Histone Acetyltransferase CfGcn5-Mediated Autophagy Governs the Pathogenicity of Colletotrichum fructicola

Camellia oleifera is a woody edible-oil plant in China, and anthracnose occurs wherever it is grown, causing serious losses each year. We previously identified that the histone acetyltransferase CfGcn5 orchestrates growth, development, and pathogenicity in Colletotrichum fructicola, the major causal agent of anthracnose on C. oleifera. To elucidate the underlying mechanism, we conducted a transcriptome analysis and found that CfGcn5 is mainly involved in ribosomes, catalytic and metabolic processes, primary metabolism, and autophagy. In addition, we provided evidence showing that CfGcn5 serves as an autophagy repressor to mediate the expression of many autophagy-related genes (ATG) and undergoes degradation during autophagy. Moreover, we found that the CfATG8 and CfATG9 gene-deletion mutants had defects in mitosis and autophagy, resulting in their decreased appressoria formation rates and lower turgor pressure. These combined effects caused the failure of their appressoria functions and caused defects on their pathogenicity, revealing the importance of autophagy in pathogenicity. Taken together, our study illustrates that the autophagy repressor CfGcn5 undergoes degradation in order to regulate autophagy-dependent pathogenicity in C. fructicola. IMPORTANCE Colletotrichum spp. is ranked in the top 10 plant fungal pathogens and serves as a model for the study of hemibiotrophic pathogens, but its molecular mechanisms of pathogenesis remain largely unknown. Among species of Colletotrichum, C. fructicola causes anthracnose disease on more than 50 plants, such as pears, apples, and the important, edible-oil plant Camellia oleifera. We previously identified that the histone acetyltransferase CfGcn5 regulates growth, development, and pathogenicity in C. fructicola. To explore the underlying mechanisms, we performed comparative transcriptomic studies and found that CfGcn5 regulates global gene expression, including multiple autophagy-related genes (ATG genes). We revealed that CfGcn5 is an autophagy repressor that undergoes degradation during autophagy to govern pathogenicity. We also showed that the autophagy-related proteins CfAtg8 and CfAtg9 are required for full pathogenicity due to their regulatory functions in mitosis and autophagy. Our findings are important because we provide the first comprehensive characterization of autophagy as well as the relationship between acetylation and autophagy functioning in the pathogenesis of Colletotrichum spp., which might offer new potential targets for the management of anthracnose disease.