Time-course dual RNA-seq analyses and gene identification during early stages of plant-Phytophthora infestans interactions

Abstract Late blight caused by Phytophthora infestans is a major threat to global potato and tomato production. Sustainable management of late blight requires the development of resistant crop cultivars. This process can be facilitated by high-throughput identification of functional genes involved in late blight pathogenesis. In this study, we generated a high-quality transcriptomic time-course dataset focusing on the initial 24 h of contact between P. infestans and 3 solanaceous plant species, tobacco (Nicotiana benthamiana), tomato (Solanum lycopersicum), and potato (Solanum tuberosum). Our results demonstrate species-specific transcriptional regulation in early stages of the infection. Transient silencing of putative RIBOSE-5-PHOSPHATE ISOMERASE and HMG-CoA REDUCTASE genes in N. benthamiana lowered plant resistance against P. infestans. Furthermore, heterologous expression of a putative tomato Golgi-localized nucleosugar transporter-encoding gene exacerbated P. infestans infection of N. benthamiana. In comparison, bioassays using transgenic tomato lines showed that the quantitative disease resistance genes were required but insufficient for late blight resistance; genetic knock-out of the susceptibility gene enhanced resistance. The same RNA-seq dataset was exploited to examine the transcriptional landscape of P. infestans and revealed host-specific gene expression patterns in the pathogen. This temporal transcriptomic diversity, in combination with genomic distribution features, identified the P. infestans IPI-B family GLYCINE-RICH PROTEINs as putative virulence factors that promoted disease severity or induced plant tissue necrosis when transiently expressed in N. benthamiana. These functional genes underline the effectiveness of functional gene-mining through a time-course dual RNA-seq approach and provide insight into the molecular interactions between solanaceous plants and P. infestans.