Sorghum Ferulate-5-hydroxylase overexpression enhances aphid proliferation and weakens brown midrib12 -linked resistance

Despite its general resilience, sorghum (Sorghum bicolor) remains vulnerable to biotic stresses, including infestation by the sugarcane aphid (SCA; Melanaphis sacchari), which is a critical pest of this crop. Ferulate-5-hydroxylase (F5H), an enzyme involved in monolignol biosynthesis in sorghum, acts upstream of caffeic acid O-methyltransferase (COMT), which is encoded by the Brown midrib12 (Bmr12) gene. Loss of COMT activity enhances SCA resistance by increasing levels of the auxin conjugate indole-3-acetic acid-aspartate (IAA-Asp). To assess the role of F5H in sorghum defense against SCA, we compared F5H-overexpressing (OE) lines with RTx430 wild-type (WT) plants. Aphid bioassays and feeding behavior analysis using an electrical penetration graph (EPG) system showed that aphids prefer to colonize and feed more on F5H-OE plants than on the WT. Biochemical analyses indicated similar lignin levels between lines, but F5H-OE plants had lower basal flavonoids. Moreover, SCA infestation suppressed auxin signal transduction genes that restrict aphid proliferation. Interestingly, exogenous application of IAA-Asp restored SCA resistance in F5H-OE plants to WT levels. While the bmr12 mutant displayed resistance to SCA, the cross between F5H-OE and bmr12 resulted in significant attenuation of the bmr12-conferred resistance. Taken together, these findings reveal that F5H-OE amplifies sorghum susceptibility to SCA by disrupting auxin and flavonoid-mediated defenses, while reaffirming that the loss of Bmr12 function confers strong aphid resistance.