Cocoa plant diseases and importance of Bacilus subtilis to induce resistance on crops in agriculture-A review

DOI: 10.18805/IJARe.A-313    | Article Id: A-313 | Page : 125-132
Citation :- Cocoa plant diseases and importance of Bacilus subtilis to induce resistance oncrops in agriculture-A review.Indian Journal Of Agricultural Research.2019.(53):125-132
Koua Saman Hervé, Alloue-Boraud Wazé Aimée Mireille, and Coulibaly N’golo Antoine Marie-David
Address : Department of Food Science and Technology Laboratory of Biotechnology and Food Microbiology, University of Nangui Abrogoua, 02 bp 801 Abidjan 02, Cote d’Ivoire.
Submitted Date : 27-11-2017
Accepted Date : 2-12-2018


Fungal and viral infections represent a major cause of cocoa disease in agriculture. Plant protection through biological control is an alternative strategy in agriculture to control pests. Recognition of certain non-pathogenic rhizobacteria by plants can trigger a systemic resistance reaction that renders the host less susceptible to subsequent infection by a virulent agent. The impact of cocoa diseases as black pod, Cocoa Shollen Shoot Virus (CSSV), witches’ broom, and frosty pod rot, has increased dramatically in the world.This paper review emphasizes cocoa disease and utilisation of Bacillus subtilis as biocontrol agent against fungal and virus from cocoa disease in Côte d’Ivoire.


Agriculture Bacillus subtilis Black pod Cocoa disease Côte d’Ivoire CSSV Systemic resistance.


  1. Abd-Alla, M.H. (1994). Phosphatases and the utilization of organic phosphorus by Rhizobium leguminosarum biovar viceae. Lett Appl Microbiol., 18: 294-296.
  2. Alibert, H. (1946). Note préliminaire sur une nouvelle maladie du cacaoyer le “swollen shoot”. Pages 34-43 in : Agronomie Tropicale., 1: 34-43.
  3. Al-Mughrabi, K.I. (2008). Salicylic Acid Induces Resistance in Potatoes against Rhizoctonia solani, the Cause of Black Scurf and Stem Canker. Int J Biol Chem., 2: 14-25.
  4. Andrade, B.S., Taranto A., Goes-Neto, A., Duante A. A. (2009). Comparative modeling of DNA and RNA polymerase from Monilio    phthoraperniciosa mitochondrial plasmid. Theor Biol Med Model., 6: 22-32.
  5. Assileva, V.M., Vassilev, N., Fenice, M., Federici, F. (2001). Immobilized cell technology applied in solubilization of insoluble inorganic (rock) phosphate and P plant acquisition. Bioresour Technol., 79: 263-271
  6. Barros, O. (1978). Algunos aspectos de la “Escoba de Bruja” en Colombia. El Cacaotero Colombiano., 7(2): 43-56.
  7. Bhattacharyya, P.N., and Jha D.K. (2012). Plant growth-promoting rhizobacteria (PGPR) : emergence in agriculture. World J. Microbiol. Biotechnol., 28: 1327-1350.
  8. Cawoy, H., Bettiol, W., Fickers, P., Ongena, M. (2011). Bacillus-Based Biological Control of Plant Diseases, Pesticides in the Modern World - Pesticides Use and Management, (Ed.), ISBN: 978-953-307-459-7. pp. 31.
  9. Chagas, J.A.F., Oliveira, A.G., Oliveira, L.A., Santos, G.R.D., Chagas, L.F.B., Lopes, A.L.D.S., Costa, D.L.J. (2015). Production of indole-3-acetic acid by bacillus isolated from Different soils. Bulg J Agric Sci., 21(2): 282-287.
  10. Chee, K.H. and Wastie, R.L. (1970). Black pod disease of cacao. Planter., 46: 294-97.
  11. Chung, S., Kong, H., Buyer, J.S., Lakshman, D.K., Lydon, J., Kim, S.D. (2008). Isolation and partial characterization of Bacillus subtilis ME488 for suppression of soilborne pathogens of cucumber and pepper. ýAppl. Microbiol. Biotechnol., 80(1): 115-23.
  12. Cleyet-Marcel, J.C., Larcher, M., Bertrand, H., Rapior, S., Pinochet, X. (2001). Plant growth enhancement by rhizobacteria. In J-F Morot-Gaudry, ed, Nitrogen Assimilation by Plants, Physiological, Biochemical and Molecular Aspects. Science Publishers, Inc., Enfeld, NH, Croft K, Juttner F, Slusarenko AJ (1993) Volatile Products, pp. 185-197.
  13. Davey, M.E., Caiazza, N.C., Toole, G.A.O. (2003). Rhamnolipid surfactant production affects biofilm architecture in Pseudomonas aeruginosa PAO1. J Bacteriol., 185: 1027-1036.
