Selection of Trichoderma stromaticum isolates for efficient biological control of witches' broom disease in cacao

Biological Control

Volumn 51, Issue 1, 2009, Pages 130-139

  Loguercio, Leandro Lopes ^a   de Carvalho, Aítala Carvalho ^a,b   Niella, Givaldo Rocha ^c   De Souza, Jorge Teodoro ^d   Pomella, Alan W Villela ^b  

^a DEPARTAMENTO DE CIÊNCIAS BIOLÓGICAS   (Brazil)

^b Almirante Cacau Ltda   (Brazil)

^c CEPEC/CEPLAC   (Brazil)

^d UNIVERSIDADE FEDERAL DO RECÔNCAVO DA BAHIA   (Brazil)

Author keywords

Antagonistic interaction; Biocontrol; Hemibiotrophic pathogen; Moniliophthora; Mycoparasitism; Screening; Theobroma cacao

Indexed keywords

FUNGI; MONILIOPHTHORA; THEOBROMA CACAO; TRICHODERMA; TRICHODERMA STROMATICUM;

EID: 69249203564     PISSN: 10499644     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocontrol.2009.06.005     Document Type: Article

References (55)

1. Anderbrhan T., Figueira A., Yamada M.M., Cascardo J., and Furtek D.B. Molecular fingerprinting suggests two primary outbreaks of witches' broom disease (Crinipellis perniciosa) of Theobroma cacao in Bahia, Brazil. European Journal of Plant Pathology 105 (1999) 167-175
2. Ayres, M., Ayres Jr., M., Ayres, D.L., dos Santos, A.A.S., 2007. BioEstat-Aplicações estatísticas nas áreas de ciências biomédicas. Fundação Mamirauá, Belém-PA, Brazil. Available from: .
3. Bajwa W.I., and Kogan M. Cultural practices: springboard to IPM. In: Koul O., Dhaliwal G.S., and Cuperus G.W. (Eds). Integrated Pest Management: Potential, Constraints and Challenges (2004), CABI Publishing, Wallingford-UK 21-38
4. Bastos C.N. Mycoparasitic nature of the antagonism between Trichoderma viride and Crinipellis perniciosa. Fitopatologia Brasileira 21 (1996) 50-54
5. Bastos C.N. Trichoderma stromaticum sp. nov. on the production of basidiomatas and on infections of shoots and cushion flowers of cocoa by Crinipellis perniciosa. Agrotrópica 12 (2000) 59-62 (portuguese)
6. Bastos C.N. Biological control of Crinipellis perniciosa by an isolate of Trichoderma sp. In: Akrofi A.Y., and Baah F. (Eds). INCOPED Fifth Proceedings of International Seminar on Cocoa Pests and Diseases (2006), San Jose, Costa Rica 1-7
7. Benitez T., Rincon A.M., Limon M.C., and Codon A.C. Biocontrol mechanisms of Trichoderma strains. International Microbiology 7 (2004) 249-260
8. Bezerra J.L., Costa J.C.B., Bastos C.N., and Faleiro F.G. Hypocrea stromatica sp. Nov. Teleomorfo de Trichoderma stromaticum. Fitopatologia Brasileira 28 (2003) 408-412
9. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72 (1976) 248-254
10. Carvalho, A.C., 2006. Bioprospection of Trichoderma stromaticum isolates for the Biological Control of the witches' broom disease of the cocoa tree. Masters Thesis. State University of Santa Cruz/UESC, Ilhéus-BA, Brazil, 82 p.
11. Chet I., Benhamou N., and Haran S. Mycoparasitism and lytic enzymes. In: Harman G.E., and Kubicek C.P. (Eds). Trichoderma and Gliocladium-Enzymes, Biological Control and Commercial Applications vol. 2 (1998), Taylor & Francis, London-UK 153-172
12. Costa J.C.B., Bezerra J.L., and Cazorla I.M. Controle biológico da vassoura-de-bruxa do cacueiro na Bahia com Trichoderma polysporum. Fitopatologia Brasileira 21 Suppl (1996) 397
