Deciphering the role of the ferulate-5-hydroxylase (F5H) gene in sorghum defense against sugarcane aphids

Sorghum, a major cereal crop grown worldwide for food, feed, and/or fuel, is attacked by sugarcane aphid (SCA; Melanaphis sacchari), a devastating sorghum pest in the United States. Lignin, a complex, heterogeneous polymer present in nearly all plant cell walls, is critical in protecting plants from biotic stresses, yet how lignin modifications in sorghum affect the plant’s resistance to aphids remains unclear. Ferulate-5-hydroxylase (F5H), an enzyme involved in sorghum monolignol biosynthesis, produces the substrate for 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. Together, these findings reveal that F5H-OE amplifies sorghum susceptibility to SCA by disrupting auxin and flavonoid-mediated defenses. Overall, our study provides vital insights into the lignin biosynthesis pathway in sorghum, which can be targeted to enhance resistance to aphids and support the development of innovative and sustainable pest control strategies.