Primed Expression of Defense-Related Genes by <i>Streptomyces cameroonensis</i>-Based Bioformulation (SCaB) on Cocoa Seedlings in a Nursery Challenged with <i>Phytophthora megakarya</i> — Oak Academic Publishing
Research ArticleOpen AccessGoogle Scholar indexed
Primed Expression of Defense-Related Genes by <i>Streptomyces cameroonensis</i>-Based Bioformulation (SCaB) on Cocoa Seedlings in a Nursery Challenged with <i>Phytophthora megakarya</i>
Laboratory of Phytoprotection and Valorization of Genetic Resources, Biotechnology Center, University of Yaounde I, Yaounde, Cameroon
,
Laboratory of Phytoprotection and Valorization of Genetic Resources, Biotechnology Center, University of Yaounde I, Yaounde, Cameroon
,
Department of Biochemistry and Molecular Biology, Indiana University School of Medicine, Indianapolis, IN, USA
,
Laboratory of Plant Physiology, Department of Biological Sciences, Higher Teacher’s Training College, Yaounde, Cameroon
,
Laboratory of Plant Physiology, Department of Biological Sciences, Higher Teacher’s Training College, Yaounde, Cameroon
,
Department of Biochemistry, Faculty of Science, University of Yaounde 1, Yaounde, Cameroon
1 Laboratory of Phytoprotection and Valorization of Genetic Resources, Biotechnology Center, University of Yaounde I, Yaounde, Cameroon
2 Laboratory of Phytoprotection and Valorization of Genetic Resources, Biotechnology Center, University of Yaounde I, Yaounde, Cameroon
3 Department of Biochemistry and Molecular Biology, Indiana University School of Medicine, Indianapolis, IN, USA
4 Laboratory of Plant Physiology, Department of Biological Sciences, Higher Teacher’s Training College, Yaounde, Cameroon
5 Laboratory of Plant Physiology, Department of Biological Sciences, Higher Teacher’s Training College, Yaounde, Cameroon
6 Department of Biochemistry, Faculty of Science, University of Yaounde 1, Yaounde, Cameroon
A Streptomyces cameroonensis based bioformulation (SCaB) has been developed and shown to be stable and effective in controlling the early proliferation of P. megakarya and promoting the growth of cocoa seedlings in nursery. This study was carried out to explore the molecular mechanisms associated with the interaction of SCaB, cocoa seedlings, and the pathogen during the early stages of seedling growth in the nursery. For this purpose, seedling treatment with 10% W/W SCaB under greenhouse conditions evaluated SCaB’s capacity to stimulate the defense mechanisms in cocoa. Agronomic growth parameters and the level of induction of defense-associated compounds were analyzed. Real-time (rt) PCR was used to assess the level of expression of defense genes. Here, we showed that the application of SCaB as a seedling treatment enhanced the growth of cocoa seedlings in the nursery by an average of 15.6% after 30 days of growth and led to an average reduction in disease severity of 64% when challenged with P. megakarya . The latter led to an increased synthesis of total phenolic compounds, flavonoids, chitinases, peroxidases, and β -1,3-glucanases and an induced up-regulation of TcChiB, TcGlu-1, TcPer-1, and TcMYBPA genes. This research provides a basis for the optimization of beneficial microorganisms as a viable alternative to chemical fungicides used in disease suppression.
