Caffeic acid O-methyltransferase-dependent flavonoid defenses promote sorghum resistance to fall armyworm infestation

Sorghum (Sorghum bicolor), one of the world's most important monocot crops, suffers severe yield losses due to attack by a polyphagous insect pest, fall armyworm (FAW; Spodoptera frugiperda). Here, we show that the Brown midrib 12 (Bmr12) gene, which encodes the caffeic acid O-methyltransferase (COMT) enzyme, promotes sorghum defense against FAW. Loss of Bmr12 function resulted in increased susceptibility, but enhanced resistance to FAW was observed in Bmr12-overexpression (OE) plants compared with wild-type (RTx430) plants. Although COMT is associated with modulating lignin levels, FAW infestation resulted in comparable lignin levels between bmr12 and Bmr12-OE sorghum plants. On the contrary, evidence presented here indicates that FAW feeding induced the accumulation of flavonoids, which was previously shown to have a negative impact on FAW growth and survival in Bmr12-OE plants compared with bmr12 and RTx430 plants. Furthermore, a combination of phytohormone profiling and transcriptomic analysis uncovered that COMT-mediated resistance to FAW depends on jasmonic acid (JA) and oxidative stress-associated pathways. Exogenous application of FAW oral secretions stimulated flavonoid accumulation in Bmr12-OE plants compared with bmr12 and RTx430 plants, indicating that COMT has an essential function in perceiving FAW oral cues. Taken together, the critical role of COMT in sorghum defense against FAW hinges upon the interplay between JA and its derivatives and hydrogen peroxide, which potentially helps to mount a robust flavonoid-based host defense upon caterpillar attack.