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

Adachi, Hiroaki; Sakai, Toshiyuki; Kourelis, Jiorgos; Hernandez, Jose L. Gonzalez; Maqbool, Abbas; Kamoun, Sophien

In plants, NLR immune receptors generally exhibit hallmarks of rapid evolution even at the intraspecific level. We reconstructed the evolutionary history of ZAR1, an atypically conserved NLR that traces its origin to early flowering plant lineages ~220 to 150 million years ago (Jurassic period). Ortholog sequence analyses revealed highly conserved features of ZAR1, including regions for pathogen effector recognition, intramolecular interactions and cell death activation. This uncovered a new conserved surface on the ZAR1 resistosome underside that is required for cell death induction. Throughout its evolution, ZAR1 acquired novel features, such as a C-terminal integration of a thioredoxin-like domain. ZAR1 duplicated into two paralog families, which underwent distinct evolutionary paths. We conclude that ZAR1 stands out among angiosperm NLRs for having experienced relatively limited gene duplication and expansion throughout its deep evolutionary history. Nonetheless, ZAR1 did also give rise to non-canonical NLR proteins with integrated domains and degenerated molecular features.