Transcriptomic and metabolomic insights into the mechanisms of pest resistance in cowpea (Vigna unguiculata L.)

• May pea black (R1) deployed rapid JA-dependent flavonoid accumulation for early defense • LD03 (R2) employed sustained MAPK-mediated alkaloid synthesis and structural reinforcement • VuLTR1 and VuLTR2 identified as core transcriptional regulators • Pyramiding both resistance modules enabled sustainable control of pesticide-resistant leafminers Cowpea is a vital protein source in semi-arid regions yet suffers annual yield losses ranging from 15% to 60% due to the American serpentine leafminer. Comparative analyses between highly resistant cultivars, namely May Pea Black (R1) and LD03 (R2), and susceptible varieties revealed distinct defensive approaches. R1 triggers a rapid chemical defense involving early activation of jasmonic acid (JA) signaling that promotes phenylpropanoid and flavonoid biosynthesis. Conversely, R2 implements structural reinforcement mediated by MAPK cascades that lead to alkaloid synthesis and cell wall strengthening while gradually increasing salicylic acid (SA) signaling. Integration of multi-omics data confirmed the coordinated regulation of the flavonoid pathway in R1 and identified VuLTR1 and VuLTR2 as significant regulators. These results indicate that resistance is shaped by temporal dynamics and JA-SA crosstalk, identifying CHS, F3H , and VuLTR2 as primary candidates for pyramiding defenses in cowpea breeding programs.