Abstract
Witches’ broom is a severe disease of Theobroma cacao L. (cacao), caused by the basidiomycete Moniliophthora perniciosa. The use of resistant cultivars is the ultimate method of control, but there are limited sources of resistance. Further, resistance from the most widely used source (‘Scavina 6’) has been overcome after a few years of deployment. New sources of resistance have been intensively searched for in the Amazon basin. Here, we evaluated for witches’ broom resistance, cacao accessions from various natural cacao populations originally collected in the Brazilian Amazon. Resistance of 43 families was evaluated under nursery and/or field conditions by artificial or natural infection, respectively, based on disease incidence. Screening for resistance by artificial inoculation under nursery conditions appeared to be efficient in identifying these novel resistance sources, confirmed by natural field evaluation over a nine-year period. The increase in natural field infection of ‘Scavina 6’ was clearly demonstrated. Among the evaluated families with the least witches’ broom incidence, there were accessions originally collected from distinct river basins, including the Jamari river (‘CAB 0371’; ‘CAB 0388’; ‘CAB 0392’; and ‘CAB 0410’); Acre (‘CAB 0169’); Javari (‘CAB 0352’); Solimões (‘CAB 0270’); and from the Purus river basin, the two most outstanding resistant accessions, ‘CAB 0208’ and ‘CAB 0214’. The large genetic diversity found in cacao populations occurring at river basins from Acre and Amazonas states, Brazil, increased the chance that the selected resistant accessions would be genetically more dissimilar, and represent distinct sources of resistance to M. perniciosa from ‘Scavina 6’.
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References
Aime MC, Phillips-Mora W (2005) The causal agent of witches’ broom and frosty pod rot of cocoa (chocolate, Theobroma cacao) form a new lineage of Marasmiaceae. Mycologia 97:1012–1022. doi:10.3852/mycologia.97.5.1012
Almeida CMVC, Machado PFR, Barriga JP, Silva FCO (1995) Coleta de cacau (Theobroma cacao L.) da Amazônia brasileira: uma abordagem histórica e analítica. Belém, Para, Brazil: Ministério de Agricultura e Reforma Agrária: Comissão Executiva do Plano da Lavoura Cacaueira, Boletim Técnico, 92 pp
Andebrhan T, Figueira A, Yamada MM, Furtek DB (1999) Molecular fingerprinting suggests two primary outbreaks of witches’ broom disease (Crinipellis perniciosa) of Theobroma cacao in Bahia, Brazil. Eur J Plant Pathol 105:167–175. doi:10.1023/A:1008716000479
Bartley BGD (1986) Cacao, Theobroma cacao. FAO Plant Production and Protection Paper 70, pp 25–42
Bartley BGD (2005) The genetic diversity of cacao and its utilization. CABI Publishing, Wallingford
Bowers JH, Bailey BA, Hebbar PK, Sanogo S, Lumsden RD (2001) The impact of plant diseases on world chocolate production. Plant Health Prog. doi:10.1094/PHP-2001-0709-01-RV
Brown JS, Schnell RJ, Motamayor JC, Lopes U, Kuhn DN, Borrone JW (2005) Resistance gene mapping for witches’ broom disease in Theobroma cacao L. in an F2 population using SSR markers and candidate genes. J Am Soc Hortic Sci 130:366–373
Dobson AJ (2002) An introduction to generalized linear models, 2nd edn. Chapman & Hall/CRC, London
Engelbrecht CJ, Harrigton TC, Alfenas A, Suarez C (2007) Genetic variation in populations of the cacao wilt pathogen Ceratocystis cacaofunesta. Plant Pathol 56:923–933. doi:10.1111/j.1365-3059.2007.01735.x
Faleiro FG, Queiroz VT, Lopes UV, Guimarães CT, Pires JL, Yamada MM, Araújo IS, Pereira MG, Souza Filho GA, Brown JS, Schnell R, Ferreira CF, Barros EG, Moreira MA (2006) Mapping QTLs for witches’ broom (Crinipellis perniciosa) resistance in cacao (Theobroma cacao L.). Euphytica 149:227–235. doi:10.1007/s10681-005-9070-7
Fonseca SEA, Albuquerque PSB (2000) Avaliação de clones de cacau na Amazônia brasileira em relação a incidência de vassoura-de-bruxa. In: Proceedings of the 12th international Cocoa research conference. Salvador, Bahia, Brazil. Cocoa Producers’ Alliance, Lagos, Nigeria, pp 149–153
Frias GA, Purdy LH, Schmidt RA (1995) An inoculation method for evaluating resistance of cacao to Crinipellis perniciosa. Plant Dis 79:787–791
Laker HA, Sreenivasan TN, Kumar DR (1988) Present status of witches’ broom disease of cocoa in Trinidad. Trop Pest Manag 34:318–323
Leal GA Jr, Albuquerque PSB, Figueira A (2007) Genes differentially expressed in Theobroma cacao associated with resistance to witches’ broom disease caused by Crinipellis perniciosa. Mol Plant Pathol 8:279–292. doi:10.1111/j.1364-3703.2007.00393.x
