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, 1780 and 3386 differentially expressed genes (DEGs) at pH 5, pH 7 and pH 9, when compared with the host pH (pH=3), and 2122 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.

The Rpd3 histone deacetylase complex is a multiple-subunit complex that mediates the regulation of chromatin accessibility and gene expression. Sin3, the largest subunit of Rpd3 complex, is conserved in a broad range of eukaryotes. Despite being a molecular scaffold for complex assembly, the functional sites and mechanism of action of Sin3 remain unexplored. In this study, we functionally characterized a glutamate residue (E810) in FgSin3, the ortholog of yeast Sin3 in Fusarium graminearum (known as wheat scab fungus). Our findings indicate that E810 was important for the functions of FgSin3 in regulating vegetative growth, sexual reproduction, wheat infection, and DON biosynthesis. Furthermore, the E810K missense mutation restored the reduced H4 acetylation caused by the deletion of FNG1, the ortholog of the human inhibitor of growth (ING1) gene in F. graminearum. Correspondingly, the defects of the fng1 mutant were also partially rescued by the E810K mutation in FgSin3. Sequence alignment and evolutionary analysis revealed that E810 residue is well-conserved in fungi, animals, and plants. Based on Alphafold2 structure modeling, E810 localized on the FgRpd3-FgSin3 interface for the formation of a hydrogen bond with FgRpd3. Mutation of E810 disrupts the hydrogen bond and likely affects the FgRpd3-FgSin3 interaction. Taken together, E810 of FgSin3 is functionally associated with Fng1 in the regulation of H4 acetylation and related biological processes, probably by affecting the assembly of the Rpd3 complex.