Resistance to Botrytis cinerea in Solanum lycopersicoides involves widespread transcriptional reprogramming

Tomato (Solanum lycopersicum), one of the world's most important vegetable crops, is highly susceptible to necrotrophic fungal pathogens such as Botrytis cinerea and Alternaria solani. Improving resistance through conventional breeding has been hampered by a shortage of resistant germplasm and difficulties in introgressing resistance into elite germplasm without linkage drag. The goal of this study was to explore natural variation among wild Solanum species to identify new sources of resistance to necrotrophic fungi and dissect mechanisms underlying resistance against B. cinerea.

Among eight wild species evaluated for resistance against B. cinerea and A. solani, S. lycopersicoides expressed the highest levels of resistance against both pathogens. Resistance against B. cinerea manifested as containment of pathogen growth. Through next-generation RNA sequencing and de novo assembly of the S. lycopersicoides transcriptome, changes in gene expression were analyzed during pathogen infection. In response to B. cinerea, differentially expressed transcripts grouped into four categories: genes whose expression rapidly increased then rapidly decreased, genes whose expression rapidly increased and plateaued, genes whose expression continually increased, and genes with decreased expression. Homology-based searches also identified a limited number of highly expressed B. cinerea genes. Almost immediately after infection by B. cinerea, S. lycopersicoides suppressed photosynthesis and metabolic processes involved in growth, energy generation, and response to stimuli, and simultaneously induced various defense-related genes, including pathogenesis-related protein 1 (PR1), a beta-1,3-glucanase (glucanase), and a subtilisin-like protease, indicating a shift in priority towards defense. Moreover, cluster analysis revealed novel, uncharacterized genes that may play roles in defense against necrotrophic fungal pathogens in S. lycopersicoides. The expression of orthologous defense-related genes in S. lycopersicum after infection with B. cinerea revealed differences in the onset and intensity of induction, thus illuminating a potential mechanism explaining the increased susceptibility. Additionally, metabolic pathway analyses identified putative defense-related categories of secondary metabolites.

In sum, this study provided insight into resistance against necrotrophic fungal pathogens in the Solanaceae, as well as novel sequence resources for S. lycopersicoides.