Rego, A.P.B., Mora-Ocampo, I.Y., Pirovani, C.P., Luz, E.D.M.N. and Corrêa, R.X. (2022) Protein Level Defense Responses of Theobroma cacao Interaction with Phytophthora palmivora. Frontiers in Agronomy, 4, Article ID: 836360. https://doi.org/10.3389/fagro.2022.836360
Dzelamonyuy, A., Téné, T.P.M., Ngassam, N.E.R., Lele, B.G., Foka, T.E., Magni, P.T.F. and Boudjeko, T. (2022) Effects of a Powder Formulation of Streptomyces cameroonensis on Growth and Resistance of Two Cocoa Hybrids from Cameroon against Phytophthora megakarya (Causal Agent of Black Pod Disease). Journal of Microbiology and Biotechnology, 32, 160-169. https://doi.org/10.4014/jmb.2110.10006
Ndoumbe-Nkeng, M., Cilas, C., Nyemb, E., Nyassé, S., Bieysse, D., Flori, A. and Sache, I. (2004) Impact of Removing Diseased Pods on Cocoa Black Pod Caused by Phytophthora megakarya and on Cocoa Production in Cameroon. Crop Protection, 23, 415-424. https://doi.org/10.1016/j.cropro.2003.09.010
Delgado-Ospina, J., Molina-Hernández, J.B., Chaves-López, C., Romanazzi, G. and Paparella, A. (2021) The Role of Fungi in the Cocoa Production Chain and the Challenge of Climate Change. Journal of Fungi, 7, Article No. 202. https://doi.org/10.3390/jof7030202
Téné, T.P.M., Mouafo, T.R.A., Yamoneka, J., Dzelamonyuy, A., Woumba, N.S.C. and Boudjeko, T. (2023) Application of Heat-Treated Oyster Shell Powder to Induce Priming of Theobroma cocoa Seedlings Plant Defense System against Phytophthora megakarya Attack. Current Plant Biology, 32, Article ID: 100283. https://doi.org/10.1016/j.cpb.2023.100283
Tamreihao, K., Ningthoujam, D.S., Nimaichand, S., Singh, E.S., Reena, P., Singh, S.H. and Nongthomba, U. (2016) Biocontrol and Plant Growth Promoting Activities of a Streptomyces corchorusii Strain UCR3-16 and Preparation of Powder Formulation for Application as Biofertilizer Agents for Rice Plant. Microbiological Research, 192, 260-270. https://doi.org/10.1016/j.micres.2016.08.005
Boudjeko, T., Tchinda, R.A.M., Zitouni, M., Nana, J.A.V.T., Lerat, S. and Beaulieu, C. (2017) Streptomyces cameroonensis sp. nov., a Geldanamycin Producer that Promotes Theobroma cacao Growth. Microbes and Environments, 32, 24-31. https://doi.org/10.1264/jsme2.ME16095
Jung, S.C., Martinez-Medina, A., Lopez-Raez, J.A. and Pozo, M.J. (2012) Mycorrhiza-Induced Resistance and Priming of Plant Defenses. Journal of Chemical Ecology, 38, 651-664. https://doi.org/10.1007/s10886-012-0134-6
Lanaud, C., Fouet, O., Clément, D., Boccara, M., Risterucci, A.M., Surujdeo-Maharaj, S., Legavre, T. and Argout, X. (2009) A Meta-QTL Analysis of Disease Resistance Traits of Theobroma cacao L. Molecular Breeding, 24, 361-374. https://doi.org/10.1007/s11032-009-9297-4
Orłowska, E., Fiil, A., Kirk, H.G., Llorente, B. and Cvitanich, C. (2012) Differential Gene Induction in Resistant and Susceptible Potato Cultivars at Early Stages of Infection by Phytophthora infestans. Plant Cell Reports, 31, 187-203. https://doi.org/10.1007/s00299-011-1155-2
Legavre, T., Ducamp, M., Sabau, X., Argout, X., Fouet, O., Dedieu, F., SurujdeoMaharaj, S., Garcia, D., Paulin, D. and Lanaud, C. (2015) Identification of Theobroma cacao Genes Differentially Expressed during Phytophthora megakarya Infection. Physiological and Molecular Plant Pathology, 92, 1-13. https://doi.org/10.1016/j.pmpp.2015.08.005
