Ancient pangenomic origins of noncanonical NLR genes underlying the recent evolutionary rescue of a staple crop
Carl VanGessel, Terry Felderhoff, Daniil M. Prigozhin, Meihua Cui, Gaël Pressoir, Adam Healey, John T. Lovell, Vamsi J. Nalam, Marc T. Nishimura, Geoffrey P. Morris
Abstract
The recent adaptation of the cereal crop sorghum to a global aphid outbreak was a fortuitous case of evolutionary rescue, but the pangenomic and molecular basis is not known. We show that RMES1 disrupts phloem feeding via activation of conserved immunity networks, with a growth-to-defense transition mediated by phytohormone signaling and activated by nucleotide-binding site–leucine-rich repeat receptor (NLR) resistance genes on a structural variant. The causative NLRs [resistance to Melanaphis sorghi 1A (RMES1A) and RMES1B] lack signaling domains and have adenosine triphosphatase mutations expected to abrogate function, suggesting that RMES1 NLRs regulate immunity via a noncanonical mechanism. The RMES1 NLR family is ancient, orthologous to phloem-feeding resistance genes in rice and syntenic across the grass superpangenome. Thus, gene birth-and-death processes at an ancient gene cluster created rare standing variation and provided the adaptive allele for evolutionary rescue.