  14. Dufour, B., Djiekpor, E.K., Paulin, D., Cilas, C. (1993). Methode de criblage pour la resistance au virus du swollen-shoot: amélioration de la transmission par cochenilles. In : Proc. 11th Int. Cocoa Res. Conf. Yamassoukro, Cote d’Ivoire. 243p.
  15. Dzahini-Obiatey, H., Domfeh, O., Amoah, F.M. (2010). Review : Over seventy years of a viral disease of cocoa in Ghana: From researchers’ perspective. Afr. J. Agric. Res., 5(7): 476-485.
  16. Dzahini-Obiatey, H. and Adu, A.Y. (2010). Cocoa swollen shoot virus : genus Badnavirus. In: Technical Guidelines for the Safe Movement of Cacao Germplasm (Revised from FAO/IPGRI Technical Guidelines No 20). Eds: End, MJ, Daymond, AJ & Hadley, P. Global Cacao Genetic Resources Network (CacaoNet). Bioversity International. Montpellier, France, pp.20-22.
  17. End, M.J., Daymond, A.J., Hadley, P. (2014). Guide technique pour les transferts sécurisés de matériel génétique de cacaoyer. Révision des Directives techniques FAO/IPGRI No. 20. Global Cacao Genetic Resources Network (CacaoNet), Bioversity International, Montpellier, France. pp. 90.
  18. Evans, H.C., Bezerra, J.L., Barreto, R.W. (2013). Of mushrooms and chocolate trees: aetiology and phylogeny of witches’ broom and frosty pod diseases of cacao. Plant Pathol., 62: 728-740.
  19. Evans, H.C. (2012). Cacao Diseases in the Americas : Myths and Misnomers. Fungy, 7p. Frias, G.A, Purdy, L.H. (1991). Infection biology of Crinipellisperniciosa on vegetative flushes of cacao. Plant Dis., 75: 552-556.
  20. Gajbhiye, A., Alok, R.R., Meshram, S.U., Dongre, A.B. (2010). Isolation, evaluation and characterization of Bacillus subtilis from cotton rhizospheric soil with biocontrol activity against Fusarium oxysporum. World J Microbiol Biotechnol., 26(7): 1187-1194.
  21. Gupta, A., Khulbe, D., Srinivas, P. (2016). Enhancing resistance of rice bean to diseases by seed treatment with Pseudomonas flourescens and Bacillus species. Legume Research., 39(6): 1013-1020.
  22. Gutjahr, C., Paszkowski, U. (2009). Weights in the balance: jasmonic acid and salicylic acid signaling in root-biotroph interactions. Mol Plant Microbe Interact., 22: 763-772.
  23. Harm, A., Kassemeyer, H-H., Seibicke, T., Regner, F. (2011). Evaluation of chemical and natural resistance inducers against downy mildew (Plasmopara viticola) in grapevine. Am. J. Enol. Vitic., 62: 184-192.
  24. ICCO (2015). What are the effects of intensive commercial production of cocoa on the environnement ? Westgate House W5 1YY, United Kingdom. Rapport Annuel ICCO. 25p.
  25. Jacques P. (2011). Surfactin and other lipopeptides from Bacillus spp. Microbiol Monogr., 20: 57-91.
  26. Kebe, B.I., Kouakou, K., N’Guessan, N.F., Assiri, A.A., Adiko, A., Aké, S., Anno, A.P. (2006). 
  27. Le swollen shoot en Cote d’Ivoire: situation actuelle et perspectives. in: Proc. 15th Int. Cocoa Res. Conf. San José, Costa Rica. pp. 907-922.
  28. Kouakou, K., Kébé, B.I., Kouassi, N., Aké, S., Cilas, C., Muller, E., (2012). Geographical distribution of Cacao swollen shoot virus molecular variability in Cote d’Ivoire. Plant Dis., 96: 1445-1450.
  29. Kumar, M.V. and Kumar, A. (2012). Plant growth promoting and phytostimulatory potential of Bacillus subtilis and Bacillus amylo    liquefaciens. ARPN J. Agric. biol. Sci., 7(7): 509-519.
  30. Liyanage, N.I.S., Wheeler B.E.J. (1989). Phytophthora katsurae from cocoa. Plant Pathol., 38: 627-912.
  31. Lozano, T.Z.E., Romero, C.S. (1984). Estudio taxonómico de aislamientos de Phytophthora patógeno de cacao. Agrociencia., 56:176-82.
  32. Maget-Dana, R., Peypoux, F. (1994). Iturins, a special class of poreforming lipopeptides: Biological and physicochemical properties. Toxicology., 87: 151-174.