Bailey, B.A., Bae, H., Strem, M.D., De Mayolo, G.A., Guiltinan, M.J., Verica, J.A., Maximova, S.N. and Bowers, J.H. (2005) Developmental Expression of Stress Response Genes in Theobroma cacao Leaves and Their Response to Nep1 Treatment and a Compatible Infection by Phytophthora megakarya. Plant Physiology and Biochemistry, 43, 611-622. https://doi.org/10.1016/j.plaphy.2005.04.006
Chandrasekaran, M. and Chun, S.C. (2016) Expression of PR-Protein Genes and Induction of Defense-Related Enzymes by Bacillus subtilis CBR05 in Tomato (Solanum lycopersicum) Plants Challenged with Erwinia carotovora subsp. carotovora. Bioscience, Biotechnology, and Biochemistry, 80, 2277-2283. https://doi.org/10.1080/09168451.2016.1206811
Chowdhury, S.P., Hartmann, A., Gao, X. and Borriss, R. (2015) Biocontrol Mechanism by Root-Associated Bacillus amyloliquefaciens FZB42—A Review. Frontiers in Microbiology, 6, Article No. 780. https://doi.org/10.3389/fmicb.2015.00780
Conrath, U. (2011) Molecular Aspects of Defence Priming. Trends in Plant Science, 16, 524-531. https://doi.org/10.1016/j.tplants.2011.06.004
Macagnan, D., Romeiro, R.D.S., de Souza, J.T. and Pomella, A.W. (2006) Isolation of Actinomycetes and Endospore-Forming Bacteria from the Cacao Pod Surface and Their Antagonistic Activity against the Witches’ Broom TND Black Pod Pathogens. Phytoparasitica, 34, 122-132. https://doi.org/10.1007/BF02981312
Palaniyandi, S.A., Yang, S.H., Zhang, L. and Suh, J.W. (2013) Effects of Actinobacteria on Plant Disease Suppression and Growth Promotion. Applied Microbiology and Biotechnology, 97, 9621-9636. https://doi.org/10.1007/s00253-013-5206-1
Keswani, C., Bisen, K., Singh, V., Sarma, B.K. and Singh, H.B. (2016) Formulation Technology of Biocontrol Agents: Present Status and Future Prospects. In: Arora, N., Mehnaz, S. and Balestrini, R., Eds., Bioformulations: For Sustainable Agriculture, Springer, New Delhi, 35-52. https://doi.org/10.1007/978-81-322-2779-3_2
Tondje, P., Roberts, D.P., Bon, M., Widmer, T., Samuels, G.J., Ismaiel, A.A., Begoude, A.D., Tchana, T., Nyemb-Tshomb, E., Ndoumbe-Nkeng, M., Bateman, R., Fontem, D. and Hebbar, K.P. (2007) Isolation and Identification of Mycoparasitic Isolates of Trichoderma asperellum with Potential for Suppression of Black Pod Disease of Cacao in Cameroon. Biological Control, 43, 202-212. https://doi.org/10.1016/j.biocontrol.2007.08.004
Nyassé, S., Cilas, C., Herail, C. and Blaha, G. (1995) Leaf Inoculation as an Early Screening Test for Cocoa (Theobroma cacao L.) Resistance to Phytophthora Black Pod Disease. Crop Protection, 14, 657-663. https://doi.org/10.1016/0261-2194(95)00054-2
Paulin, D., Ducamp, M. and Lachenaud, P. (2008) New Sources of Resistance to Phytophthora megakarya Identified in Wild Cocoa Tree Populations of French Guiana. Crop Protection, 27, 1143-1147. https://doi.org/10.1016/j.cropro.2008.01.004
Boudjeko, T., Djocgoue, P.F., Nankeu, J.D., Mbouobda, H.D., Omokolo, D.N. and El Hadrami, I. (2007) Luteolin Derivatives and Heritability of Resistance to Phytophthora megakarya in Theobroma cacao. Australasian Plant Pathology, 36, 56-61. https://doi.org/10.1071/AP06083
Marigo, G. (1973) On a Fractionation Method and Estimation of the Phenolic Compounds in Plants. Analysis, 2, 106-110.
Kramling, T.E. and Singleton, V.L. (1969) An Estimate of the Nonflavonoid Phenols in Wines. American Journal of Enology and Viticulture, 20, 86-92.
