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Detection of genetic resistance to cocoa black pod disease caused by three Phytophthora species

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Abstract

Disease has become a major limiting factor for the production of cacao crops. Black pod disease, which is caused by Phytophthora spp., has caused losses of 40 % of the worldwide production of cacao crops. The most efficient way to control black pod disease is to use resistant crop varieties. In this study, a total of 262 genotypes obtained from F1 cacao segregating progeny (TSH 1188 × CCN 51) were evaluated for their genetic resistance to infection by three species of Phytophthora. The descriptive estimates of resistance were significant (p < 0.01), and a high level of heritability was observed for Phytophthora spp. (h2 = 0.759 for P. citrophthora, h2 = 0.839 for P. palmivora, h2 = 0.799 for P. capsici). Statistically distinct homogeneous groups (p < 0.01; Scott–Knott) were observed. Ten genotypes that are resistant to Phytophthora spp. were identified. The frequency of the individuals within each homogeneous group suggests that resistance to black pod disease is oligogenic. Our results, which suggest that resistance to black pod disease in cocoa trees is most likely oligogenic, have extremely important implications for cocoa breeding programs. Resistance to the various species that cause black pod disease in cocoa is associated with genetic variability. This result is very important for cocoa breeding programs that aim to use molecular markers to increase genetic selection gain per unit time. The genotypes of the cocoa progeny segregating in the F1 generation (TSH 1188 × CCN 51) are very useful in studies aimed at increasing cocoa resistance to black pod disease.

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References

  • Appiah AA, Flood J, Archer SA, Bridge PD (2004) Molecular analysis of the major Phytophthora species on cocoa. Plant Pathol 53(2):209–219

    Article  CAS  Google Scholar 

  • Ayres M, Ayres Jr M, Ayres DL, Santos AAS (2005) BioStat 4.0. Aplicações estatísticas nas áreas das ciências biomédicas. Versão 5.0, Belém, Pará: Sociedade Civil Mamirauá, MCT-CNPq, p 324

  • Bahia RCS (2007) Caracterização fenotípica da população F1 (TSH 1188 × CCN 51) de cacaueiro quanto a resistência à podridão-parda e ao número de óvulos por ovário. PhD Thesis, Universidade Estadual de Santa Cruz

  • Bartley BGD (1986) Cocoa, Theobroma cocoa. FAO Plant Production and Protection Paper

  • Bowers JH, Bailey BA, Hebbar PK, Sanogo S, Lumsden RD (2001) The impact of plant diseases on world chocolate production. Plant Health Progress IOP Publishing PhysicsWeb. http://www.apsnet.org/publications/apsnetfeatures/Pages/WorldChocolateProduction.aspx. Accessed 05 Nov 2015

  • Boza EJ, Motamayor JC, Amores FM, Cedeño-Amador S, Tondo CL, Livingstone-III DS, Schnell RJ, Gutiérrez AO (2014) Genetic Characterization of the Cacao Cultivar CCN 51: its Impact and Significance on Global Cacao Improvement and Production. J Am Soc Hortic Sci 139(2):219–229

    CAS  Google Scholar 

  • Campello AMFL, Luz EDMN (1981) Etiologia da podridão-parda nos estados da Bahia e Espírito Santo. Fitopatologia Brasileira 6(3):313–321

    Google Scholar 

  • Campello AMFL, Luz EDNM, Resnik FCZ (1982) Podridão-parda do cacaueiro no Estado da Bahia, Brasil. 1. Virulência das espécies de Phytophthora. Rev Theobroma 12(1):1–6

    Google Scholar 

  • Cilas C, Despreaux D (2004) Improvement of cocoa tree resistance to Phytophthora diseases. CIRAD, Montpellier, pp 77–102

  • Costa JLS, Menge JA, Casale WL (2000) Biological control of Phytophthora root rot of avocado with microorganisms grown in organic mulches. Braz J Microbiol 31:239–246

