TY - JOUR
T1 - Jurassic NLR: Conserved and dynamic evolutionary features of the atypically ancient immune receptor ZAR1
AU - Adachi, Hiroaki
AU - Sakai, Toshiyuki
AU - Kourelis, Jiorgos
AU - Pai, Hsuan
AU - Gonzalez Hernandez, Jose L.
AU - Utsumi, Yoshinori
AU - Seki, Motoaki
AU - Maqbool, Abbas
AU - Kamoun, Sophien
N1 - 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).
PY - 2023/10
Y1 - 2023/10
N2 - 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.
AB - 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.
UR - http://www.scopus.com/inward/record.url?scp=85168431643&partnerID=8YFLogxK
U2 - 10.1093/plcell/koad175
DO - 10.1093/plcell/koad175
M3 - Article
C2 - 37467141
AN - SCOPUS:85168431643
VL - 35
SP - 3662
EP - 3685
JO - The Plant Cell
JF - The Plant Cell
SN - 1040-4651
IS - 10
ER -