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

Hiroaki Adachi, Toshiyuki Sakai, Jiorgos Kourelis, Hsuan Pai, Jose L. Gonzalez Hernandez, Yoshinori Utsumi, Motoaki Seki, Abbas Maqbool, Sophien Kamoun

Research output: Contribution to journalArticlepeer-review

6 Citations (Scopus)

Abstract

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.

Original languageEnglish
Pages (from-to)3662-3685
Number of pages24
JournalPlant Cell
Volume35
Issue number10
Early online date19 Jul 2023
DOIs
Publication statusPublished - Oct 2023

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