    Article  Google Scholar 

  • Dias LAS (2001) Origem e dispersão de Theobroma cocoa L.: um novo cenário. In: Dias LAS (ed) Melhoramento genético do cacaueiro Funape, Viçosa, pp 81–127

  • Efombagna MIB, Nyassé S, Sounigo O, Kolesnikova-Allenc M, Eskes AB (2007) Participatory cocoa (Theobroma cocoa) selection in Cameroon: phytophthora pod rot resistant accessions identified in farmers’ fields. Crop Prot 26:1467–1473

    Article  Google Scholar 

  • Evans HC (2007) Cocoa diseases—The trilogy revisited. Phytopathology 97:1640–1643

    Article  PubMed  Google Scholar 

  • Fulton RH (1989) The cocoa disease trilogy: black pod, monilia pod rot, and witches’-broom. Plant Dis 73:601–603

    Article  Google Scholar 

  • Furtado FD (2011) SisVar: a computer statistical analysis system. Ciênc Agrotecnologia (UFLA) 35(6):1039–1042

    Google Scholar 

  • Garcia CH (1989) Tabelas para classificação do coeficiente de variação. Circular técnica IPEF 10

  • Gregory PH, Maddison AC (1981) Epidemiology of Phytophthora on cocoa in Nigeria. Phytopathological paper No 25. Commonwealth Micological Intitute, Kew

  • Iwaro AD, Sreenivasan TN, Umaharan P (1997) Foliar resistance to Phytophthora palmivora as an indicator of pod resistance in Theobroma cocoa. Plant Dis 81:619–624

    Article  Google Scholar 

  • Iwaro AD, Sreenivasan TN, Umaharan P (1998) Cocoa resistance to Phytophthora: effect of pathogen species, inoculation depths and pod maturity. Eur J Plant Pathol 104:11–15

    Article  Google Scholar 

  • Iwaro AD, Bekele FL, Butler DR (2003) Evaluation and utilization of cocoa (Theobroma cocoa L.) germplasm at the International Cocoa Genebank. Trinidad Euphytica 130:207–221

    Article  CAS  Google Scholar 

  • Iwaro AD, Butler DR, Eskes AB (2006) Sources of resistance to Phytophthora pod rot at the International Cocoa Genebank, Trinidad. Genet Res Crop Evol 53:99–109

  • Konam JK (2004) Guest DI (2004) Role of beetles (Coleoptera: Scolytidae and Nitidulidae) in the spread of Phytophthora palmivora pod rot of cocoa in Papua New Guinea. Australas Plant Pathol 33(1):55–59

    Article  Google Scholar 

  • Luz EDMN, Silva SDVM (2001) Podridão-parda dos frutos, cancro e outras doenças causadas por Phytophthora no cacaueiro. In: Luz EDMN, Santos AF, Matsuoka K, Bezerra JL (eds) Doenças causadas por Phytophthora no Brasil. Livraria Rural, Campinas, pp 175–265

    Google Scholar 

  • Luz EDMN, Yamada MM (1985) Índices para avaliar a reação de cultivares de cacau a Phytophthora spp. Rev Theobroma 14(3):181–188

    Google Scholar 

  • Luz EDMN, Mitchell DL, Brugnerotto MIB (1992) Levantamento populacional de Phytophthora spp. em solo de cacaueiro na Bahia. Fitopatol Bras 17(2):152

    Google Scholar 

  • Luz EDMN, Silva SDVM, Yamada MM, Lopes UV, Braga MCT, Brugnerotto MIB (1996) Selection of cacao genotypes resistant to Phytophthora capsici, P. palmivora and P. citrophthora in Bahia. Brasil Fitopatol Bras 21:71–79

    Google Scholar 

  • Luz EDMN, Ram A, Rocha CSS, Freitas DB (2003) Aumento da frequência de ocorrência de Phytophthora citrophthora em cacaueiros no sul da Bahia. Fitopatol Bras 28:214–215

