Endophytic fungi as potential biocontrol agents of Phytophthora palmivora in the cocoa plant
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Abstract. Simamora AV, Hahuly MV, Henuk JBD. 2021. Endophytic fungi as potential biocontrol agents of Phytophthora palmivora in the cocoa plant. Biodiversitas 22: 2601-2609. In Indonesia, the cocoa tree is one of the essential cultivation crops for farmers. Despite the importance of cocoa cultivation in Indonesia's economy, the productivity of this crop has declined. Cocoa black pod disease caused by Phytophthora palmivora (Butl.) is one of the most severe diseases affecting this crop worldwide, with average annual losses above 40%. Instead of using manufactured chemicals, biological control is an effective and eco-friendly alternative control measure against plant pathogens. This work aimed to assess the potential of endophytic fungi isolated from healthy cocoa pods to control Phytophthora palmivora in vitro and in vivo. Endophytic fungal isolates were classified based on the morphological characteristics of their cultures and reproductive structures. All isolates found were tested to inhibit P. palmivora in the dual culture method, and the best 10 isolates were continued for detached pod assay. Then, the best five isolates (Aspergillus4, Aspergillus5, Aspergillus6, Fusarium6, Ramichloridium sp.) were evaluated for their capability to reduce P. palmivora in cocoa seedlings and in the field plants. Aspergillus, Fusarium, and Ramichloridium showed maximum activity against P. palmivora in dual culture, pod, and seedling assays. Nevertheless, when all these five isolates were applied in the field, they did not suppress the disease development.
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References
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Busby PE, Ridout M, Newcombe G. 2016. Fungal endophytes: modifiers of plant disease. Plant. Mpl. Biol. 90: 645-655.
Chitnis VR, Suryanarayanan TS, Nataraja KN, Prasad R, Oelmüller R, Shaanker RU. 2020. Fungal endophytesw-mediated crop improvement: the way ahead. Frontiers in Plant Science 11:561007. DOI: 10.3389/fpls.2020.561007.
De Silva N, Brooks S, Lumyong S, Hyde KD. 2019. Use of endophytes as biocontrol agents. Fungal Biology Review 33: 133-148.
Doilom M, Manawasinghe IS, Jeewon R, Jayawardena RS , Tibpromma S, Hongsanan S, Meepol W, Lumyong S, Jones EBG, Hyde KD. 2017 – Can ITS sequence data identify fungal endophytes from cultures? A case study from Rhizophora apiculata. Mycosphere 8:1869–1892.
Fadiji AE, Babalola OO. 2020a. Elucidating mechanisms of endophytes used in plant protection and other bioactivities with multifunctional prospects. Frontiers in Bioengineering and Biotechnology. DOI: 10.3389/fbioe.2020.00467.
Fadiji AE, Babalola OO. 2020b. Exploring the potentialities of beneficial endophytes for improved plant growth. Saudi Journal of Biological Sciences 27: 3622-3633.
Fitriarni D, Kasiamdari RS. 2018 Isolation and identification of endophytic fungi from leave and stem of Calopogonium mucunoides. Journal of Tropical Biodiversity and Biotechnology 3: 30-36.
Gassa A, Mulia S, Yumarto, Junaid M. 2016. Phytophthora black pod disease of cocoa caused by Phytophthora palmivora: development of bio-fungicidal package in controlling the disease and the vector by food bait. Journal of Chemical and Pharmaceutical Research 8(6): 129-125.
Gautam AK, Kant M, Thakur Y. 2013. Isolation of endophytic fungi from Cannabis sativa and study their antifungal potential. Arch Phytopathol Plant Protect 46:627–635.
Gouda SG, Das G, Sen SK, Shin HS, Patra JK. 2016. Endophytes: a treasure house of bioactive compounds of medicinal importance. Frontiers in Mycrobiologi 7(148). DOI: 10.3389/fmicb.2016.01538.
Hakkar AK, Rosmana A, MD Rahim MD. 2014. Pengendalian Penyakit Busuk Buah Phytophthora pada kakao dengan Jamur Endofit Trichoderma asperellum. Jurnal Fitopatologi Indonesia 10(5): 139-144. [Indonesian].
