Maize plant infection by Ustilago maydis is regulated by the Fungal Sulfur Metabolism.

Abstract

The sulfur metabolism is tightly regulated in cells. Cysteine, at physiological concentrations, plays a crucial role in protein assembly, as well as in coenzyme and metabolic intermediate synthesis. Additionally, cysteine is biotransformed into H2S, a gasotransmitter with several roles on cells, ranging from regulating mitochondrial metabolism to producing metabolic intermediates and mediating post-translational modification of proteins. While H2S has been shown to participate in the infection processes of animal pathogenic fungi, its role in phytopathogenic fungi remains unexplored. Here, we describe the conditions required to induce endogenous production of H2S in plant pathogenic fungi Ustilago maydis. Under these conditions, we observed an increased infection rate and more pronounced symptoms in maize plants. A label-free proteomic assay to examine adaptations of U. maydis under H2S-producing conditions shown an increased expression of extracellular enzymes required for virulence and mitochondrial proteins related to cellular respiration, ATP synthesis, and fatty acid degradation, along with enhanced expression of proteins involved in proteasomal degradation. Conversely, we found reduced expression of proteins associated with antioxidant responses, glycolysis, and the pentose phosphate pathway. These mitochondrial protein alterations correlated with increased mitochondrial biogenesis, ultrastructural changes, inhibition of the cytochrome respiratory pathway, and elevated activity of an alternative oxidase. Additionally, H2O2 production increased, while the enzymatic capacity for its detoxification decreased. Impaired lipid accumulation and altered intracellular distribution were also observed. Thus, in U. maydis, the modulation of cysteine metabolism regulates mitochondrial function, protein expression, lipid metabolism and infectious processes. Author SummaryUstilago maydis is a basidiomycete fungus that infects corn plants, inducing tumor formation. While in some countries this infection causes significant losses in maize crops, in Mexico, U. maydis, known as "huitlacoche," is celebrated as a culinary delicacy with important nutritional value. Additionally, it serves as an interesting model for studying infection by dimorphic phytopathogenic fungi. Animal models of fungal pathogenesis show that hydrogen sulfide (H2S), whether exogenously provided or induced by supplementation with its precursor cysteine, plays a role in infection processes in both the pathogen and the host cell. In this study, we explored the role of cysteine in the morphology, metabolism, and pathogenicity of U. maydis. Our findings indicate that cysteine treatment triggers an overproduction of H2S, alters mitochondrial morphology and nitrogen metabolism, and disrupts the oxidative balance in U. maydis. Furthermore, fungi to cysteine enhance tumor formation and anthocyanins accumulation in Zea mays plants. These findings suggest that H2S may play a key role in the infection efficiency of phytopathogenic fungi.