Global mRNA and microRNA expression dynamics in response to anthracnose infection in sorghum

BACKGROUND: Anthracnose is a damaging disease of sorghum caused by the fungal pathogen Colletotrichum sublineolum. Genome-wide mRNA and microRNA (miRNA) profiles of resistant and susceptible sorghum genotypes were studied to understand components of immune responses, and fungal induced miRNA and target gene networks. RESULTS: A total of 18 mRNA and 12 miRNA libraries from resistant and susceptible sorghum lines were sequenced prior to and after inoculation with C. sublineolum. Significant differences in transcriptomes of the susceptible and resistant genotypes were observed with dispersion distance and hierarchical cluster tree analyses. Of the total 33,032 genes predicted in the sorghum genome, 19,593 were induced by C. sublineolum, and 15,512 were differentially expressed (DEGs) between the two genotypes. The resistant line was marked by significant reprogramming of the transcriptome at 24 h post inoculation (hpi), and a decrease at 48 hpi, whereas the susceptible line displayed continued changes in gene expression concordant with elevated fungal growth in the susceptible genotype. DEGs encode proteins implicated in diverse functions including photosynthesis, synthesis of tetrapyrrole, carbohydrate and secondary metabolism, immune signaling, and chitin binding. Genes encoding immune receptors, MAPKs, pentatricopeptide repeat proteins, and WRKY transcription factors were induced in the resistant genotype. In a parallel miRNA profiling, the susceptible line displayed greater number of differentially expressed miRNAs than the resistant line indicative of a widespread suppression of gene expression. Interestingly, we found 75 miRNAs, including 36 novel miRNAs, which were differentially expressed in response to fungal inoculation. The expression of 50 miRNAs was significantly different between resistant and susceptible lines. Subsequently, for 35 differentially expressed miRNAs, the corresponding 149 target genes were identified. Expression of 56 target genes were significantly altered after inoculation, showing inverse expression with the corresponding miRNAs. CONCLUSIONS: We provide insights into genome wide dynamics of mRNA and miRNA profiles, biological and cellular processes underlying host responses to fungal infection in sorghum. Resistance is correlated with early transcriptional reprogramming of genes in various pathways. Fungal induced genes, miRNAs and their targets with a potential function in host responses to anthracnose were identified, opening avenues for genetic dissection of resistance mechanisms. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-020-07138-0.