Emergence of isochorismate-based salicylic acid biosynthesis within Brassicales.

IF 9.4 1区 综合性期刊 Q1 MULTIDISCIPLINARY SCIENCES
Kunqi Hong, Masahito Nakano, Ying Tang, Linda Jeanguenin, Wenshang Kang, Yongliang Wang, Lu Zuo, Pengyue Li, Jingjng He, Wanqing Jiang, Ruidong Huang, Hidenori Matsui, Yiming Wang, Hirofumi Nakagami, Bo Li, Xia Li, Kabin Xie, Kenji Fukushima, Liang Guo, Xiaowei Han, Fumiaki Katagiri, Motoyuki Hattori, Kenichi Tsuda
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Abstract

Salicylic acid (SA) is a major defense phytohormone. In Arabidopsis thaliana, the isochorismate (IC) pathway is the primary route for pathogen-induced SA biosynthesis. First, the IC synthase (ICS) catalyzes the isomerization of chorismate to IC in chloroplasts. Second, the chloroplast-localized MATE transporter EDS5 appears to transport IC from chloroplasts to the cytosol. Cytosolic IC is then further converted to SA via the GH3 amino acid-conjugating enzyme PBS3. While this pathway is genetically well-characterized in A. thaliana, its evolutionary origin and conservation remain controversial. In this study, through comprehensive phylogenetic, structural, and functional analyses, we demonstrate that the IC pathway emerged within the Brassicales order in a time span between the divergence of Carica papaya and Capparis spinosa. The evolution of the IC pathway was driven by three key adaptations during the time span: 1) enhancement of ICS activity, 2) neofunctionalization of EDS5 after duplication of its ancestral gene, and 3) evolution of a PBS3, whose activity is specialized for glutamate-conjugation to IC. Structural modeling and functional assays reveal that an enhanced salt bridge network in ICS enhanced its activity. One of the duplicated genes, EDS5, acquired key amino acid substitutions in the C-lobe, which contributed to the EDS5 neofunctionalization. In addition, the functional PBS3 clade, including A. thaliana PBS3, is restricted to a Brassicales clade. Taken together, this study addresses the evolutionary trajectory of IC-based SA biosynthesis.

十字花科植物中以异氯酸盐为基础的水杨酸生物合成的出现。
水杨酸(Salicylic acid, SA)是植物的主要防御激素。在拟南芥中,等chorismate (IC)途径是病原体诱导SA生物合成的主要途径。首先,IC合成酶(ICS)在叶绿体中催化氯酸盐异构化成IC。其次,叶绿体定位的MATE转运体EDS5似乎将IC从叶绿体运输到细胞质。然后,胞质IC通过GH3氨基酸偶联酶PBS3进一步转化为SA。虽然这一途径在拟南芥中有很好的遗传特征,但其进化起源和保护仍然存在争议。本研究通过系统发育、结构和功能的综合分析,证明了IC通路是在番木瓜(Carica papaya)和红椒(Capparis spinosa)分化过程中出现的。IC通路的进化是由三个关键的适应所驱动的:1)ICS活性的增强,2)EDS5在其祖先基因复制后的新功能化,以及3)PBS3的进化,其活性专门用于谷氨酸与IC的偶联。结构建模和功能分析表明,ICS中增强的盐桥网络增强了其活性。其中一个重复基因EDS5在C-lobe获得了关键氨基酸的替换,这有助于EDS5的新功能化。此外,包括拟南芥在内的功能性PBS3分支仅限于芸苔科分支。综上所述,本研究解决了基于ic的SA生物合成的进化轨迹。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
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来源期刊
CiteScore
19.00
自引率
0.90%
发文量
3575
审稿时长
2.5 months
期刊介绍: The Proceedings of the National Academy of Sciences (PNAS), a peer-reviewed journal of the National Academy of Sciences (NAS), serves as an authoritative source for high-impact, original research across the biological, physical, and social sciences. With a global scope, the journal welcomes submissions from researchers worldwide, making it an inclusive platform for advancing scientific knowledge.
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