes laid the foundations for the cross-talk between UV-B signals and endogenous hormone responses. Importantly, we observed signatures that reflect plant adaptations to high UV-B irradiance in subaerial/terrestrial environments, including positive selection in UVR8 and RUPs and increased copy number of some vital TFs. These results revealed that green plants not only experienced adaptive modifications in the canonical UVR8-COP1/SPA-HY5-RUP signaling pathway, but also diversified their UV-B signal transduction mechanisms through increasing cross-talk with other pathways, such as those associated with brassinosteroids and auxin. This study greatly expands our understanding of molecular evolution and adaptive mechanisms underlying plant UV-B acclimation.

中文翻译：

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植物陆化过程中 UV RESISTANCE LOCUS 8 介导信号的起源和适应性进化

抗紫外线位点 8 (UVR8) 通过调节一系列转录因子 (TF) 的转录来介导光形态发生反应和对 UV-B 辐射的适应。然而，UVR8 介导的信号通路的起源和进化仍然很大程度上未知。在这项研究中，我们研究了 UVR8 介导的信号通路主要成分的起源和进化（UVR8、UV-B 光形态发生的抑制物 [RUP]、BRI1-EMS-SUPPRESSOR1 [BES1]、BES1-INTERACTING MYC-LIKE 1） (BIM1)、WRKY DNA 结合蛋白 36 (WRKY36)、MYB 域蛋白 73/77/13 [MYB73/MYB77/MYB13] 和 PHYTOCHROME 相互作用因子 4/5 [PIF4 和 PIF5]）使用比较基因组学和系统发育方法。我们发现，中央调控因子UVR8在植物进化过程中呈现保守的进化路线，下游负调控因子和转录因子的进化史与绿色植物系统发育不同。经典的UVR8-组成性光形态1（COP1）/PHYA-105抑制剂（SPA）-延长的下胚轴5（HY5）-RUP信号通路起源于叶绿藻，赋予绿藻应对UV-B辐射的额外能力。此外，轮藻中多种 UVR8 介导的信号通路的出现为 UV-B 信号与内源激素反应之间的串扰奠定了基础。重要的是，我们观察到了反映植物对地面/陆地环境中高 UV-B 辐照度的适应的特征，包括 UVR8 和 RUP 的正选择以及一些重要 TF 的拷贝数增加。这些结果表明，绿色植物不仅在经典的 UVR8-COP1/SPA-HY5-RUP 信号通路中经历了适应性修饰，而且还通过增加与其他通路（例如与油菜素类固醇和生长素。这项研究极大地扩展了我们对植物 UV-B 适应的分子进化和适应机制的理解。