Transcriptional variation in glucosinolate biosynthetic genes and inducible responses to aphid herbivory on field-grown Arabidopsis thaliana

Recently, increasing attempts have been made to understand how plant genes function in natura studies. To determine whether plant defense genes are activated under multiple biotic stimuli, we combined a high-throughput RNA-Seq with insect survey data on 19 accessions of Arabidopsis thaliana growing on the field site of Switzerland. We found that genes with GO annotations “glucosinolate biosynthetic process” and “response to insects” were the most significantly enriched, exhibiting largely variable expression among plant accessions. Nearly half of the total expression variation in glucosinolate biosynthetic genes, AOPs, ESM1, ESP, and TGG1, was explained by among-accession variance. Combined with the field RNA-Seq data, bioassays confirmed that AOP3 was up-regulated in response to the mustard aphid Lipaphis erysimi. In addition, we also found that the expression of a major cis-jasmone activated gene CYP81D11 was positively correlated with the number of the flea beetles Phyllotreta spp. The combined results from RNA-Seq and insect surveys suggested that plants can activate their defenses even when they are exposed to multiple biotic stimuli in natura.