Jurassic NLR: Conserved and dynamic evolutionary features of the atypically ancient immune receptor ZAR1

Adachi, Hiroaki, Sakai, Toshiyuki, Kourelis, Jiorgos ORCID: https://orcid.org/0000-0002-9007-1333, Pai, Hsuan, Gonzalez Hernandez, Jose L., Utsumi, Yoshinori, Seki, Motoaki, Maqbool, Abbas and Kamoun, Sophien ORCID: https://orcid.org/0000-0002-0290-0315 (2023) Jurassic NLR: Conserved and dynamic evolutionary features of the atypically ancient immune receptor ZAR1. Plant Cell, 35 (10). pp. 3662-3685. ISSN 1040-4651

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Plant nucleotide-binding leucine-rich repeat (NLR) immune receptors generally exhibit hallmarks of rapid evolution, even at the intraspecific level. We used iterative sequence similarity searches coupled with phylogenetic analyses to reconstruct the evolutionary history of HOPZ-ACTIVATED RESISTANCE1 (ZAR1), an atypically conserved NLR that traces its origin to early flowering plant lineages ∼220 to 150 million yrs ago (Jurassic period). We discovered 120 ZAR1 orthologs in 88 species, including the monocot Colocasia esculenta, the magnoliid Cinnamomum micranthum, and most eudicots, notably the Ranunculales species Aquilegia coerulea, which is outside the core eudicots. Ortholog sequence analyses revealed highly conserved features of ZAR1, including regions for pathogen effector recognition and cell death activation. We functionally reconstructed the cell death activity of ZAR1 and its partner receptor-like cytoplasmic kinase (RLCK) from distantly related plant species, experimentally validating the hypothesis that ZAR1 evolved to partner with RLCKs early in its evolution. In addition, ZAR1 acquired novel molecular features. In cassava (Manihot esculenta) and cotton (Gossypium spp.), ZAR1 carries a C-terminal thioredoxin-like domain, and in several taxa, ZAR1 duplicated into 2 paralog families, which underwent distinct evolutionary paths. ZAR1 stands out among angiosperm NLR genes for having experienced relatively limited duplication and expansion throughout its deep evolutionary history. Nonetheless, ZAR1 also gave rise to noncanonical NLRs with integrated domains and degenerated molecular features.

Item Type: Article
Additional Information: Funding Information: This work was funded by the Gatsby Charitable Foundation, Biotechnology and Biological Sciences Research Council (BBSRC, UK), and European Research Council (ERC BLASTOFF projects). J.L.G.H. acknowledges support from the South Dakota Agricultural Experiment Station (SD00H605-16). H.A. was funded by the Japan Society for the Promotion of Science (21K20583 and 22K14893) and Japan Science and Technology Agency Precursory Research for Embryonic Science and Technology (JPMJPR21D1). Publisher Copyright: © 2023 American Society of Plant Biologists. All rights reserved.
Uncontrolled Keywords: plant science ,/dk/atira/pure/subjectarea/asjc/1100/1110
Faculty \ School: Faculty of Science > The Sainsbury Laboratory
Faculty of Science > School of Biological Sciences
UEA Research Groups: Faculty of Science > Research Groups > Plant Sciences
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Depositing User: LivePure Connector
Date Deposited: 09 Jan 2024 01:37
Last Modified: 01 Feb 2024 03:07
URI: https://ueaeprints.uea.ac.uk/id/eprint/94110
DOI: 10.1093/plcell/koad175

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