Hanada R, Pomella AWW, Costa HS, Bezerra JL, Loguercio LL, Pereira HS. 2010. Endophytic fungal diversity in Theobroma cacao (cacao) and T. grandiflorum (cupuacu) trees and their potential for growth promotion and biocontrol of black-pod disease. Fungal Biology 114: 901-910.
Hanada R, Pomella AWW, Soberanis W, Loguercio LL, Pareira JO. 2009. Biocontrol potential of Trichoderma martiale against the black-pod disease (Phytophthora palmivora) of cacao. Biological Control 50: 143-149.
Hardoim PR, van Overbeek LS, Berg G, Pirttilä AM, Compant S, Campisano A. et al. 2015. The hidden world within plants: ecological and evolutionary consideartions for defining funtioning of microbial endophytes. Microbiol. Mol. Biol. Rev. 79:293-320.
Harni R, Taufiq E, Amaria W. 2014. Pengaruh formula fungisida nabati minyak cengkeh dan serai wangi terhadap penyakit busuk buah kakao. Jurnal Tanaman Industri dan Penyegar1(1): 41–48. Doi: http://dx.doi.org/ 10.21082/jtidp. [Indonesian].
Jain P. Pundir RK. 2017. Potential role of endophytes in sustainable agriculture-recent development and future prospects. In; K. Maheshwari (ed.), Endophytes: Biology and biotechnology, sustainable development and biodiversity 15, pp. 145-160. Swizterland: Springer International Publishing AG. DOI: 10.1007/978-3-319-66541-1_1.
Khan AL, Hamayun M, Kim YH, Kang SM, Lee IJ. 2011. Ameliorative symbiosis of endophyte (Penicillium funiculosum LHL06) under salt stress elevated plant growth of Glycine max L. Plant Physiol Biochem 49:852–861.
Kirschner R, Piepenbring M. 2014. New records of three Ramichloridium species on banana leaves in Panama and Taiwan. Mycoscience 55(4): 260-267.
Lugtenberg BJJ, Caradus JR, Johnson LJ. 2016. Fungal endophytes for sustainable crop production. FEMS Microbiology Ecology 92. DOI: 10.1093/femsec/fiw194.
Mejía LC, Rojas EI, Maynard Z, Van Bael S, Arnold AE, Hebbar P, Samuels GJ, Robbins N, Herre EA. 2008. Endophytic fungi as biocontrol agents of Theobroma cacao pathogens. Biological Control 46(1): 4-14.
Mmbaga MT, Gurung S, Maheshwari A. 2018. Screening of plant endophytes as biocontrol agents against root rot pathogens of pepper (Capsicum annum L.). Journal of Plant Pathology & Microbiology 9:3. DOI: 10.4172/2157-7471.1000435.
Myrchiang P, Dkhar MS, Haoboam RD. 2014. Studies on fungi associated with medicinally important aromatic plant Artemisia nilagirica (C.B. Clarke) Pamp. and their antagonistic activity against Phytophthora infestans. Journal of Advanced Laboratory Research in Biology 5(4): 112-119.
Nath R, Sharma GD, Barooah M. 2012. Efficiency of tricalcium phosphate solubilization by two different endophytic Penicillium sp. isolated from tea (Camellia sinensis L.). European. J Exp Biol 2(4):1354–1358.
Nur Amin. 2013. Investigation of culture filtrate of endophytic fungi Nigrospora sp. isolate RS 10 in different concentrations towards root-knot nematode Meloydogine spp. Indian Journal of Science and Technology 6(9): 5177-5181.
Nur Amin, Muslim S, Junaid M, Baco MS. 2014. Isolation and identification of endophytic fungi from cocoa plant resistance VSD M.05 and cocoa plant susceptible VSD M.01 in South Sulawesi, Indonesia. Int. J.Curr. Microbiol. App. Sci. 3(2): 459-467.
Nur Amin, Muslim S, Asman, Ryan, Danial R. 2015. Investigation of Fungi Towwards Vascular Streak Dieback Oncobasidium theobromae of seedling od cocoa plant. Journal of Applied Biological Sciences 9(2): 86-89.
Olokkaran R, Mathew S, Alakkatt J, Sunny SK. 2019. Isolation and morphological identification of aflatoxigenic Aspergillus flavus in finishef feed for farmed Nile tilapia, Oreochromis niloticus (Linnaeus, 1758). International Journal of Fisheries and Aquatic Studies 7(6): 280-286.
