The Interplay of Theobroma cacao Genetics and Its Pod Mycobiome on Controlling Pathogenic Fungus Moniliophthora roreri

Abstract

The tropical tree crop Theobroma cacaohas many cultivars that differ genetically and show differences in resistance to disease. These cultivars also host diverse microbiomes, including endophytic fungi, with the capacity to protect the plant against diseases. Further research is needed to utilize these fungi effectively in biological control. This study aimed to (i) assess whether host genotypic differences affect the diversity and taxonomic composition of cacao fruit’s endophytic mycobiome, at one cacao producer locality in Panama; (ii) determine whether the biocontrol capacity of endophytic fungi against the cacao frosty pod pathogen, Moniliophthora rorer i, varies depending on host genotypes with contrasting levels of disease resistance; and (iii) evaluate endophytic fungi effects on the secondary chemistry profile of T. cacaopods. Internal transcribed spacer-based metabarcoding of the cacao pod fungal endophyte community associated with four host genotypes revealed 342 amplicon sequence variants representing 13 classes, 33 orders, 62 families, and 92 genera. Alpha diversity of the fungal endophyte community was influenced by host genotype. A field trial to evaluate the biocontrol efficacy of fungal endophytes Waltergamsia zeylanicaand Clonostachys roseaagainst M. roreriin two T. cacaogenotypes showed that C. rosea significantly reduced M. rorerisporulating lesions, and this effect was larger in the most susceptible genotype. Inoculation with both fungi downregulated specific metabolites in the fruit of cacao. This study shows that host genotype affects the composition of the cacao pod mycobiome and that the mycobiome can be manipulated to enhance disease resistance in what is normally considered a susceptible genotype.