    Google Scholar 

  • Luz EDMN, Sgrillo RB, Santos Filho LP (2005) Estimativas de danos e perdas causadas por doenças no cacaueiro. In: Proceedings of the Primeiro Workshop de Epidemiologia de Doenças de Plantas. Universidade Federal de Viçosa, Viçosa

  • Mckinney HH (1923) Influence of soil, temperature and moisture on infection of wheat seedlings by Helminthosporium sativum. J Agric Res 2:195–217

    Google Scholar 

  • Medeiros AG (1967) Evolução da podridão-parda nos cacaueiros. Comissão Executiva do Plano da lavoura cacaueira: Informe Técnico no 40

  • Micheli F, Guiltinan MJ, Gramacho KP, Wilkinson MJ, Figueira AVO, Cascardo JCM, Maximova SN, Lanaud C (2010) Functional genomics of cacao. In: Jean-Claude K, Michel D (eds) Advances in botanical research: 55. Academic Press, Londres, pp 119–177

    Chapter  Google Scholar 

  • Ndoumbe-Nkeng M, Cilas C, Nyemb E, Nyassé S, Bieysse D, Flori A, Sache I (2004) Impact of removing diseased pods on cocoa black pod caused by Phytophthora megakarya and on cocoa production in Cameroon. Crop Prot 23:415–424

    Article  Google Scholar 

  • Nyassé S, Cilas C, Hérail C, Blaha G (1995) Leaf inoculation as an early screening test cocoa (Theobroma cocoa L.) resistance to Phytophthora black pod disease. Crop Prot 14:657–663

    Article  Google Scholar 

  • Nyassé S, Despréaux D, Cilas C (2002) Validity of a leaf inoculation test to assess the resistance to Phytophthora megakarya in a cocoa (Theobroma cocoa L.) diallel mating design. Euphytica 123:395–399

    Article  Google Scholar 

  • Nyassé S, Efombagn-Mousseni IB, Eskes AB (2003) Selection for resistance to black pod disease and yield gains prediction by use of selected cocoa varieties in Cameroon. Plant Genetic Resour 1(2–3):157–160

    Article  Google Scholar 

  • Oliveira ML, Luz EDMN (2005) Identificação e manejo das principais doenças do cacaueiro no Brasil: CEPLAC/CEPEC/SEFIT

  • Paulin D, Ducamp M, Lachenaud P (2008) New sources of resistance to Phytophthora megakarya identified in wild cocoa tree populations of French Guiana. Crop Prot 27:1143–1147

    Article  Google Scholar 

  • Peixoto LA, Ferreira A, Silva MF, Cruz CD (2014) Valuation of methodologies for mapping oligogenic trait loci in Recombinant Inbred Lines (RILs). Acta Sci 36(1):19–26

    Google Scholar 

  • Pokou ND, N’Goran JAK, Kébé I, Eskes A, Tahi M, Sangaré A (2008) Levels of resistance to Phytophthora pod rot in cocoa accessions selected on-farm in Côte d’Ivoire. Crop Prot 27:302–309

    Article  Google Scholar 

  • Pugh T (2005) Etude du déséquilibre de liaison chez le cocoayer appartenant aux groupes Criollo/Trinitario. Application au marquage génétique d’inté rêt pour la sélection. PhD Thesis, Ecole National Supérieur de Agriculture

  • Raizer AJ, Vencovsky R (1999) Estabilidade fenotípica de novas variedades de cana–de–açúcar para o Estado de São Paulo. Pesq Agropecu Bras 34:2241–2246

    Google Scholar 

  • Risterucci AM, Paulin D, Ducamp M, N’Goran JAK, Lanaud C (2003) Identification of QTLs related to cocoa resistance to three species of Phytophthora. Theor Appl Genet 108(1):168–174

    Article  CAS  PubMed  Google Scholar 

  • Santos CEN, Mendes MAS (1967) Ministério da agricultura, Pecuária e Abastecimento Coordenação-Geral de Agrotóxicos e Afins/DFIA/DAS