Perrine-Walker F. 2020. Phytophthora palmivora-Cocoa interaction. Journal of Fungi 6, 167. DOI: 10.3390/jof6030167.
Praseptiangga D, Guevara Zambrano JM, Sanjaya AP, Muhammad DRA. 2020. Challenges in the development of the cocoa and chocolate industry in Indonesia: A case study in Madiun, East Java. AIMS Agriculture and Food, 5(4): 920–937. DOI: 10.3934/agrfood.2020.4.920.
Rashmi M, Kushveer JS, Sarma VV. 2019. A worldwide list of endophytic fungi with notes on ecology and diversity. Mycosphere 10(1): 798-1079.
Rubiyo, Amaria D. 2013. Ketahanan Tanaman Kakao Terhadap Penyakit busuk Buah (Phytophthora palmivora Bult.). Balai Penelitian Tanaman Industri dan Penyegar 12 : 25-36. [Indonesian].
Sella PG, Fardah. 2020. Indonesia earns US$549 million from processed cocoa exports. https://en.antaranews.com/news/158489/indonesia-earns-us549-million-from-processed-cocoa-exports.
Sreja K, Anandaraj M, Bhai RS. 2016. In vitro evaluation of fungal endophytes of black pepper against Phytophthora capsici and Radopholus similis. Journal of Spices and Aromatic Crops 25(2):113-122.
Sriwati R, R Muarif. 2012. Characteristic symptoms of Phytophthora palmivora on cocoa leaves. Jurnal Natural 12(2) : 30-34. [Indonesian].
Sriwati R, Melnick RL, Muarif R, Strem MD, Samuels GD, Bailey BA. 2015. Trichoderma from Aceh Sumatra reduce Phytophthora lesions on pods and cacao seedlings. Biological Control 89: 33-41.
Sutton BC. 2014. Fungi. Classification of the Deuteromycetes.Encyclopedia of Food Microbiology. 2nd edition. https://doi.org/10.1016/B978-0-12-384730-0.00140-3.
Villamixar-Gallardo RA, Ortiz-Rodriguez OO, Escobar JW. 2017. Symbiotic and endophytic fungi as biocontrols against cocoa (Theobroma cacao L.) Phytopathogens. Summa Phytopathologica 43(2): 87-93.
Vyas P, Bansal A. 2018. Fungal endophytes: role in sustainable agriculture. In: Gehlot, Praveen, Singh, Joginder (eds). Fungi and their Role in Agriculture. Springer Singapore. DOI: 10.1007/978-981-13-0393-7.
Wardhany M, Adzim F. 2018. Determinant of Cocoa Export in Indonesia. Economics Development Analysis Journal 7(3): 286-293.
Watanabe T. 2010. Pictorial atlas of soil and seed fungi. Morphologies and cultured fungi and key to species. 3rd ed. CRC Press Boca Raton.
Wei F, Zhang Y, Shi Y, Feng H, Zhao L, Feng Z, Zhu H. 2019. Evaluation of the biocontrol potential of endophytic fungus Fusarium solani CEF559 against Verticillium dahliae in cotton plant. Hindawi. Biomed Research International, article ID 3187943.
Witjaksono J, Asmin. 2016. Cocoa Farming System in Indonesia and Its Sustainability Under Climate Change. Agriculture, Forestry and Fisheries 5(5): 170-180. Doi: 10.11648/j.aff.20160505.15.
Xie L, Usui E, Narisawa K. 2016. A endophytic fungus, Ramichloridium cerophilum, promotes growth of a non-mycorrhizal plant, Chinese cabbage. African Journal of Biotechnology 15(25): 1299-1305. DOI: 10.5897/AJB2016.15398.
Zheng H, Zefen Yu, Jianping Xu, Castañeda-Ruiz RF, Min Qiao. 2020. Ramichloridium endophyticum sp. nov., a novel species of endophytic fungus from Potamogeton pectinatus. International Journal of Systematic and Evolutionary Microbiology. DOI: 10.1099/ijsem.0.004190.
Abo Nouh FA 2019. Endophytic fungi for sustainable agriculture. Microbial Biosystems 4(1): 31-44.
