ORIGINAL PAPER The interaction of Theobroma cacao and Moniliophthora perniciosa, the causal agent of witches’ broom disease, during parthenocarpy Rachel L. Melnick & Jean-Philippe Marelli & Richard C. Sicher & Mary D. Strem & Bryan A. Bailey Received: 26 October 2011 / Revised: 13 April 2012 / Accepted: 19 April 2012 / Published online: 15 May 2012 # Springer-Verlag (outside the USA) 2012 Abstract Witches’ broom disease of Theobroma cacao L. is caused by the hemibiotrophic basidiomycete Monilioph- thora perniciosa. Infection of flower cushions by M. perni- ciosa results in parthenocarpy. Healthy and parthenocarpic immature cacao pods were obtained from seven cacao clones. Microscopic observations of parthenocarpic pods from two clones confirmed that fruits lack viable seed. Septate mycelia colonized parthenocarpic pods, but were absent from healthy pods. Parthenocarpic pods had in- creased concentrations of leucine, methionine, serine, phe- nylalanine, and valine. Major transport metabolites sucrose and asparagine were decreased by 63 and 40 %, respective- ly, during parthenocarpy. M. perniciosa expressed sequence tags (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 biosyn- thesis were repressed ( MpGAox , MpCPS , MpDES , MpGGPPS, and MpCAO) in parthenocarpic pods. RT- 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 (TcGA20OX1B) were repressed in parthenocarpic pods. Ca- cao ESTs putatively related to maintaining cytokinin (TcCKX3 and TcCKX5) and IAA (TcGH3.17a, TcGH3.1, TcARF18) homeostasis were induced in parthenocarpic pods, suggesting an attempt to regulate cytokinin and auxin concentrations. In conclusion, M. perniciosa expresses spe- cific sets of transcripts targeting nutrient acquisition and survival while altering the host physiology without causing significant necrosis resulting in parthenocarpy. Only a gen- eral host defense response is elicited. Keywords Parthenocarpy . Cacao . Moniliophthora perniciosa . Witches’ broom . Plant–microbe interaction Introduction Theobroma cacao L. is an understory tropical tree with seeds that are processed into cocoa products. Throughout Central and South America, cacao production has been severely limited by fungal diseases (Hebbar 2007). Witches’ broom, caused by the hemibiotrophic agaric basidiomycete Moniliophthora perniciosa (Aime and Phillips-Mora 2005), occurs in all major cacao-producing areas in South America (Meinhardt et al. 2008). Introduction of witches’ broom to Bahia, Brazil caused the country to fall from the third largest cocoa producer in the world to having to import beans for production (Meinhardt et al. 2008). In Latin America, most cacao is produced on family farms of about 20–30 ha Communicated by R. Sederoff Electronic supplementary material The online version of this article (doi:10.1007/s11295-012-0513-8) contains supplementary material, which is available to authorized users. R. L. Melnick (*) : M. D. Strem : B. A. Bailey USDA-ARS Sustainable Perennial Crops Lab, BARC-WEST, BLDG 001, Beltsville, MD 20705, USA e-mail: rachel.melnick@ars.usda.gov J.-P. Marelli Mars Center for Cocoa Science, Fazenda Almirante, CP 55, Itajuipe, Bahia 4630-000, Brazil R. C. Sicher USDA-ARS Crop Systems & Global Change Lab, Beltsville, MD 20705, USA Tree Genetics & Genomes (2012) 8:1261–1279 DOI 10.1007/s11295-012-0513-8