13. Costa J.C.B., Bezerra J.L., Veloso J.L.M., Niella G.R., and Bastos C.N. Controle Biológico da vassoura-de-bruxa do cacaueiro. In: Venzon M., Paula Júnior T.J., and Pallini A. (Eds). Tecnologias alternativas para o controle de pragas e doenças (2006), EPAMIG, Viçosa-MG, Brazil 25-47
14. Deberdt P., Mfegue C.V., Tondje P.R., Bon M.C., Ducamp M., Hurard C., Begoude B.A.D., Ndoumbe-Nkeng M., Hebbar K.P., and Cilas C. Impact of environmental factors, chemical fungicide and biological control on cacao pod production dynamics and black pod disease (Phytophthora megakarya) in Cameroon. Biological Control 44 (2008) 149-159
15. De Marco, J.L., Felix, C.R., 2002. Characterization of a protease produced by a Trichoderma harzianum which controls cocoa plant witches' broom disease. BMC Biochemistry, 3, 3. Available from: .
16. De Marco J.L., Lima L.H.C., Souza M.V., and Felix C.R. A Trichoderma harzianum chitinase destroys the cell wall of the phytopathogen Crinipellis perniciosa, the causal agent of witches' broom disease of cocoa. World Journal of Microbiology and Biotechnology 16 (2000) 383-386
17. De Souza J.T., Pomella A.W.V., Bowers J., Pirovani C.P., Loguercio L.L., and Hebbar P. Genetic and biological diversity of Trichoderma stromaticum, a mycoparasite of the cacao witches' broom pathogen. Phytopathology 96 (2006) 61-67
18. De Souza J.T., Bailey B.A., Pomella A.W.V., Erbe E.F., Murphy C.A., Bae H., and Hebbar K.P. Colonization of cacao seedlings by Trichoderma stromaticum, a mycoparasite of the witches' broom pathogen, and its influence on plant growth and resistance. Biological Control 46 (2008) 36-45
19. Dhingra O.D., and Sinclair J.B. Basic Plant Pathology Methods (1985), CRC Press, Boca Raton-USA 355 p
20. Donald P.F. Biodiversity impacts of some agricultural commodity production systems. Conservation Biology 18 (2004) 17-37
21. Druzhinina I., and Kubicek C.P. Species concepts and biodiversity in Trichoderma and Hypocrea: from aggregate species to species clusters?. Journal of Zhejiang University Science 6B (2005) 100-112
22. Elad Y. Biocontrol of foliar pathogens: mechanisms and application. Communications in Agriculture and Applied Biological Sciences 68 (2003) 17-24
23. Griffith G.W., Nicholson J., Nenninger A., Birch R.N., and Hedger J.N. Witches' brooms and frosty pods: two major pathogens of cacao. New Zealand Journal of Botany 41 (2003) 423-435
24. Hanada R.E., De Souza J.T., Pomella A.W.V., Hebbar K.P., Pereira J.O., Ismaiel A., and Samuels G.J. Trichoderma martiale sp. Nov., a new endophyte from sapwood of Theobroma cacao and a potential agent of biological control. Mycological Research 112 (2008) 1335-1343
25. Hanada R.E., Pomella A.W.V., Soberanis W., Loguercio L.L., and Pereira J.O. Biocontrol potential of Trichoderma martiale (ALF 247) against black-pod disease (Phytophthora palmivora) of cacao. Biological Control 50 (2009) 143-149
26. Hermosa M.R., Grondona I., Iturriaga E.A., Diaz-Minguez J.M., Castro C., Monte E., and Garcia-Acha I. Molecular characterization and identification of biocontrol isolates of Trichoderma spp. Applied and Environmental Microbiology 66 (2000) 1890-1898
27. Hjeljord L., and Tronsmo A. Trichoderma and Gliocladium in biological control: an overview. In: Harman G.E., and Kubicek C.P. (Eds). Trichoderma and Gliocladium-Enzymes, Biological Control and Commercial Applications vol. 2 (1998), Taylor & Francis, London-UK 131-151
