Cocoa Apoplastic Washing Fluid Remodels the Proteomic Profile of the Saprophytic Mycelium of Moniliophthora perniciosa, the Causal Agent of Witches’ Broom Disease

Witches’ broom disease (WBD), caused by the fungus Moniliophthora perniciosa, poses a major threat to cocoa production and little is yet known about how the fungus adapts at the molecular level, particularly in the apoplastic environment during early infection. Here, we investigated how apoplastic washing fluid (AWF) from two cocoa genotypes with contrasting resistance to WBD modulates the mycelial protein profile of two M. perniciosa isolates: (i) Mp553—low infection level; and (ii) Mp565—high infection level. A total of 1272 proteins were identified. Mp565, showed increased accumulation of proteins associated with oxidative stress response, energy metabolism, and virulence when exposed to AWF from the resistant variety TSH1188. Key proteins such as phosphoglycerate kinase, enolase, and heat shock were significantly modulated. Interestingly, AWF from the resistant variety promoted the suppression of metabolic proteins, suggesting an effective defense response in the resistant genotype. Furthermore, interaction network analysis revealed the central role of the MPER₁1800 protein, a potential regulator of fungal adaptation. The findings underscore the importance of the T. cacao apoplast in both plant defense and fungal adaptation. The study also reveals key molecular targets, such as MPER₁1800, for potential strategies to control WBD. These insights enhance our understanding of M. perniciosa pathogenicity and offer valuable directions for developing novel interventions to mitigate the impact of this devastating disease.