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

Abstract

Zucchini (Cucurbita pepo L.) is widely cultivated in temperate regions. One of the major production challenges is the damage caused by Aphis gossypii (Homoptera: Aphididae), a polyphagous aphid, which can negatively affect its host plant, both directly by feeding and indirectly by vectoring viruses. To gain insights into the transcriptome events that occur during the zucchini–aphid interaction and to understand the early-to-late defense response through gene expression profiles, we performed RNA-sequencing (RNA-Seq) on zucchini leaves challenged by A. gossypii (24, 48, and 96 h post-infestation; hpi). Data analysis indicated a complex and dynamic pattern of gene expression and a transient transcriptional reconfiguration that involved more than 700 differentially expressed genes (DEGs), including a large number of defense-related genes. The down-regulation of key genes of plant immunity, such as leucine-rich repeat (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 infested plants and observed a reduced emission of (E)-β-caryophyllene at 48 hpi, likely the result of aphid effectors, which reflects the down-regulation of two genes involved in the biosynthesis of terpenoids. We showed that (E)-β-caryophyllene emission was modified by the duration of plant infestation and by aphid density and that this molecule highly attracts Aphidius colemani, a parasitic wasp of A. gossypii. With our results we contributed to the identification of genes involved in cucurbit plant interactions with phloem feeders. Our findings may also help pave the way toward developing tolerant zucchini varieties and to identify molecules for sustainable management of harmful insect populations.

Comparative Transcriptome Analysis Reveals Genetic Mechanisms of Sugarcane Aphid Resistance in Grain Sorghum

“…It is not clear if immune receptor-mediated mechanisms mediate responses to SCA feeding in sorghum as they do in the Arabidopsis-Myzus persicae system [28]. However, susceptible plant responses to aphid feeding have been shown to involve the downregulation of key genes involved in plant immunity, as in zucchini plants responding to feeding by Aphis gossypii (Glover) [54].…”

Taxonomic Insights and Its Type Cyclization Correlation of Volatile Sesquiterpenes in Vitex Species and Potential Source Insecticidal Compounds: A Review

“…EβC is involved in the indirect defense of several plants, attracting the natural enemies of above and below-ground pests [12,17,171,172]. The attack of herbivorous insects or treatment with MeJa induced the expression of genes responsible for the transcription of EβC synthase from corn (ZmTPS23), rice (OsTPS3), sorghum (SbTPS4), cotton (GhTPS1), and Switchgrass (PvTPS14), which were responsible for the emission of EβC, attracting herbivore parasitoids and entomopathogenic nematodes [16,42,[172][173][174][175].…”

Development of a Self‐Adhesive Oleogel Formulation Designed for the Slow Release of Semiochemicals

“…𝛽caryophyllene was identified as an attractant for the summer apple psyllid Cacopsylla picta [2] and as a potential repellent for the citrus psyllid Diaphorina citri, [3] both being important phytoplasma vector insects. It was also identified as an attractant for the parasitic wasps Aphidius ervi [4] and A. colemani [5] and was found to be released by root-damaged maize plants as an attractant for the predatory nematode Heterorhabditis megidis. [6] Due to the high volatility and chemical instability of semiochemicals against UV light and oxidation [7] the use of semiochemicals for insect control purposes is often limited.…”