28. Hjorth, S., Pomella, A.W.V., Hockenhull, J., Hebbar, K.P., 2003. Biological control of witches' broom disease (Crinipellis perniciosa) with the co-evolved fungus Trichoderma stromaticum: testing different delivery regimes. In: 14th International Cocoa Research Conference-Towards a Sustainable Cocoa Economy: What Strategies to this End? vol. 2. COPAL, Accra-Ghana, pp. 691-697.
29. Howell C.R. Mechanisms employed by Trichoderma species in the biological control of plant diseases: the history and evolution of current concepts. Plant Disease 87 (2003) 4-10
30. Knudsen I.M.B., Hockenhull J., Funck-Jensen D., Gerhardson B., Hökeberg M., Tahvonen R., Teperi E., Sundheim L., and Henriksen B. Selection of biological control agents for controlling soil and seed-borne diseases in the field. European Journal of Plant Pathology 103 (1997) 775-784
31. Krauss U., Ten Hoopen G.M., Hidalgo E., Martínez A., Stirrup T., Arroyo C., García J., and Palacios M. The effect of cane molasses amendment on biocontrol of frosty pod rot (Moniliophthora roreri) and black pod (Phytophthora spp.) of cocoa (Theobroma cacao) in Panama. Biological Control 39 23 (2006) 2-239
32. Krauss U., and Soberanis W. Biocontrol of cocoa pod diseases with mycoparasite mixtures. Biological Control 22 (2001) 149-158
33. Krauss U., and Soberanis W. Effect of fertilization and biocontrol application frequency on cocoa pod diseases. Biological Control 24 (2002) 82-89
34. Kubicek C.P., Mach R.L., Peterbauer C.K., and Lorito M. Trichoderma: from genes to biocontrol. Journal of Plant Pathology 83 special issue (2001) 11-23
35. Lopes, V.L., Monteiro, W.R., Pires, J.L., da Rocha, J.B., Pinto, L.R.M., 2003. On farm selection for witches' broom resistance in Bahia, Brazil-a historical retrospective. In: 14th International Cocoa Research Conference-Towards a Sustainable Cocoa Economy: What Strategies to this End? vol. 2. COPAL, Accra-Ghana, pp. 1001-1006.
36. Lilliefors H. On the Kolmogorov-Smirnov test for normality with mean and variance unknown. Journal of the American Statistical Association 62 (1967) 399-402
37. Loguercio L.L., Barreto M.L., Rocha T.L., Santos C.G., Teixeira F.F., and Paiva E. Combined analysis of supernatant-based feeding bioassays and PCR as a first-tier screening strategy for Vip-derived activities in Bacillus thuringiensis strains effective against tropical fall armyworm. Journal of Applied Microbiology 93 (2002) 269-277
38. Loguercio, L.L., Santos, L.S., Niella, G.R., Miranda, R.A.C., de Souza, J.T., Collins, R.T., Pomella, A.W.V., 2009. Canopy-microclimate effects on the antagonism between Trichoderma stromaticum and Moniliophthora perniciosa in shaded cacao. Plant Pathology, in press.
39. Lorito M. Chitinolytic enzymes and their genes. In: Harman G.E., and Kubicek C.P. (Eds). Trichoderma and Gliocladium-Enzymes, Biological Control and Commercial Applications vol. 2 (1998), Taylor & Francis, London-UK 73-99
40. Meinhardt L.W., Rincones J., Bailey B.A., Aime M.C., Griffith G.W., Zhang D., and Pereira G.A.G. Moniliophthora perniciosa, the causal agent of witches' broom disease of cacao: what's new from this old foe?. Molecular Plant Pathology 9 (2008) 577-588
41. Niella, G.R., 2005. Produção massal de Trichoderma stromaticum para o controle da vassoura-de-bruxa do cacaueiro. In: 9° Simpósio de Controle Biológico-Anais. Entomological Society of Brazil, Recife-PE, p. 45.
