Abstract

Plants have evolved a variety of ways to defend themselves against biotic attackers. This has resulted in the presence of substantial variation in defense mechanisms among plants, even within a species. Genome-wide association (GWA) mapping is a useful tool to study the genetic architecture of traits, but has so far only had limited exploitation in studies of plant defense. Here, we study the genetic architecture of defense against the phloem-feeding insect cabbage whitefly (Aleyrodes proletella) in Arabidopsis thaliana. We determined whitefly performance, i.e. the survival and reproduction of whitefly females, on 360 worldwide selected natural accessions and subsequently performed GWA mapping using 214,051 SNPs. Substantial variation for whitefly adult survival and oviposition rate (number of eggs laid per female per day) was observed between the accessions. We identified 39 candidate SNPs for either whitefly adult survival or oviposition rate, all with relatively small effects, underpinning the complex architecture of defense traits. Among the corresponding candidate genes, i.e. genes in linkage disequilibrium (LD) with candidate SNPs, none have previously been identified as a gene playing a role in the interaction between plants and phloem-feeding insects. Whitefly performance on knock-out mutants of a number of candidate genes was significantly affected, validating the potential of GWA mapping for novel gene discovery in plant-insect interactions. Our results show that GWA analysis is a very useful tool to gain insight into the genetic architecture of plant defense against herbivorous insects, i.e. we identified and validated several genes affecting whitefly performance that have not previously been related to plant defense against herbivorous insects.

Highlights

  • In nature, plants are constantly exposed to a wide range of herbivorous insects that can severely affect their growth and reproduction

  • To detect variation for direct defense against A. proletella, whitefly adult survival and oviposition rate were monitored using a no-choice assay on 360 accessions of A. thaliana grown under controlled conditions

  • These data suggest that certain traits can affect oviposition rate without influencing adult survival, a phenomenon that has previously been shown for the silverleaf whitefly Bemisia tabaci on wild tomato plants [41]

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Summary

Introduction

Plants are constantly exposed to a wide range of herbivorous insects that can severely affect their growth and reproduction. Certain traits that plants have evolved to counteract herbivore attack are involved in direct defense, i.e. physical and/or chemical barriers that negatively affect the performance of the attacker [6]. Physical barriers, such as trichomes, hinder or prevent insects from moving or feeding on a plant whereas toxic or antifeedant compounds form a chemical barrier to herbivores. These traits can alter the physiology of herbivorous insects resulting in reduced growth rate, adult size, survival probability and reproduction success [7]

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