Transcriptomic and metabolomic reprogramming in cotton after Apolygus lucorum feeding implicated in enhancing recruitment of the parasitoid Peristenus spretus

Different types of insect feeding can activate distinct plant resistance mechanisms and trigger the generation of specific volatile compounds. Transcriptomic changes and the genomic basis underlying plant defense in response to chewing herbivores or phloem-feeding insects have been relatively well investigated, while better insight into molecular mechanisms underlying the plant defense response, in particular, volatile emissions triggered by sap-feeding insects such as the green plant bug Apolygus lucorum is needed. Here, we monitored transcriptomic and volatile metabolomic changes in cotton over time during A. lucorum infestation. RNA-seq analysis showed that 1614 transcripts were differentially expressed (log2|Ratio| ≥ 1; q ≤ 0.05) in cotton leaves infested by A. lucorum. All differentially expressed genes (DEGs) in jasmonic acid (JA; 48 genes) and salicylic acid (SA; 5 genes) pathways were upregulated, highlighting a central role of JA in A. lucorum-induced signaling without attenuating the SA pathway. Moreover, all DEGs (30 genes) involved in herbivore-induced volatile biosynthesis were upregulated. Consistently, A. lucorum-induced cotton volatile blends and synthetic methyl salicylate significantly attracted the parasitoid Peristenus spretus. The present data indicated that cotton plants after A. lucorum infestation undergo rapid, extensive transcriptome reprogramming mediated by complex signaling networks in which the JA and SA pathways act synergistically, leading to a specific volatile profile involved in an indirect plant defense.