  33. Malfanova, N., Kamilova, F., Validov, S. H., Shcherbakov, A., Chebotar, V., Tikhonovich, I., Lugtenberg, B. (2011). Characterization of Bacillus subtilis HC8, a novel plant-beneficial endophytic strain from giant hogweed. Microbiol Biotechnol., 4: 523-532.
  34. Martens, H. (2011). Le cacao un levier de développement. CTB-BTC, 147 Rue Haute – B- 1000 Bruxelles, Belgique. 48p.
  35. Meinhardt, L.W., Rincones, J., Bailey, B.A., Aime, M.C., Griffith, G.W., Zhang, D. (2008). Moniliophthoraperniciosa, the causal agent of witches’ broom disease of cacao: what’s new from this old foe? Mol. Plant Pathol., 9: 577-588.
  36. Mohali, S., Burgess, T.I., Wingfield, M.J. (2005). Diversity and host association of the tropical tree endophyte Lasiodiplodia theobromae revealed using simple sequence repeat markers. Forest Pathology., 35: 385-396.
  37. Mohiddin, F.A., Khan M.R. (2018). Efficacy of newly developed biopesticides for the management of wilt disease complex of chickpea (Cicer arietinum L.). Legume Research., DOI: 10.18805/LR-3873
  38. Mohnider, K., Sapna, S., Atul, M. (2011). Influence of phosphate solubilizing Pseudomonas and Bacillus strains on the Growth of Ashvagandha. Indian J. Agric. Res., 45(2): 128- 133
  39. Monteiro, S., Clemente, J., Henriques, A.O., Gomes, R., Carrondo, M., Cunha, A. (2005). A procedure for high-yield spore production by Bacillus subtilis. Biotechnol Prog., 21: 1026-1039.
  40. Muller E. (2008). Cacao swollen shoot virus. In Encyclopedia of Virology, 3rd ed. [B. W. J. Mahy and M. H. V. Van Regenmortel, eds.] Elsevier, Oxford. pp. 403-409
  41. Nyasse, S., Efombagn, M.I.B., Kebe, B.I., Tahi, M., Despréaux, D., Cilas, C. (2007). Integrated management of Phytophthora diseases on cocoa (Theobroma cacao L): impact of plant breeding on pod rot incidence. Crop Prot., 26:40-45.
  42. Ollenu, L.A.A., Owusu, G.K., Thresh, J.M. (1989). Spread of cocoa swollen shoot virus (CSSV) to recent plantings in Ghana. Crop Prot., 8:251-164.
  43. Ongena, M. (2014). Biopesticides : une protection plus naturelle pour les cultures. Université de Liège -, 10p.
  44. Ongena M. and Jacques, P. (2008). “Bacillus lipopeptides: versatile weapons for plant disease biocontrol,” Trends Microbiol., 16(3): 115-125.
  45. Ongena, M., Adam, A., Jourdan, E., Paquot, M., Brans, A., Joris, B., Arpigny, J.L., Thonart, P. (2007). Surfactin and fengycin lipopeptides of Bacillus subtilis as elicitors of induced systemic resistance in plants. Environ. Microbiol., 9: 1084-1090.
  46. Opoku, I.Y., Assuah, M.K., Aneani, F. (2007). Management of black-pod disease of cocoa with reduced number of fungicide application and crop sanitation. Afr. J. Agric. Res., 2: 601-604.
  47. Persello-Cartieaux, F., Nussaume, L., Robaglia, C. (2003). Tales from the underground: molecular plant-rhizobacterial interactions. Plant Cell Environ., 26: 189-199.
  48. Piggot, P., Hilbert, D. (2004). Sporulation of Bacillus subtilis. Curr Opin Microbiol., 7 (6) : 579-586.
  49. Pires, A.B.L., Gramacho, K.P., Silva, D.C., Goes-Neto, A., Silva, M.M., Muniz-Sobrinho, J.S., Porto, R.F., Villela-Dias, C., Brendel, M., Cascardo, J.C.M., Pereira, G.A.G. (2009). Early development of Moniliophthora perniciosa basidiomata and developmentally regulated genes. BMC Microbiology., 9: 18-25
  50. Raaijmakers, J.M., De, B.I., Nybroe, O., Ongena, M. (2010). Natural functions of lipopeptides from Bacillus and Pseudomonas: more than surfactants and antibiotics. FEMS Microbiol Rev., 34: 1037-1062. 
  51. Romero, D., De V.A., Rakotoaly, R., Dufour, S., Veening J., Arrebola E. (2007). The iturin and fengycin families of lipopeptides are key factors in antagonism of Bacillus subtilis toward Podosphaera fusca. Mol Plant Microbe Interact., 20: 430-440
  52. Roongsawang, N., Washio, K., Morikawa, M. (2011). “Diversity of non ribosomal peptide synthetases involved in the biosynthesis of lipopeptide biosurfactants, Int. J. Mol. Sci., 12: 41-172.
