The histone deacetylase Cfhos2 is a key epigenetic factor regulating appressorium development and pathogenesis in apple Glomerella leaf spot fungus Colletotrichum fructicola

Abstract

Glomerella leaf spot (GLS) is a devastating fungal disease that damages the leaves and fruits and reduces tree vigor of apple (Malus domestica). The pathogen infection mechanism, however, remains elusive. Histone-modifying enzymes, which regulate eukaryotic chromatin conformation and gene expression, are key epigenetic factors controlling fungal development, virulence, and secondary metabolism. To dissect the epigenetic regulation of GLS pathogenesis, we characterized a histone deacetylase gene Cfhos2 in Colletotrichum fructicola, the causing agent of GLS. Cfhos2 deletion mutants were mildly reduced in vegetative growth rate, but almost lost pathogenicity on apple leaves. Cfhos2 deletion mutants induced strong plant defense responses manifested by epidermal cell browning, granulation, and distortion of pathogen invasive hyphae. The mutants also showed defect in appressorial development on cellophane, but not on parafilm or on apple leaf surface, suggesting that the defect in appressorial development is surface-dependent. RNA-seq based transcriptome analysis highlighted that Cfhos2 regulates secondary metabolism-related virulence genes during infection. Moreover, the expression of an apple defense-related F-box protein was strongly induced by infection with Cfhos2 deletion mutants. Taken together, we demonstrate that Cfhos2 is a key epigenetic factor regulating appressorium development, virulence gene expression, and GLS pathogenesis in C. fructicola. The results provide important information for understanding the virulence mechanisms of C. fructicola.