  • Santos RMF, Lopes UV, Bahia RC, Machado RCR, Ahnert D, Correa RX (2007) Marcadores microssatelites relacionados com a resistência a vassoura-de-bruxa do cacaueiro. Pesq Agropecu Bras 42:1137–1142

    Article  Google Scholar 

  • Santos ESL, Cerqueira-Silva CBM, Clement DPL, Luz EDMN (2009) Identificação de resistência genética do cacaueiro à podridão-parda. Pesq Agropecu Bras 44(4):413–416

    Google Scholar 

  • Santos ESL, Cerqueira-Silva CBM, Clement D, Luz EDMN (2011) Resistance gradient of black pod disease in cocoa and selection by leaf disk assay. Crop Breed Appl Biotechnol 1:297–303

    Article  Google Scholar 

  • Silva CL, Paim MCA, Santos ESL, Cerqueira-Silva CBM, Lopes UW, Luz EDNM (2008) Avaliação da reação de clones de cacaueiro à inoculação com Phytophthora citrophthora. In: Proceedings of the XX Congresso Brasileiro de Fruticultura, Vitória. Society for Tropical Horticulture

  • Surujdeo-Maharaj S, Umaharan P, Iwaro AD (2001) A study of genotype-isolate interaction in cocoa (Theobroma cocoa L.): resistance of cocoa genotypes to isolates of Phytophthora palmivora. Euphytica 118:295–303

    Article  Google Scholar 

  • Tahi GM, Kébé BI, Eskes AB, Ouattara S, Sangaré A, Mondeil F (2000) Rapid screening of cocoa genotypes for field resistance to Phytophthora palmivora using leaves, twigs and roots. Eur J Plant Pathol 106:87–94

    Article  Google Scholar 

  • Tahi GM, Kébe BI, Sangre A, Mondeil A, Cilas C, Eskes AB (2006) Foliar resistance of cocoa (Theobroma cocoa) to Phytophthora palmivora as an indicator of pod resistance in the field: interaction of cocoa genotype, leaf age and duration of incubation. Plant Pathol 55:776–782

    Article  Google Scholar 

  • Tahi GM, Kébé BI, Sangare A, Cilas C, Eskes AB (2007) Foliar resistance of cocoa (Theobroma cocoa) to Phytophthora palmivora as an indicator of pod resistance in the field: the effect of light intensity and time of day of leaf collection. Plant Pathol 56:219–226

    Article  Google Scholar 

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Acknowledgments

The authors wish to thank the National Council for Scientific and Technological Development (CNPq), the Research Foundation of the State of São Paulo (FAPESP, proc. 2008/52197-4) and Coordination of Higher Education Personnel Improvement (CAPES PROCAD NF-2008) for funding and felowships. We would also like to thank the researchers at the Laboratory of Molecular Genetic Analysis (LAGM) of the Molecular Biology and Genetic Engineering Center (CBMEG) at the University of Campinas (UNICAMP/SP, Brasil) and the Center for Biotechnology and Genetics (CBG-UESC/BA, Brazil), as well as the Laboratory of Phytophthora (PhytoLab-CEPLAC/Cepec/BA, Brazil) for providing the facilities required for the execution of this study. We would also like to thank Dr. J. C. Motamayor at the Mars Center of Cocoa Science (MCCS/BA, Brazil) for providing the MP-01 mapping population and logistical support for the collection of field samples. In addition, we are grateful for our collaborators Fernanda Bispo, Ademilde Cerqueira, Tita Primo and Cenilda Rocha for their assistance with black pod phenotyping. We are also grateful for Joaquim Manoel da Silva for performing the statistical analyses.

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Correspondence to A. P. Souza.

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Barreto, M.A., Santos, J.C.S., Corrêa, R.X. et al. Detection of genetic resistance to cocoa black pod disease caused by three Phytophthora species. Euphytica 206, 677–687 (2015). https://doi.org/10.1007/s10681-015-1490-4

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