ChCpc1, a bZIP transcription factor, coordinates amino acid synthesis and autophagy and modulates conidiation and virulence in Cochliobolus heterostrophus.

Cochliobolus heterostrophus, a fungal plant pathogen, is the causal agent of southern corn leaf blight. The bZIP transcription factor Cpc1 is required for response to oxidative stress and amino acid starvation in the saprobe, Neurospora crassa, and the human pathogen, Candida albicans. However, although conserved in fungal plant pathogens, Cpc1 function and regulatory mechanisms are still largely unknown. Through targeted gene deletion, we demonstrated that ChCPC1 was necessary for nitrogen assimilation and response to amino acid starvation during conidiation and the infection process. In addition, amino acid synthesis and autophagy induction were also impaired in ΔChcpc1 mutants. We found that ChCpc1 binds to the promoter region of ChARG1 and ChARG4 to activate arginine synthesis to counteract amino acid depletion. Amino acid deprivation induced autophagy in C. heterostrophus, and it depended on the direct activation of ChATG genes by ChCpc1, which confirmed the genetic relationship between ChCpc1 and ChATG genes. Additionally, we demonstrated that ChCpc1 forms a heterodimer with another bZIP transcription factor, ChAtf1, to enhance the binding of ChCpc1 to the promoter regions of ChARG4 and ChATG8. Furthermore, mitogen-activated protein kinase ChChk1 phosphorylated ChCpc1 to counteract amino acid depletion in C. heterostrophus, and the other two components of the MAPK pathway (ChSte7 and ChSte11) were also involved in the response to amino acid starvation stress, conidiation, and virulence in C. heterostrophus. This study confirmed that ChCpc1 coordinates amino acid synthesis and autophagy to modulate conidiation and virulence in C. heterostrophus.IMPORTANCESouthern corn leaf blight (SCLB) caused by Cochliobolus heterostrophus is a destructive disease that threatens global maize (Zea mays) production. The bZIP transcription factor Cpc1 is conserved in fungal plant pathogens; however, the biological function and the regulatory mechanism are still largely unknown. In this study, we characterized the function of ChCpc1 in C. heterostrophus, especially noting that ChCpc1 was found to be involved in response to amino acid starvation and autophagy. Additionally, we revealed that ChCpc1 directly targets arginine synthesis genes and autophagy-related genes to counteract amino acid depletion during the infection process of C. heterostrophus. Importantly, we found that another bZIP transcription factor, ChAtf1, and protein kinase ChChk1 were also important for responding to amino acid depletion functioning upstream of ChCpc1. The discoveries could broaden the understanding of how plant pathogenic fungi respond to nutrient stress to ensure successful infection.