Téné, T.P.M., Dzelamonyuy, A., Omokolo, N.D. and Boudjeko, T. (2019) Enhancement of Theobroma cacao Seedling Growth and Tolerance to Phytophthora megakarya by Heat-Treated Oyster Shell Powder. American Journal of Plant Sciences, 10, 578-594. http://doi.org/10.4236/ajps.2019.104042
Leelasuphakul, W., Sivanunsakul, P. and Phongpaichit, S. (2006) Purification, Characterization, and Synergistic Activity of β-1, 3-Glucanase and Antibiotic Extract from an Antagonistic Bacillus subtilis NSRS 89-24 against Rice Blast and Sheath Blight. Enzyme and Microbial Technology, 38, 990-997. https://doi.org/10.1016/j.enzmictec.2005.08.030
Pirovani, C.P., Carvalho, H.A.S., Machado, R.C.R., Gomes, D.S., Alvim, F.C., Pomella, A.W.V., Gramacho, K.R., Cascardo, J.C.M., Pereira, G.A.G. and Micheli, F. (2008) Protein Extraction for Proteome Analysis from Cacao Leaves and Meristems, Organs Infected by Moniliophthora perniciosa, the Causal Agent of the Witches’ Broom Disease. Electrophoresis, 29, 2391-2401. https://doi.org/10.1002/elps.200700743
Schmittgen, T.D. and Livak, K.J. (2008) Analyzing Real-Time PCR Data by the Comparative CT Method. Nature Protocols, 3, 1101-1108. https://doi.org/10.1038/nprot.2008.73
Verhagen, B.W.M., Trotel-Aziz, P., Couderchet, M., Höfte, M. and Aziz, A. (2010) Pseudomonas Spp.-Induced Systemic Resistance to Botrytis cinerea Is Associated with Induction and Priming of Defence Responses in Grapevine. Journal of Experimental Botany, 61, 249-260. https://doi.org/10.1093/jxb/erp295
Zhang,Y., Smith, P., Maximova, S.N. and Guiltinan, M.J. (2015) Application of Glycerol as a Foliar Sprays Activates the Defence Response and Enhances Disease Resistance of Theobroma cacao. Molecular Plant Pathology, 16, 27-37. https://doi.org/10.1111/mpp.12158
Liu, Y., Shi, Z., Maximova, S.N., Payne, M.J. and Guiltinan, M.J. (2015) Tc-MYBPA Is an Arabidopsis TT2-Like Transcription Factor and Functions in the Regulation of Proanthocyanidin Synthesis in Theobroma cacao. BMC Plant Biology, 15, Article No. 160. https://doi.org/10.1186/s12870-015-0529-y
Thomas, B.R., Inouhe, M., Simmons, C.R. and Nevins, D.J. (2000) Endo-1,3;1,4-Beta-Glucanase from Coleoptiles of Rice and Maize: Role in the Regulation of Plant Growth. International Journal of Biological Macromolecules, 27, 145-149. https://doi.org/10.1016/S0141-8130(00)00110-0
Li, J. and Liu, J. (2003) Cotton Gene Encoding a New Class of Chitinase Is Inducible by Salicylic Acid. Acta Botanica Sinica, 45, 1489-1496. https://doi.org/10.1080/07352689.2011.616043
Terrier, N., Torregrosa, L., Ageorges, A., Vialet, S., Verriès, C., Cheynier, V. and Romieu, C. (2008) Ectopic Expression of Vvmybpa2 Promotes Proanthocyanidin Biosynthesis in Grapevine and Suggests Additional Targets in the Pathway. Plant Physiology, 149, 1028-1041. https://doi.org/10.1104/pp.108.131862
Wright, D.C., Park, W.D., Leopold, N.R., Hasegawa, P.M. and Janick, J. (1982) Accumulation of Lipids, Proteins, Alkaloids, and Anthocyanins during Embryo Development in Vivo of Theobroma cacao L. Journal of the American Oil Chemists’ Society, 59, 475-479. https://doi.org/10.1007/BF02636146
Raffaele, S., Rivas, S. and Roby, D. (2006) An Essential Role for Salicylic Acid in Atmyb30-Mediated Control of the Hypersensitive Cell Death Program in Arabidopsis. FEBS Letters, 580, 3498-3504. https://doi.org/10.1016/j.febslet.2006.05.027
Vallad, G.E. and Goodman, R.M. (2004) Systemic Acquired Resistance and Induced Systemic Resistance in Conventional Agriculture. Crop Science, 44, 1920-1934. https://doi.org/10.2135/cropsci2004.1920
de Sousa, W.N., Brito, N.F., Felsemburgh, C.A., Vieira, T.A. and Lustosa, D.C. (2021) Evaluation of Trichoderma spp. Isolates in Cocoa Seed Treatment and Seedling Production. Plants, 10, Article No. 1964. https://doi.org/10.3390/plants10091964
Zamioudis, C. and Pieterse, C.M.J. (2012) Modulation of Host Immunity by Beneficial Microbes. Molecular Plant-Microbe Interactions, 25, 139-150. https://doi.org/10.1094/MPMI-06-11-0179