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Title: The interaction of Theobroma cacao and Moniliophthora perniciosa, the causal agent of witches’ broom disease, during parthenocarpy

item Melnick, Rachel
item MARELLI, JEAN-PHILIPPE - M & M Mars Company - Brazil
item Sicher Jr, Richard
item Strem, Mary
item Bailey, Bryan

Submitted to: Tree Genetics and Genomes
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/19/2011
Publication Date: 5/17/2012
Citation: Melnick, R.L., Marelli, J., Sicher, Jr., R.C., Strem, M.D., Bailey, B.A. 2012. The interaction of Theobroma cacao and Moniliophthora perniciosa, the causal agent of witches’ broom disease, during parthenocarpy. Tree Genetics and Genomes. DOI: 10.1007/s11295-012-0513-8.

Interpretive Summary: Cocoa is combined with United States agricultural commodities providing a direct benefit to the American farmer. Witches’ broom disease, caused by the fungus Moniliophthora perniciosa, causes large yield losses for cacao (Theobroma cacao L.), the source of cocoa. When the fungus infects cacao flowers, it causes fruit to develop without fertilization, leading to seedless fruit and no cocoa beans. These seedless fruit rot and produce spores that spread the disease. We used microscopy, the molecular tool of quantitative real time PCR, and metabolite analysis to characterize how the fungus causes fruit to develop without seeds. The fungus grows throughout the seedless fruit causing significant changes in sugar and amino acid content without inducing a strong resistance response that would limit disease. Our improved knowledge of witches’ broom disease may lead to the development of new management tools for use by cacao farmers. It will provide cacao breeders with genetic markers to use during selection of resistant trees. By reducing the negative impact of disease on cacao yield, cocoa supplies may be stabilized resulting in increased benefits to the cocoa industry, and the American farmer.

Technical Abstract: Infection of Theobroma cacao L. flower cushions by Moniliophthora perniciosa induces parthenocarpy. Healthy and parthenocarpic immature cacao pods were obtained from seven cacao clones. Microscopic observations of parthenocarpic pods confirmed fruits lack viable seed. Septate mycelium colonized parthenocarpic pods, but were absent from healthy pods. Parthenocarpic pods had increased concentrations of leucine, methionine, serine, phenylalanine, and valine. Major transport metabolites sucrose and asparagine were decreased by 63% and 40%, respectively, during parthenocarpy. M. perniciosa ESTs related to detoxification (MpSOD2 and MpCTA1) and nutrient acquisition (MpAS, MpAK, MpATG8, MpPLY, and MpPME) were induced in parthenocarpic pods. Most M. perniciosa ESTs related to plant hormone biosynthesis were repressed (MpGAox, MpCPS, MpDES, MpGGPPS, and MpCAO) during parthenocarpy at the stage studied. QPCR analysis was conducted for 54 defense related cacao ESTs and 93 hormone related cacao ESTs. Specific cacao ESTs related to plant defense were induced (TcPR5, TcChi4, TcThau-ICS) while others were repressed (TcPR1, TcPR6, TcP12, and TcChiB). Cacao ESTs related to GA biosynthesis (TcGA20OX1, TcGA20OX1B, and TcGA20OX3a) were repressed in parthenocarpic pods. Cacao ESTs putatively related to cytokinin (TcCKX3 and TcCKX5) and IAA (TcGH3.6, TcGH3.17b, TcGH3.1, TcARF18) homeostasis were induced in parthenocarpic pods, suggesting an attempt to regulate cytokinin and auxin concentrations.