Marita JM, Nienhuis J, Pires JL, Aitken WM (2001) Analysis of genetic diversity in Theobroma cacao with emphasis on witches’ broom disease resistance. Crop Sci 41:1305–1316
McCullagh P, Nelder JA (1989) Generalized linear models, 2nd edn. Chapman & Hall, London
Mondego JMC, Carazzolle MF, Costa GGL, Formighieri EF, Parizzi LP, Rincones J, Cotomacci C, Carraro DM, Cunha AF, Carrer H, Vidal RO, Estrela RC, García O, Thomazella DPT, Oliveira BV, Pires ABL, Rio MCS, Araújo MRR, Moraes MH, Castro LAB, Gramacho KP, Gonçalves MS, Moura Neto JP, Góes Neto A, Barbosa LV, Guiltinan MJ, Bailey BA, Meinhardt LW, Cascardo JCM, Pereira GAG (2008) A genome survey of Moniliophthora perniciosa gives new insights into Witches’ Broom Disease of cacao. BMC Genomics 9:548. doi:10.1186/1471-2164-9-548
Motamayor JC, Lachenaud P, Mota JWS, Loor R, Kuhn DN, Brown JS, Schnell RJ (2008) Geographic and genetic population differentiation of the Amazonian chocolate tree (Theobroma cacao L.). PLOS One 3:e3311. doi:10.1371/journal.pone.0003311
Paim VRLM, Luz EDMN, Pires JL, Silva SDVM, Souza JT, Albuquerque PSB, Santos LP (2006) Sources of resistance to Crinipellis perniciosa in progenies of cacao accessions collected in the Brazilian Amazon. Sci Agricola 63:572–578. doi:10.1590/S0103-90162006000600011
Poland JA, Balint-Kurti PJ, Wisser RJ, Pratt RC, Nelson RJ (2009) Shades of gray: the world of quantitative disease resistance. Trends Plant Sci 14:21–29. doi:10.1016/j.tplants.2008.10.006
Pound FJ (1943) Cacao and witches’ broom disease (Marasmius pernicious). In: Toxopeus H (ed) Reprint archives of cocoa research. American Cocoa Research Institute, USA, pp 73–92
Purdy LH, Schimdt RA (1996) Status of cacao witches broom: biology, epidemiology, and management. Annu Rev Phytopathol 34:573–594. doi:10.1146/annurev.phyto.34.1.573
Rincones J, Scarpari LM, Carazzolle MF, Mondego JMC, Formighieri EF, Barau JG, Costa GGL, Carraro DM, Brentani HP, Vilas-Boas LA, Oliveira BV, Sabha M, Dias R, Cascardo JM, Azevedo RA, Meinhardt LW, Pereira GAG (2008) Differential gene expression between the biotrophic-like and saprotrophic mycelia of the witches’ broom pathogen Moniliophthora perniciosa. Mol Plant Microbe Interact 21:891–908. doi:10.1094/MPMI-21-7-0891
Rios-Ruiz RA (2001) Melhoramento para resistência a doenças. In: Dias LAS (ed) Melhoramento genético do cacaueiro. FUNAPE UFG, Brazil, pp 290–324
Rudgard SA, Andebrhan T, Maddison AC, Schmidt RA (1993) Future prospects for improvement in disease management. In: Rudgard SA, Maddison AC, Andebrhan T (eds) Disease management in cocoa: comparative epidemiology of witches’ broom. Chapman & Hall, London, pp 213–220
SAS Institute (1988) SAS/STAT user’s guide. Release 6.03. Statistical Systems Institute, Cary, 1028 pp
Sereno ML, Albuquerque PSB, Vencovsky R, Figueira A (2006) Genetic diversity and natural population structure of cacao (Theobroma cacao L.) from the Brazilian Amazon evaluated by microsatellite markers. Conserv Genet 7:13–24. doi:10.1007/s10592-005-7568-0
Shaw MW, Vandenbon AE (2007) A qualitative host–pathogen interaction in the Theobroma cacao–Moniliophthora perniciosa pathosystem. Plant Pathol 56:277–285. doi:10.1111/j.1365-3059.2006.01549.x
Wheeler BEJ, Suarez C (1993) The pathosystem. In: Rudgard SA, Maddison AC, Andebrhan T (eds) Disease management in cocoa: comparative epidemiology of witches’ broom. Chapman & Hall, London, pp 9–19
Zhang D, Boccara M, Motilal L, Butler DR, Umaharan P, Mischke S, Meinhardt L (2008) Microsatellite variation and population structure in the ‘Refractario’ cacao of Ecuador. Conserv Genet 9:327–337. doi:10.1007/s10592-007-9345-8
Acknowledgements
This work was financially supported by CEPLAC, Ministry of Agriculture, American Cocoa Research Institute, Ministry of Science and Technology (PP-G7), and CNPq. We wish to acknowledge the special help of the staff of the Plant Pathology sections at CEPLAC/CEPEC and CEPLAC/ERJOH.
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de Albuquerque, P.S.B., Silva, S.D.V.M., Luz, E.D.M.N. et al. Novel sources of witches’ broom resistance (causal agent Moniliophthora perniciosa) from natural populations of Theobroma cacao from the Brazilian Amazon. Euphytica 172, 125–138 (2010). https://doi.org/10.1007/s10681-009-0068-4
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DOI: https://doi.org/10.1007/s10681-009-0068-4