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

Yasuhiro Sato,Kentaro K Shimizu,Misako Yamazaki,Rie Shimizu-Inatsugi,Atsushi J Nagano

doi:10.1186/s12870-019-1705-2

Abstract

BackgroundGenetic 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.ResultsFifteen insect species inhabited the plant accessions, with the insect community composition significantly attributed to variations among plant accessions. The total abundance of leaf-chewing herbivores was negatively correlated with trichome density at both field sites, while glucosinolates had variable effects on leaf chewers between the sites. Interestingly, there was a parallel tendency for the abundance of leaf chewers to be higher on gl1–1 and gl1–2 than on 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.ConclusionsOverall, our results indicate that insect community composition significantly varies among A. thaliana accessions 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 effect of a single plant gene on crucifer-feeding insects in the field.

Highlights

Genetic variation in plants alters insect abundance and community structure in the field; little is known about the importance of a single gene among diverse plant genotypes
The accessions with a strong dormancy and late-flowering phenotype, such as Kas-2, are predominantly winter-annuals with only one generation within a calendar year [54]. These different life-cycles of A. thaliana accessions depend on the level of seed dormancy, which can be attributed to the allelic status of the DELAY OF GERMINATION1 (DOG1) and DOG6 genes [51, 52, 54] and the duration to flower development, which is determined by FRIGIDA, FLOWERING LOCUS C and several other genes [54, 55]
Based on the sum of squares, the redundancy analysis indicated that 13% of variation in the insect community composition can be explained by the plant accessions and accession-by-site effects

Summary

Introduction

Genetic variation in plants alters insect abundance and community structure in the field; 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. A growing number of studies on community genetics has revealed that genetic variation in plant resistance traits exerts cascading effects on insect abundance and community composition [2,3,4,5]. These insect indices projected on individual plants, called extended phenotype [5], can be explained by variation among plant genotypes [6,7,8]. Knowledge remains limited about (i) how many insect species occupy A. thaliana in the field, (ii) whether plant defense traits contribute to insect abundance and community composition and (iii) the host genes that are responsible for community members and overall community composition

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Conclusion