Plant trichomes and a single gene GLABRA1 contribute to insect community composition on field-grown Arabidopsis thaliana

Background: Genetic variation in plants alters insect abundance and community structure in the field; however, little is known about the importance of a single gene among diverse plant genotypes. In this context, Arabidopsis trichomes provide an excellent system to discern the roles of natural variation and a key gene, GLABRA1, in shaping insect communities. In this study, we transplanted two independent glabrous mutants (gl1-1 and gl1-2) and 17 natural accessions of Arabidopsis thaliana to two localities in Switzerland and Japan.\n\nResults: Fifteen insect species inhabited plant accessions, with 10-30% broad-sense heritability of community indices being detected, such as species richness and diversity. The total abundance of leaf-chewing herbivores was negatively correlated with trichome density at both the field sites, while glucosinolates had variable effects on leaf chewers between the two sites. Interestingly, there was a parallel tendency for the abundance of leaf chewers to be higher on gl1-1 and gl1-2 than for their different parental accessions, Ler-1 and Col-0, respectively. Furthermore, the loss of function in the GLABRA1 gene significantly decreased the resistance of plants to the two predominant chewers, flea beetles and turnip sawflies.\n\nConclusions: Overall, our results indicate that insect community composition on A. thaliana is heritable across two distant field sites, with GLABRA1 playing a key role in altering the abundance of leaf-chewing herbivores. Given that such a trichome variation is widely observed in Brassicaceae plants, the present study exemplifies the community-wide impact of a single plant gene on crucifer-feeding insects in the field.