Dynamic changes in pod and fungal physiology associated with the shift from biotrophy to necrotrophy during the infection of Theobroma cacao by Moniliophthora roreri

Theobroma cacao pods were inoculated with meiospores of Moniliophthora roreri (Mr), a hemibiotrophic basidiomycete causing frosty pod rot. Pods were malformed 30 days after inoculation (DAI) and sporulation was observed 60 DAI. Glucose and asparagine concentrations decreased and mannitol and malonate increased in infected pods 30 DAI. By 60 DAI, most carbohydrates, amino acids, and organic acids were drastically reduced by infection. Mannitol and succinic acid levels increased 60 DAI and likely originated from Mr. RT-qPCR analysis of cacao ESTs indicated a strong response to infection 30 DAI in malformed pod. Evidence indicated that biotrophic hyphae colonized pods and a shift to necrotrophic growth occurred later (during the end stages of infection). Expression of cacao ESTs associated with plant hormone biosynthesis and action was altered. Changes in the expression of Mr ESTs in response to nutrient deficiency in pure culture were small. Changes in Mr gene expression patterns and levels of specific metabolites in necrotic sporulating pods 60 DAI compared to malformed pods 30 DAI indicated that the glyoxylate cycle of Mr was up regulated during the shift from biotrophic to necrotrophic phases of the disease cycle.

Figure optionsDownload as PowerPoint slideHighlights
► M. roreri biotrophic mycelia are thick and convoluted in malformed green pods.
► M. roreri biotrophy reduces the concentrations of glucose and asparagine in pods.
► Large changes in cacao gene expression occur late in the biotrophic phase of disease.
► M. roreri gene expression is altered by the shift from biotrophy to necrotrophy.
► M. roreri genes associated with the glyoxylate cycle are induced during necrotrophy.