Combined transcriptomics and metabolomics reveals the molecular mechanism by which rice responds to Ustilaginoidea virens infection.

Abstract

Rice false smut caused by Ustilaginoidea virens is a major fungal disease of rice in rice-growing regions throughout the world. However, the key genes and key metabolites related to U. virens resistance in rice remain unclear. Here, we used transcriptomics and metabolomics to determine the gene expression and metabolite accumulation changes in rice at 5, 7, and 9 d after inoculation with U. virens. By comparing the transcriptomes of IR27 (resistant cultivar) and 9311 (susceptible cultivar) spikelets, variable transcriptional responses under control and infection conditions were revealed. In total, 11,235 and 13,453 differentially expressed genes (DEGs) were identified in IR27 and 9311, respectively. The results of Kyoto Encyclopedia of Genes and Genomes and co‑expression analyses showed that the DEGs involved in flavonoid biosynthesis, phenylpropanoid biosynthesis, and plant hormone signal transduction responded to disease resistance. Several WRKY transcription factors were also differentially regulated in the resistant and susceptible cultivars. The metabolome analysis identified 343 and 303 differentially accumulated metabolites in IR27 and 9311, respectively, including salicylic acid, jasmonic acid, gibberellin, d-pantothenic acid, and p-coumaric acid. Many of these are primarily involved in plant hormone signal transduction, phenylpropanoid biosynthesis, and flavonoid biosynthesis pathways. Furthermore, the combined transcriptome and metabolome analysis revealed that plant hormone signal transduction, phenylpropanoid biosynthesis, and flavonoid biosynthesis were significantly enriched in resistant rice varieties. Therefore, these results provide valuable information on the molecular mechanisms by which rice defends against U. virens infection, and they will facilitate the development of disease‑resistant rice cultivars.