Ancient pangenomic origins of noncanonical NLR genes underlying the recent evolutionary rescue of a staple crop

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.