Sorghum <i>ferulate-5-hydroxylase</i> overexpression enhances aphid proliferation and weakens <i>brown midrib12</i> -linked resistance

Despite its resilience, sorghum (Sorghum bicolor) remains vulnerable to biotic stresses, including infestation by the sugarcane aphid (SCA; Melanaphis sacchari), a critical pest of sorghum. Ferulate-5-hydroxylase (F5H), an enzyme involved in sorghum monolignol biosynthesis, 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) plants. Aphid bioassays and feeding behavior analysis using Electrical Penetration Graph (EPG) revealed that aphids prefer to colonize and feed more on F5H-OE plants than on RTx430. Biochemical analyses revealed 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 RTx430 levels. While bmr12 displayed resistance to SCA, the combination of F5H-OE with bmr12 (bmr12-F5H-OE) significantly attenuated the bmr12-conferred resistance. 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.