Barnett HL, Hunter BB. 1998. Illustrated genera of imperfect fungi. 4th ed. APS Press, St. Paul. p. 218.
Busby PE, Ridout M, Newcombe G. 2016. Fungal endophytes: modifiers of plant disease. Plant. Mpl. Biol. 90: 645-655.
Chitnis VR, Suryanarayanan TS, Nataraja KN, Prasad R, Oelmüller R, Shaanker RU. 2020. Fungal endophytesw-mediated crop improvement: the way ahead. Frontiers in Plant Science 11:561007. DOI: 10.3389/fpls.2020.561007.
De Silva N, Brooks S, Lumyong S, Hyde KD. 2019. Use of endophytes as biocontrol agents. Fungal Biology Review 33: 133-148.
Doilom M, Manawasinghe IS, Jeewon R, Jayawardena RS , Tibpromma S, Hongsanan S, Meepol W, Lumyong S, Jones EBG, Hyde KD. 2017 – Can ITS sequence data identify fungal endophytes from cultures? A case study from Rhizophora apiculata. Mycosphere 8:1869–1892.
Fadiji AE, Babalola OO. 2020a. Elucidating mechanisms of endophytes used in plant protection and other bioactivities with multifunctional prospects. Frontiers in Bioengineering and Biotechnology. DOI: 10.3389/fbioe.2020.00467.
Fadiji AE, Babalola OO. 2020b. Exploring the potentialities of beneficial endophytes for improved plant growth. Saudi Journal of Biological Sciences 27: 3622-3633.
Fitriarni D, Kasiamdari RS. 2018 Isolation and identification of endophytic fungi from leave and stem of Calopogonium mucunoides. Journal of Tropical Biodiversity and Biotechnology 3: 30-36.
Gassa A, Mulia S, Yumarto, Junaid M. 2016. Phytophthora black pod disease of cocoa caused by Phytophthora palmivora: development of bio-fungicidal package in controlling the disease and the vector by food bait. Journal of Chemical and Pharmaceutical Research 8(6): 129-125.
Gautam AK, Kant M, Thakur Y. 2013. Isolation of endophytic fungi from Cannabis sativa and study their antifungal potential. Arch Phytopathol Plant Protect 46:627–635.
Gouda SG, Das G, Sen SK, Shin HS, Patra JK. 2016. Endophytes: a treasure house of bioactive compounds of medicinal importance. Frontiers in Mycrobiologi 7(148). DOI: 10.3389/fmicb.2016.01538.
Hakkar AK, Rosmana A, MD Rahim MD. 2014. Pengendalian Penyakit Busuk Buah Phytophthora pada kakao dengan Jamur Endofit Trichoderma asperellum. Jurnal Fitopatologi Indonesia 10(5): 139-144. [Indonesian].
Hanada R, Pomella AWW, Costa HS, Bezerra JL, Loguercio LL, Pereira HS. 2010. Endophytic fungal diversity in Theobroma cacao (cacao) and T. grandiflorum (cupuacu) trees and their potential for growth promotion and biocontrol of black-pod disease. Fungal Biology 114: 901-910.
Hanada R, Pomella AWW, Soberanis W, Loguercio LL, Pareira JO. 2009. Biocontrol potential of Trichoderma martiale against the black-pod disease (Phytophthora palmivora) of cacao. Biological Control 50: 143-149.
Hardoim PR, van Overbeek LS, Berg G, Pirttilä AM, Compant S, Campisano A. et al. 2015. The hidden world within plants: ecological and evolutionary consideartions for defining funtioning of microbial endophytes. Microbiol. Mol. Biol. Rev. 79:293-320.
Harni R, Taufiq E, Amaria W. 2014. Pengaruh formula fungisida nabati minyak cengkeh dan serai wangi terhadap penyakit busuk buah kakao. Jurnal Tanaman Industri dan Penyegar1(1): 41–48. Doi: http://dx.doi.org/ 10.21082/jtidp. [Indonesian].
Jain P. Pundir RK. 2017. Potential role of endophytes in sustainable agriculture-recent development and future prospects. In; K. Maheshwari (ed.), Endophytes: Biology and biotechnology, sustainable development and biodiversity 15, pp. 145-160. Swizterland: Springer International Publishing AG. DOI: 10.1007/978-3-319-66541-1_1.
