Globally deployed sorghum aphid resistance gene RMES1 is vulnerable to biotype shifts but is 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 have not been clarified and characterized for most sources. In order to assess the current threat of a sorghum aphid (Melanaphis sorghi) biotype shift, we characterized the phenotype of Resistance to Melanaphis sorghi 1 (RMES1) and additional HPR architecture in globally admixed populations selected under severe sorghum 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, Resistance to Melanaphis sorghi 2 (RMES2), was 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 sorghum aphid resistance, RMES1 and RMES2 were selected for demonstrating a lack of severe antagonistic pleiotropy. Associations with resistance colocated with cyanogenic glucoside biosynthesis genes support additional HPR sources. Globally, therefore, an HPR source vulnerable to biotype shift via selection pressure (RMES1) is bolstered by a second common source of resistance in breeding programs (RMES2), which may be staving off a biotype shift and is critical for sustainable sorghum production. Global sorghum production is threatened by herbivorous insects and, recently, sorghum aphids. We tested hypotheses regarding global host plant resistance (HPR) and its risk of being overcome by emergent aphid populations. Sources of sorghum aphid HPR are limited and largely uncharacterized, with a few hypothesized mechanisms proposed. Using greenhouse and field aphid experiments combined with genetic data, we established the selection pressure of the globally used HPR source (Resistance to Melanaphis sorghi 1 [RMES1]) on aphid populations and the availability of additional HPR sources providing resistance in wild and breeding genotypes. Responding to injurious cereal aphid biotype shifts has historically been slow and economically costly. A proactive genotype-to-phenotype map of RMES1 and additional sources for HPR durability will inform cereal-aphid breeding efforts and address a major threat to global agricultural resilience.