Transcriptome responses to different herbivores reveal differences in defense strategies between populations of Eruca sativa

Abstract

Background: Intraspecific variations among induced responses might lead to understanding of adaptive variations in defense strategies against insects. We employed RNA-Seq transcriptome screening to elucidate the molecular basis for phenotypic differences between two populations of Eruca sativa (Brassicaceae), in defense against larvae of the generalist and specialist insects, Spodoptera littoralis and Pieris brassicae, respectively. The E. sativa populations originated from desert and Mediterranean sites, where the plants grow in distinct habitats. Results: Responses to elicitation of the plants' defenses against wounding and insect herbivory resulted in more upregulated transcripts in plants of the Mediterranean population than in those of the desert. PCA analysis differentiated between the two populations and between the elicitation treatments. Comprehensive analysis indicated that defense responses involved induction of the salicylic acid and jasmonic acid pathways in plants of the desert and Mediterranean populations, respectively. In general, the defense response involved upregulation of the aliphatic glucosinolates pathway in plants of the Mediterranean population, whereas herbivory caused downregulation of this pathway in desert plants. Further quantitative RT-PCR analysis indicated that defense response in the desert plants involved higher expression of nitrile-specifier protein (NSP) than in the Mediterranean plants, suggesting that in the desert plants glucosinolates breakdown products are directed to simple-nitriles rather than to the more toxic isothiocyanates. In addition, the defense response in plants of the desert population involved upregulation of flavonoid synthesis and sclerophylly. Conclusions: The results indicated that differing defense responses in plants of the two populations are governed by different signaling cascades. We suggest that adaptive ecotypic differentiation in defense strategies could result from generalist and specialist herbivore pressures in the Mediterranean and desert populations, respectively. Moreover, the defense responses in plants of the desert habitat, which include upregulation of mechanical defenses, also could be associated with their dual role in defense against both biotic and abiotic stresses.