Acidic environment favors the development and pathogenicity of the grape white rot fungus Coniella vitis

Grape white rot caused by Coniella vitis is a global concern in the grape industry. pH regulation is essential for cell growth, reproductive processes and pathogenicity in phytopathogenic fungi. In this study, we observed that the growth rate, spore production and virulence of C. vitis significantly declined in alkaline pH, as well as the suppressive effect on secretion of hydrolytic enzymes. Transcriptomic and metabolomic analyses were used to investigate the responses of C. vitis to acidic (pH 5), neutral (pH 7) and alkaline environments (pH 9). We identified 728, 1,780 and 3,386 differentially expressed genes (DEGs) at pH 5, pH 7 and pH 9, when compared with the host pH (pH 3), and 2,122 differently expressed metabolites (DEMs) in negative and positive ion mode. Most DEGs were involved in carbohydrate metabolic process, transmembrane transport, tricarboxylic acid cycle, peptide metabolic process, amide biosynthetic process, and organic acid metabolic process. In addition, metabolomic analysis revealed ABC transporters, indole alkaloid biosynthesis, diterpenoid biosynthesis, and carotenoid biosynthesis pathways in response to the pH change. Furthermore, we found that the aspartate synthesis metabolic route associated with the TCA cycle is a key limiting factor for the growth and development of C. vitis in alkaline environments, and aspartate supplementation enables C. vitis to grow in alkaline environments. Plant cell wall-degrading enzymes (PCWDEs) could contribute to the pathogenicity, when C. vitis infected at pH 3. Importantly, aflatrem biosynthesis in acidic environment might contribute to the virulence of C. vitis and has a risk of causing human health problems due to its acute neurotoxic effects.