The response of rhubarb to smut infection is revealed through a comparative transcriptome and metabolome study.

ABSTRACT

MAIN CONCLUSION: Integrated transcriptome and metabolome analysis have unveiled the physiological and molecular responses of rhubarb to infection by smut fungi. Rhubarb is an important medicinal plant that is easily infected by smut fungi during its growth. Thus far, no research on the influence of smut fungi on the growth of rhubarb and its secondary metabolism has been conducted. In this study, petioles of Chinese rhubarb (Rheum officinale) [healthy or infected with smut fungus (Thecaphora schwarzmaniana)] were characterized. Microscopic structure, global gene expression profiling, global metabolic profiling, and key enzyme activity and metabolite levels in infected plants were analyzed. Infection by smut fungi resulted in numerous holes inside the petiole tissue and led to visible tumors on the external surface of the petiole. Through metabolic changes, T. schwarzmaniana induced the production of specific sugars, lipids, and amino acids, and inhibited the metabolism of phenolics and flavonoids in R. officinale. The concentrations of key medicinal compounds (anthraquinones) were decreased because of smut fungus infection. In terms of gene expression, the presence of T. schwarzmaniana led to upregulation of the genes associated with nutrient (sugar, amino acid, etc.) transport and metabolism. The gene expression profiling showed a stimulated cell division activity (the basis of tumor formation). Although plant antioxidative response was enhanced, the plant defense response against pathogen was suppressed by T. schwarzmaniana, as indicated by the expression profiling of genes involved in biotic and abiotic stress-related hormone signaling and the synthesis of plant disease resistance proteins. This study demonstrated physiological and molecular changes in R. officinale under T. schwarzmaniana infection, reflecting the survival tactics employed by smut fungus for parasitizing rhubarb.