42. Pereira J.L., Almeida L.C.C., and Santos S.M. Witches' broom disease of cocoa in Bahia: attempts at eradication and containment. Crop Protection 15 (1996) 743-752
43. Pomella A.W.V., de Souza J.T., Niella G.R., Bateman R.P., Hebbar K.P., Loguercio L.L., and Lumsden R.D. The use of Trichoderma stromaticum in the management of witches' broom disease of cacao in Bahia State, Brazil. In: Vincent C., Goettel M., and Lazarovits G. (Eds). Biological Control: A Global Perspective-Case Studies from Around the World (2007), CABI Publishing, Wallingford-UK 210-217
44. Purdy L.H., and Schmidt R.A. Status of cacao witches' broom: Biology, epidemiology, and management. Annual Review of Phytopathology 34 (1996) 573-594
45. Rajkumar M., Lee W.H., and Lee K.J. Screening of bacterial antagonists for biological control of Phytophthora blight of pepper. Journal of Basic Microbiology 45 (2005) 55-63
46. Samuels G.J., Pardo-Schultheiss R., Hebbar K.P., Lumsden R.D., Bastos C.N., Costa J.C., and Bezerra J.L. Trichoderma stromaticum sp. Nov., a parasite of the cacao witches broom pathogen. Mycological Research 104 (2000) 760-764
47. Samuels G.J., Suarez C., Solis K., Holmes K.A., Thomas S.E., Ismaiel A., and Evans H.C. Trichoderma theobromicola and T. Paucisporum: two new species isolated from cacao in South America. Mycological Research 110 (2006) 381-392
48. Sanogo S., Pomella A., Hebbar K.P., Bailey B., Costa J.C.B., Samuels G.J., and Lumsden R.D. Production and germination of conidia of Trichoderma stromaticum, a mycoparasite of Crinipellis perniciosa on cacao. Phytopathology 92 (2002) 1032-1037
49. Santos, L.S., 2005. Antagonistic interaction Trichoderma stromaticum-Crinipellis perniciosa: climate effects in the biocontrol of cacao witches' broom and development of microssatelite markers. Masters Thesis. State University of Santa Cruz/UESC, Ilhéus-BA, Brazil. 72 p.
50. Silva S.D.V.M., Luz E.D.M.N., Almeida O.C., Gramacho K.P., and Bezerra J.L. Redescription of the symptomatology caused by Crinipellis perniciosa in cacao. Agrotrópica 14 (2002) 1-24 portuguese
51. Steel R.G., and Torry J.H. Principles and Procedures of Statistics. 2nd ed. (1980), McGraw-Hill Book Co, New York-USA
52. Steyaert J.M., Ridgway H.J., Elad Y., and Stewart A. Genetic basis of mycoparasitism: a mechanism of biological control by species of Trichoderma. New Zealand Journal of Crop and Horticultural Sciences 31 (2003) 281-291
53. Tondje P.R., Roberts D.P., Bon M.C., Widmer T., Samuels G.J., Ismaiel A., Begoude A.D., Tchana T., Nyemb-Tshomb E., Ndoumbe-Nkeng M., Bateman R., Fontem D., and Hebbar K.P. Isolation and identification of mycoparasitic isolates of Trichoderma asperellum with potential for suppression of black pod disease of cacao in Cameroon. Biological Control 43 (2007) 202-212
54. Van-Zwieten, L., Merrington, G., Van-Zwieten, M., 2004. Review of impacts on soil biota caused by copper residues from fungicide application. In: SuperSoil 2004-3rd Australian New Zealand Soils Conference. University of Sydney, Australia, pp. 1-8.
55. Van-Zwieten, L., 2004. Impact of pesticides on soil biota. In: Lines-Kelly, R. (Ed.), Soil biology in agriculture-Proceedings. Tamworth Sustainable Farming Training Centre, NSW Department of Primary Industries, Orange, pp. 72-79.