Zucchini Plants Alter Gene Expression and Emission of (E)-Caryophyllene Following Aphis gossypii Infestation

Zucchini (Cucurbita pepo L.) is widely cultivated in temperate regions. One of themajor production challenges is the damage caused by Aphis gossypii (Homoptera:Aphididae), a polyphagous aphid, which can negatively affect its host plant, both directlyby feeding and indirectly by vectoring viruses. To gain insights into the transcriptomeevents that occur during the zucchini-aphid interaction and to understand the early-tolate defense response through gene expression profiles, we performed RNA-sequencing(RNA-Seq) on zucchini leaves challenged by A. gossypii (24, 48, and 96 h postinfestation; hpi). Data analysis indicated a complex and dynamic pattern of geneexpression and a transient transcriptional reconfiguration that involved more than 700differentially expressed genes (DEGs), including a large number of defense-relatedgenes. The down-regulation of key genes of plant immunity, such as leucine-richrepeat (LRR) protein kinases, transcription factors, and genes associated with direct(i.e., protease inhibitors, cysteine peptidases, etc.) and indirect (i.e., terpene synthase)defense responses, suggests the aphid ability to manipulate plant immune responses.We also investigated the emission of volatile organic compounds (VOCs) from infestedplants and observed a reduced emission of (E)-?-caryophyllene at 48 hpi, likely theresult of aphid effectors, which reflects the down-regulation of two genes involvedin the biosynthesis of terpenoids. We showed that (E)-?-caryophyllene emission wasmodified by the duration of plant infestation and by aphid density and that this moleculehighly attracts Aphidius colemani, a parasitic wasp of A. gossypii. With our results wecontributed to the identification of genes involved in cucurbit plant interactions withphloem feeders. Our findings may also help pave the way toward developing tolerantzucchini varieties and to identify molecules for sustainable management of harmfulinsect populations.