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

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Abstract

Witches’ broom disease of Theobroma cacao L. is caused by the hemibiotrophic basidiomycete Moniliophthora perniciosa. Infection of flower cushions by M. perniciosa 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 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 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 biosynthesis 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. Cacao 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 specific sets of transcripts targeting nutrient acquisition and survival while altering the host physiology without causing significant necrosis resulting in parthenocarpy. Only a general host defense response is elicited.

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  1. USDA-ARS Sustainable Perennial Crops Lab, BARC-WEST, BLDG 001, Beltsville, MD, 20705, USA

    Rachel L. Melnick, Mary D. Strem & Bryan A. Bailey

  2. Mars Center for Cocoa Science, Fazenda Almirante, CP 55, Itajuipe, Bahia, 4630-000, Brazil

    Jean-Philippe Marelli

  3. USDA-ARS Crop Systems & Global Change Lab, Beltsville, MD, 20705, USA

    Richard C. Sicher

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  1. Rachel L. Melnick
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Melnick, R.L., Marelli, JP., Sicher, R.C. et al. The interaction of Theobroma cacao and Moniliophthora perniciosa, the causal agent of witches’ broom disease, during parthenocarpy. Tree Genetics & Genomes 8, 1261–1279 (2012). https://doi.org/10.1007/s11295-012-0513-8

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