College of Life Sciences, Nanjing Normal University, Nanjing 210023, China.
National Key Laboratory of Plant Molecular Genetics (NKLPMG), CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology (SIPPE), Chinese Academy of Sciences, Shanghai 200032, China.
Plant Physiol. 2022 Jan 20;188(1):332-346. doi: 10.1093/plphys/kiab486.
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.
UV 抵抗基因座 8（UVR8）通过调控一系列转录因子（TFs）的转录，介导光形态建成响应和对 UV-B 辐射的适应。然而，UVR8 介导的信号通路的起源和进化在很大程度上仍然未知。在这项研究中，我们利用比较基因组学和系统发育分析的方法，研究了 UVR8 介导的信号通路的主要成分（UVR8、UV-B 光形态建成抑制物 [RUP]、BRI1-EMS 抑制物 1 [BES1]、BES1 相互作用 MYC 样蛋白 1 [BIM1]、WRKY DNA 结合蛋白 36 [WRKY36]、MYB 结构域蛋白 73/77/13 [MYB73/MYB77/MYB13] 和 PHYTOCHROME INTERACTING FACTOR 4/5 [PIF4 和 PIF5]）的起源和进化。我们表明，中心调节因子 UVR8 在植物进化过程中呈现出保守的进化途径，而下游负调节因子和 TFs 的进化历史与绿色植物的系统发育不同。规范的 UVR8-CONSTITUTIVELY PHOTOMORPHOGENIC 1（COP1）/SUPPRESSOR OF PHYA-105（SPA）-ELONGATED HYPOCOTYL 5（HY5）-RUP 信号通路起源于绿藻，并赋予绿藻额外的能力来应对 UV-B 辐射。此外，在轮藻门中出现的多种 UVR8 介导的信号通路为 UV-B 信号与内源性激素反应之间的串扰奠定了基础。重要的是，我们观察到反映植物适应高 UV-B 辐照的特征，包括 UVR8 和 RUPs 的正选择和一些重要 TFs 的拷贝数增加。这些结果表明，绿色植物不仅在规范的 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途径的串扰，如与油菜素内酯和生长素相关的途径，多样化了它们的 UV-B 信号转导机制。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。
