Emergence of isochorismate-based salicylic acid biosynthesis within Brassicales
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.
Article Details
Journal Info
Proceedings of the National Academy of Sciences
National Academy of Sciences
Authors (23)
Kunqi Hong
National Key Laboratory of Agricultural Microbiology, Hubei Hongshan Laboratory, Hubei Key Laboratory of Plant Pathology, College of Plant Science and Technology, Huazhong Agricultural University
Masahito Nakano
National Key Laboratory of Agricultural Microbiology, Hubei Hongshan Laboratory, Hubei Key Laboratory of Plant Pathology, College of Plant Science and Technology, Huazhong Agricultural University
Ying Tang
Linda Jeanguenin
Department of Plant and Microbial Biology, University of Minnesota—Twin Cities
Wenshang Kang
National Key Laboratory of Agricultural Microbiology, Hubei Hongshan Laboratory, Hubei Key Laboratory of Plant Pathology, College of Plant Science and Technology, Huazhong Agricultural University
Yongliang Wang
National Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, College of Plant Science and Technology, Huazhong Agricultural University
Lu Zuo
National Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, College of Plant Science and Technology, Huazhong Agricultural University
Pengyue Li
National Key Laboratory of Agricultural Microbiology, Hubei Hongshan Laboratory, Hubei Key Laboratory of Plant Pathology, College of Plant Science and Technology, Huazhong Agricultural University
Jingjng He
National Key Laboratory of Agricultural Microbiology, Hubei Hongshan Laboratory, Hubei Key Laboratory of Plant Pathology, College of Plant Science and Technology, Huazhong Agricultural University
Wanqing Jiang
National Key Laboratory of Agricultural Microbiology, Hubei Hongshan Laboratory, Hubei Key Laboratory of Plant Pathology, College of Plant Science and Technology, Huazhong Agricultural University
Ruidong Huang
National Key Laboratory of Agricultural Microbiology, Hubei Hongshan Laboratory, Hubei Key Laboratory of Plant Pathology, College of Plant Science and Technology, Huazhong Agricultural University
Hidenori Matsui
Plant Proteomics Research Unit, RIKEN Center for Sustainable Resource Science
Yiming Wang
Hirofumi Nakagami
Bo Li
Xia Li
Kabin Xie
Kenji Fukushima
Center for Frontier Research, National Institute of Genetics
Liang Guo
Department of Chemistry
Xiaowei Han
National Key Laboratory of Agricultural Microbiology, Hubei Hongshan Laboratory, Hubei Key Laboratory of Plant Pathology, College of Plant Science and Technology, Huazhong Agricultural University
Fumiaki Katagiri
Department of Plant and Microbial Biology, University of Minnesota—Twin Cities
Motoyuki Hattori
State Key Laboratory of Genetics and Development of Complex Phenotypes, Collaborative Innovation Center of Genetics and Development, Department of Physiology and Neurobiology, School of Life Sciences, Fudan University
Kenichi Tsuda
National Key Laboratory of Agricultural Microbiology, Hubei Hongshan Laboratory, Hubei Key Laboratory of Plant Pathology, College of Plant Science and Technology, Huazhong Agricultural University