Acaricide resistance mechanisms and host plant responses in the tomato specialist Aculops lycopersici.

Abstract

The mite Aculops lycopersici is a major tomato pest with extremely reduced gene families involved in chemoreception and detoxification. How this limited detoxification toolbox affects the evolution of resistance to acaricides in tomato russet mite(s) (TRM) remains enigmatic. Moreover, although a tomato specialist, TRM has been observed on other Solanaceae and Convolvulaceae plant species, raising questions about transcriptional plasticity underlying host exchange. We identified a field strain with strongly decreased susceptibility to both abamectin and spiromesifen. We detected target-site resistance caused by mutations at conserved positions in two glutamate-gated chloride channels (GluCl), as well as four overexpressed detoxification genes. We then examined transcriptional responses after host shift from tomato to two Solanaceae (potato and black nightshade) and two Convolvulaceae (sweet potato and hedge bindweed) species, as more challenging host plants. Transcriptional responses varied significantly between host plant families, with key differentially expressed genes (DEGs) related to proteolytic, metabolic and detoxification processes. Last, we also identified DEGs encoding for secreted proteins potentially involved in TRM-host plant interactions. Despite a limited detoxification toolbox, A. lycopersici might quickly evolve target-site resistance, probably facilitated by strong selection pressure on the genetic variation associated with enormous population size in field settings. Responses to host plant changes include plasticity in genes related to digestion and detoxification, while most responsive genes are of unknown function and remain to be investigated. © 2024 Society of Chemical Industry.