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Abstract
Interactions between herbivorous insects and their host plants are a central component of terrestrial food webs and a critical topic in agriculture, where a substantial fraction of potential crop yield is lost annually to pests. Important insights into plant–insect interactions have come from research on specific plant defences and insect detoxification mechanisms. Yet, much remains unknown about the molecular mechanisms that mediate plant–insect interactions. Here we use multiple genome-wide approaches to map the molecular basis of herbivory from both plant and insect perspectives, focusing on butterflies and their larval host plants. Parallel genome-wide association studies in the cabbage white butterfly, Pieris rapae, and its host plant, Arabidopsis thaliana, pinpointed a small number of butterfly and plant genes that influenced herbivory. These genes, along with much of the genome, were regulated in a dynamic way over the time course of the feeding interaction. Comparative analyses, including diverse butterfly/plant systems, showed a variety of genome-wide responses to herbivory, as well as a core set of highly conserved genes in butterflies as well as their host plants. These results greatly expand our understanding of the genomic causes and evolutionary consequences of ecological interactions across two of nature’s most diverse taxa, butterflies and flowering plants.
Highlights
The A. thaliana genes we found associated with herbivory did not overlap with those from a recent genomewide association (GWA) study of methionine-derived glucosinolates in A. thaliana[20]
We found that a total of 14,563 genes were differentially expressed in Arabidopsis leaves after P. rapae egg deposition (Fig. 2i)
To further explore the potential role of Osi9E in butterflies, we surveyed spatial and temporal patterns its expression in the four butterfly species and found elevated expression during larval stages, as opposed to pupae and adult, and expression in the larval gut (Supplementary Figs. 7 and 8 and Supplementary Tables 6 and 7). These results suggest Osi9E expression is upregulated in response to contact with host plant tissue
Summary
Genome-wide associations with herbivory in the host plant Arabidopsis thaliana. First, we investigated the genetics of butterfly. –host herbivory by mapping associated variants in parallel GWA studies focused on the flowering plant Arabidopisis thaliana and its natural insect herbivore, the cabbage white butterfly, Pieris rapae For these experiments, we used either 96 natural accessions of A. thaliana (Supplementary Table 1) and a single lab strain of P. rapae (for the plant GWA studies), or the offspring of 96 field-caught females of P. rapae (Supplementary Table 2) and a single accession of A. thaliana (for the butterfly GWA studies). A subset of 12 well-supported candidate genes contained three or more associated SNPs each (Fig. 1a) Eight of these genes were functionally validated using SALK T-DNA mutants, showing increased larval weight gain and/or increased plant material eaten in knockouts versus control (Fig. 1c and Supplementary Table 3). Nature EcOlOgy & EvOlutiOn | VOL 2 | SEPTEMBER 2018 | 1418–1427 | www.nature.com/natecolevol
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