Novel Genes Affecting the Interaction between the Cabbage Whitefly and Arabidopsis Uncovered by Genome-Wide Association Mapping

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.

Coherent synthesis of genomic associations with phenotypes and home environments

“…Note that our study, like that of Fournier- Level et al (2011a) is based on association mapping, which may suffer from identification of more false positives compared with linkage mapping approaches (Hall et al 2010;Anderson et al 2013;Ågren et al 2013). Followup experimental study of phenotypic effects of variation at individual loci is required to 610 confirm the results of association mapping (Verslues et al 2014;Broekgaarden et al 2015). The SNPs that exhibited the strongest evidence for SNP×climate interaction effects on fitness often fell within the coding regions of strong candidate genes based on known roles in environmental responses, suggesting our approach is a useful for identifying loci underlying local adaptation.…”

Genome‐wide association study reveals novel players in defense hormone crosstalk in Arabidopsis

“…GWA mapping is a method initially utilized in human population studies to identify the genetic basis of complex traits (Hirschhorn & Daly, 2005). GWA mapping has also been successfully utilized in plant studies (Aranzana et al, 2005;Atwell et al, 2010;Bac-Molenaar et al, 2015;Broekgaarden et al, 2015;Chan, Rowe, & Kliebenstein, 2010;Kloth, Thoen, Bouwmeester, Jongsma, & Dicke, 2012;Li, Huang, Bergelson, Nordborg, & Borevitz, 2010;Thoen et al, 2017;Wintermans, Bakker, & Pieterse, 2016). The underlying rationale of GWA mapping is that natural variation in the phenotype of a given trait is caused by genetic differences in the population under study.…”

Genetic variants affecting plant size and chemical defenses jointly shape herbivory inArabidopsis

“…In controlled experiments where herbivores are placed directly onto individual plants, genetic differences among plants typically explain a substantial proportion of variation in herbivory (e.g., 23 ). If these genotypic effects are masked by stochasticity intrinsic to herbivore foraging decisions, experiments in which herbivores are allowed to forage may lack power to identify loci underlying variation in herbivory unless they employ extremely large sample sizes.…”

“…Many experiments place herbivores directly onto different plant genotypes or simulate herbivory (e.g., [23][24][25][26][27] , but see 28,29 ). This approach yields precise measurements of plant resistance and herbivore performance phenotypes 10 and has enabled the discovery of novel loci shaping plantherbivore interactions using genetic mapping techniques (e.g., [23][24][25][26][27] ), but does so at the cost of minimizing the importance of whether a plant genotype will be encountered and attacked by a foraging herbivore. Consequently, the known catalog of genetic polymorphisms mediating plant-herbivore interactions is likely biased toward polymorphisms involved in resisting herbivory, such as those affecting physical and chemical defensive traits, while polymorphisms that mediate herbivore foraging behavior are likely underrepresented.The fact that herbivore choice is often restricted in genetic mapping studies in the lab, whereas herbivores can move more freely in trait-based studies conducted in the field, may contribute to current uncertainty 8 regarding which plant traits are the primary determinants of herbivory.…”

“…In practice, however, the design of assays used to measure herbivory phenotypes often introduces bias by excluding the effects of herbivore foraging behavior. Many experiments place herbivores directly onto different plant genotypes or simulate herbivory (e.g., [23][24][25][26][27] , but see 28,29 ). This approach yields precise measurements of plant resistance and herbivore performance phenotypes 10 and has enabled the discovery of novel loci shaping plantherbivore interactions using genetic mapping techniques (e.g., [23][24][25][26][27] ), but does so at the cost of minimizing the importance of whether a plant genotype will be encountered and attacked by a foraging herbivore.…”