Globally-deployed sorghum aphid resistance gene RMES1 is vulnerable to biotype shifts but being bolstered by RMES2

Durable host plant resistance (HPR) to insect pests is critical for sustainable agriculture. Natural variation exists for aphid HPR in sorghum (Sorghum bicolor) but the genetic architecture and phenotype has not been clarified for most sources. To assess the threat of a sorghum aphid (Melanaphis sorghi) biotype shift, we characterized the phenotype of Resistance to Melanaphis sorghi 1 (RMES1) and contributing HPR architecture in globally-admixed populations selected under severe aphid infestation in Haiti. We found RMES1 reduces sorghum aphid fecundity but not bird cherry-oat aphid (Rhopalosiphum padi) fecundity, suggesting a discriminant HPR response typical of gene-for-gene interaction. A second resistant gene, RMES2, were more frequent than RMES1 resistant alleles in landraces and historic breeding lines. RMES2 contributes early and mid-season aphid resistance in a segregating F2 population, however RMES1 was only significant with mid-season fitness. In a fixed population with high aphid resistance, RMES1 and RMES2 were selected for demonstrating a lack of significant antagonistic pleiotropy. Associations with resistance co-located with cyanogenic glucoside biosynthesis genes support additional HPR sources. Globally, therefore, a vulnerable HPR source (RMES1) is bolstered by a second common source of resistance in breeding programs (RMES2) which may be staving off a biotype shift. HIGHLIGHTThe globally-deployed sorghum aphid resistance gene, RMES1, reduces aphid reproduction and therefore is vulnerable to a biotype shift. A second major gene, RMES2, and cyanogenesis may increase global durability of resistance.