Impaired Brown midrib12 function orchestrates sorghum resistance to aphids via an auxin conjugate indole-3-acetic acid-aspartic acid.

Lignin, a complex heterogenous polymer present in virtually all plant cell walls, plays a critical role in protecting plants from various stresses. However, little is known about how lignin modifications in sorghum will impact plant defense against sugarcane aphids (SCA), a key pest of sorghum. We utilized the sorghum brown midrib (bmr) mutants, which are impaired in monolignol synthesis, to understand sorghum defense mechanisms against SCA. We found that loss of Bmr12 function and overexpression (OE) of Bmr12 provided enhanced resistance and susceptibility to SCA, respectively, as compared with wild-type (WT; RTx430) plants. Monitoring of the aphid feeding behavior indicated that SCA spent more time in reaching the first sieve element phase on bmr12 plants compared with RTx430 and Bmr12-OE plants. A combination of transcriptomic and metabolomic analyses revealed that bmr12 plants displayed altered auxin metabolism upon SCA infestation and specifically, elevated levels of auxin conjugate indole-3-acetic acid-aspartic acid (IAA-Asp) were observed in bmr12 plants compared with RTx430 and Bmr12-OE plants. Furthermore, exogenous application of IAA-Asp restored resistance in Bmr12-OE plants, and artificial diet aphid feeding trial bioassays revealed that IAA-Asp is associated with enhanced resistance to SCA. Our findings highlight the molecular underpinnings that contribute to sorghum bmr12-mediated resistance to SCA.