Integrated miRNA and mRNA expression profiling reveals the response regulators of a susceptible tomato cultivar to early blight disease

Early blight, caused by the fungus Alternaria solani, is a devastating foliar disease of tomatoes, causes massive yield loss each year worldwide. Molecular basis of the compatible host-pathogen interaction was elusive. We adopted next generation sequencing approach to decipher miRNAs and mRNAs that are differentially expressed during Alternaria-stress in tomato. Some of the interesting findings were also validated by alternative techniques. Our analysis revealed 181 known-miRNAs, belonging to 121 miRNA families, of which 67 miRNAs showed at least 2-fold change in expression level with the majority being downregulated. Concomitantly, 5,450 mRNAs were significantly regulated in the same diseased tissues. Differentially expressed genes were most significantly associated with response to stimulus process, photosynthesis, biosynthesis of secondary metabolites, plant-pathogen interaction and plant hormone signal transduction pathways. GO term enrichment-based categorization of gene-functions further supported this observation, as terms related to pathogen perception, disease signal transduction, cellular metabolic processes including oxidoreductase and kinase activity were over represented. In addition, we have discovered 102 miRNA-mRNA pairs which were regulated antagonistically, and careful study of the targeted mRNAs depicted that multiple transcription factors, nucleotide-binding site leucine-rich repeats, receptor-like proteins and enzymes related to cellular ROS management were profoundly affected. These studies have identified key regulators of Alternaria-stress response in tomato and the subset of genes that are likely to be post-transcriptionally silenced during the infection.