  53. Rosas-Garcia, N. (2009). Biopesticide production from Bacillus thuringiensis : an environmentally friendly alternative. Recent Pat Biotechnol., 3: 28-36.
  54. Rubini, M. R., Silva-Ribeiro, R.T., Pomella, A.W., Maki, C.S., Araujo, W.L., Dos-Santos, D.R., Azevedo, J.L. (2005). Diversity of endophytic fungal community of cacao (Theobroma cacao L.) and biological control of Crinipellis perniciosa, causal agent of Witches’ Broom Disease. Int J Biol Sci., 1: 24-33.
  55. Ryu, C., Farag, M.A., Hu, C., Reddy, M.S., Kloepper, J.W., Pare, P.W. (2004). Bacterial Volatiles Induce Systemic Resistance in Arabidopsi, Plant Physiol., 137: 1475-1486.
  56. Scarpari, L.M., Meinhardt, L.W., Mazzafera, P., Pomella, A.W.V., Schiavinato, M.A., Cascardo, J.C.M., Pereira, G.A.G. (2005). Biochemical changes during the development of witches’broom: the most important disease of cocoa in Brazil caused by Crinipellis perniciosa. J. Exp. Bot., 56(413): 865-877. 
  57. Shoresh, M., Harman, G., Mastouri, F. (2010). Induced systemic resistance and plant responses to fungal biocontrol agents. Annu Rev Phytopathol., 48:21-43.
  58. Sicuia, O.A., Florica, C., Cornea, C.P. (2015). Biodiversity of Bacillus subtilis group and beneficial traits of Bacillus species useful in plant protection. Rom Biotech Lett., 20(5): 10737-10750
  59. Silva, S.D.V.M., Luz, E.D.M.N., Almeida, L.C., Gramacho, K.P., Bezerra, J.L. (2002). Redescicao da sintomatologia causada por Crinipellis perniciosa em cacaueiro. Agrotropica., 14(1): 1-10
  60. Stanley, N.R., Britton, R.A., Grossman, A.D, Lazazzera, B.A. (2003). Identification of catabolite repression as a physiological regulator of biofilm formation by Bacillus subtilis by use of DNA microarrays. J Bacteriol., 185: 1951-1957. 
  61. Steven, W.F. (1936). A new disease of cocoa in the Gold Coast. Gold Coast Farmer., 5(122): 144-165.
  62. Sudhapriyadharsini, S., Balaji, S., Vivek, M. (2016). Production, purification and application of plant growth hormones (IAA and Gibberellic acid) by bacillus subtilis. J Biospectra., 1(5): 1-4.
  63. Susilene, E.L.D.S., Cerqueira-Silva, C.B.M., Didier, C., Edna, D.M.N.L. (2011). Resistance gradient of black pod disease in cocoa and selection by leaf disk assay. Crop Breed Appl Biot., 11: 297-303.
  64. Thresh, J.M. (1991). The ecology of tropical plant viruses. Plant Pathol., 40 : 324-339.
  65. Toure, Y., Ongena, M., Jacques, P., Guiro, A., Thonart, P. (2004). Role of lipopeptides produced by Bacillus subtilis GA1 in the reduction of grey mould disease caused by Botrytis cinerea on apple. J Appl Microbiol., 96: 1151-1160.
  66. Twumasi, P., Ohene-Mensah, G., Moses, E. (2014). The rot fungus Botryodiplodia theobromae strains cross infect cocoa, mango, banana and yam with significant tissue damage and economic losses. Afr. J. Agric. Res., 9(6): 613-619.
  67. Vos, J.G.M., Ritchie, B.J., Flood, J. (2003). Fiche de données sur les parasites. In : A la 
  68. découverte du cacao. Un guide stimulant pour la formation des facilitateurs. CABI Biosciences, eds. Wallingford, UK. pp. 11-58. Xie, S.S., Wu, H.J., Zang, H.Y., Wu, L.M., Zhu, Q.Q., Gao, X.W. (2014). Plant Growth Promotion by Spermidine- Producing Bacillus subtilis OKB105. Mol. Plant Microbe Interact., 27(7): 655-663.
  69. Yang, Y., Shah, J., Klessig, D.F. (2011). Signal perception and transduction in plant defence responses. Genes Dev., 11: 1621-1639.
  70. Zehnder, G.W., Yao, C., Murphy, J.F., Sikora, E.J., Kloepper, J.W. (2000). Induction of resistance in tomato against cucumber mosaic cucumovirus by plant growth-promoting rhizobacteria. Biocontrol., 45: 127–137. 
  71. Zhao, Y. (2010). Auxin biosynthesis and its role in plant development. Annu Rev Plant Biol., 61: 49-64. 

Global Footprints