The origin and evolution of salicylic acid signaling and biosynthesis in plants

The origin and evolution of salicylic acid signaling and biosynthesis in plants
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植物水杨酸信号传导和生物合成的起源和进化

DOI:
10.1016/j.molp.2022.12.002
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发表时间:
2023
期刊:
影响因子:
27.5
通讯作者:
Yi, Keke
Yi, Keke
中科院分区:
生物学1区
文献类型:
--
作者:
Jia, Xianqing;Wang, Long;Zhao, Hongyu;Zhang, Yibo;Chen, Zhixiang;Xu, Lei;Yi, Keke

文献摘要

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水杨酸(SA)在植物对生物和非生物胁迫的响应中起着关键作用。一些核心的SA信号调节因子和SA生物合成中的关键蛋白已经被很好地描述。然而,关于植物SA信号和生物合成中的核心元件的起源、进化和早期多样化仍有许多未知之处。在这项研究中,我们确定了10个核心蛋白家族在SA信号和生物合成跨绿色植物谱系。我们发现,关键的SA信号受体是病程相关(NPR)蛋白的不表达者,起源于陆地植物最近的共同祖先(MRCA),并在种子植物的祖先中形成了不同的类群。然而,SA信号的关键转录因子TGACG基序结合蛋白(TGACG Motif-bindingProteins,TGAs)起源于链柄植物的MRCA,支持植物中SA核心信号的逐步进化。SA不同于种子植物祖先中核心SA信号通路的组装,SA广泛存在于绿色植物中,包括绿藻和链藻。然而,基于异分支酸合成酶(ICS)的完整SA合成途径首先在陆地植物的MRCA中组装。我们进一步揭示了古异常花序分生组织1(AIM1)的β氧化途径是绿藻SA生物合成的关键,这一生物合成途径可能促进了早期分化的绿藻对陆地高光强环境的适应。综上所述,我们的发现为植物SA信号和生物合成途径的早期进化和多样化提供了重要的见解,突出了SA在植物区域化过程中的逆境耐受性中的关键作用。
Salicylic acid (SA) plays a pivotal role in plant response to biotic and abiotic stress. Several core SA signaling regulators and key proteins in SA biosynthesis have been well characterized. However, much remains unknown about the origin, evolution, and early diversification of core elements in plant SA signaling and biosynthesis. In this study, we identified 10 core protein families in SA signaling and biosynthesis across green plant lineages. We found that the key SA signaling receptors, the nonexpresser of pathogenesis-related (NPR) proteins, originated in the most recent common ancestor (MRCA) of land plants and formed divergent groups in the ancestor of seed plants. However, key transcription factors for SA signaling, TGACG motif-binding proteins (TGAs), originated in the MRCA of streptophytes, arguing for the stepwise evolution of core SA signaling in plants. Different from the assembly of the core SA signaling pathway in the ancestor of seed plants, SA exists extensively in green plants, including chlorophytes and streptophyte algae. However, the full isochorismate synthase (ICS)-based SA synthesis pathway was first assembled in the MRCA of land plants. We further revealed that the ancient abnormal inflorescence meristem 1 (AIM1)-based β-oxidation pathway is crucial for the biosynthesis of SA in chlorophyte algae, and this biosynthesis pathway may have facilitated the adaptation of early-diverging green algae to the high-light-intensity environment on land. Taken together, our findings provide significant insights into the early evolution and diversification of plant SA signaling and biosynthesis pathways, highlighting a crucial role of SA in stress tolerance during plant terrestrialization.