Genome-wide association study reveals WRKY42 as a novel plant transcription factor that influences oviposition preference of Pieris butterflies

Insect herbivores are amongst the most destructive plant pests, damaging both naturally occurring and domesticated plants. As sessile organisms, plants make use of structural and chemical barriers to counteract herbivores. However, over 75% of herbivorous insect species are well adapted to their host's defenses and these specialists are generally difficult to ward off. By actively antagonizing the number of insect eggs deposited on plants, future damage by the herbivore's offspring can be limited. Therefore, it is important to understand which plant traits influence attractiveness for oviposition, especially for specialist insects that are well adapted to their host plants. In this study, we investigated the oviposition preference of Pieris butterflies (Lepidoptera: Pieridae) by offering them the choice between 350 different naturally occurring Arabidopsis accessions. Using a genome-wide association study of the oviposition data and subsequent fine mapping with full genome sequences of 164 accessions, we identified WRKY42 and AOC1 as candidate genes that are associated with the oviposition preference observed for Pieris butterflies. Host plant choice assays with Arabidopsis genotypes impaired in WRKY42 or AOC1 function confirmed a clear role for WRKY42 in oviposition preference of female Pieris butterflies, while for AOC1 the effect was mild. In contrast, WRKY42-impaired plants, which were preferred for oviposition by butterflies, negatively impacted offspring performance. These findings exemplify that plant genotype can have opposite effects on oviposition preference and caterpillar performance. This knowledge can be used for breeding trap crops or crops that are unattractive for oviposition by pest insects. Pierisbutterfly preference for oviposition on naturally occurring and genetically diverse Arabidopsis accessions is associated with WRKY42impairment and negatively impacts caterpillar performance.

Automated summary

Insect herbivores, especially specialist species, are difficult to ward off due to their adaptation to host plant defenses. This study identified WRKY42 and AOC1 as candidate genes associated with the oviposition preference in Pieris butterflies. Impairment in WRKY42 influenced the preference for oviposition, while AOC1 had a mild effect. However, the preference for impaired plants negatively impacted caterpillar performance. This knowledge can be applied in breeding strategies to develop trap crops or unattractive crops for pest insects.