The role of plant susceptibility genes in mite-plant interactions

Spider mites are a pest on many important crops. They make their host plants more susceptible via secretion of salivary proteins that interact with plant proteins thereby reprogramming the host’s metabolism. In the first chapter of this thesis, I describe the identification of genes that render plants more susceptible to spider mites. We identified the spider mite salivary protein SHOT2b as interactor of a plant kinase protein called MLK4. MLK4 belongs to a family of four kinases, that regulate light signalling and metabolite accumulation, among others. Upon infestation of spider mites, the expression of MLK4 is upregulated. Absence of this particular MLK gene is detrimental to spider mites, as we observed that the reproductive performance of spider mites decreases by almost 50% on MLK4 knock-out mutant plants. Therefore, we deemed MLK4 a so-called Susceptibility gene (S-gene), since its expression makes the plant more susceptible to spider mites. In the second chapter of this thesis, we explore the transcriptomic, proteomic, and phosphoproteomic signatures of the MLK4-mediated susceptibility. We established that spider mites upregulate accumulation of transcripts and proteins involved in glucosinolate regulation. Glucosinolates are a family of toxins that protect the plant against herbivores and some pathogens. In the third chapter of this thesis, we measured the mite-induced accumulation of glucosinolates in Arabidopsis plants, and concluded that MLK4 expression negatively correlates with glucosinolate accumulation. Infested mutant plants that lacked the MLK4 gene accumulated more glucosinolates than infested wild type plants and were less susceptible to these mites. The data also suggest that SHOT2b enhances or attenuates the effect of MLK4 as negative regulator of glucosinolates. Therefore, I conclude that spider mites secrete the protein SHOT2b via their saliva into plants to reduce glucosinolate accumulation by hijacking a glucosinolate regulator, thus increasing the plant’s susceptibility and suitability as a spider mite host.