Khan AL, Hamayun M, Kim YH, Kang SM, Lee IJ. 2011. Ameliorative symbiosis of endophyte (Penicillium funiculosum LHL06) under salt stress elevated plant growth of Glycine max L. Plant Physiol Biochem 49:852–861.
Kirschner R, Piepenbring M. 2014. New records of three Ramichloridium species on banana leaves in Panama and Taiwan. Mycoscience 55(4): 260-267.
Lugtenberg BJJ, Caradus JR, Johnson LJ. 2016. Fungal endophytes for sustainable crop production. FEMS Microbiology Ecology 92. DOI: 10.1093/femsec/fiw194.
Mejía LC, Rojas EI, Maynard Z, Van Bael S, Arnold AE, Hebbar P, Samuels GJ, Robbins N, Herre EA. 2008. Endophytic fungi as biocontrol agents of Theobroma cacao pathogens. Biological Control 46(1): 4-14.
Mmbaga MT, Gurung S, Maheshwari A. 2018. Screening of plant endophytes as biocontrol agents against root rot pathogens of pepper (Capsicum annum L.). Journal of Plant Pathology & Microbiology 9:3. DOI: 10.4172/2157-7471.1000435.
Myrchiang P, Dkhar MS, Haoboam RD. 2014. Studies on fungi associated with medicinally important aromatic plant Artemisia nilagirica (C.B. Clarke) Pamp. and their antagonistic activity against Phytophthora infestans. Journal of Advanced Laboratory Research in Biology 5(4): 112-119.
Nath R, Sharma GD, Barooah M. 2012. Efficiency of tricalcium phosphate solubilization by two different endophytic Penicillium sp. isolated from tea (Camellia sinensis L.). European. J Exp Biol 2(4):1354–1358.
Nur Amin. 2013. Investigation of culture filtrate of endophytic fungi Nigrospora sp. isolate RS 10 in different concentrations towards root-knot nematode Meloydogine spp. Indian Journal of Science and Technology 6(9): 5177-5181.
Nur Amin, Muslim S, Junaid M, Baco MS. 2014. Isolation and identification of endophytic fungi from cocoa plant resistance VSD M.05 and cocoa plant susceptible VSD M.01 in South Sulawesi, Indonesia. Int. J.Curr. Microbiol. App. Sci. 3(2): 459-467.
Nur Amin, Muslim S, Asman, Ryan, Danial R. 2015. Investigation of Fungi Towwards Vascular Streak Dieback Oncobasidium theobromae of seedling od cocoa plant. Journal of Applied Biological Sciences 9(2): 86-89.
Olokkaran R, Mathew S, Alakkatt J, Sunny SK. 2019. Isolation and morphological identification of aflatoxigenic Aspergillus flavus in finishef feed for farmed Nile tilapia, Oreochromis niloticus (Linnaeus, 1758). International Journal of Fisheries and Aquatic Studies 7(6): 280-286.
Perrine-Walker F. 2020. Phytophthora palmivora-Cocoa interaction. Journal of Fungi 6, 167. DOI: 10.3390/jof6030167.
Praseptiangga D, Guevara Zambrano JM, Sanjaya AP, Muhammad DRA. 2020. Challenges in the development of the cocoa and chocolate industry in Indonesia: A case study in Madiun, East Java. AIMS Agriculture and Food, 5(4): 920–937. DOI: 10.3934/agrfood.2020.4.920.
Rashmi M, Kushveer JS, Sarma VV. 2019. A worldwide list of endophytic fungi with notes on ecology and diversity. Mycosphere 10(1): 798-1079.
Rubiyo, Amaria D. 2013. Ketahanan Tanaman Kakao Terhadap Penyakit busuk Buah (Phytophthora palmivora Bult.). Balai Penelitian Tanaman Industri dan Penyegar 12 : 25-36. [Indonesian].
Sella PG, Fardah. 2020. Indonesia earns US$549 million from processed cocoa exports. https://en.antaranews.com/news/158489/indonesia-earns-us549-million-from-processed-cocoa-exports.
Sreja K, Anandaraj M, Bhai RS. 2016. In vitro evaluation of fungal endophytes of black pepper against Phytophthora capsici and Radopholus similis. Journal of Spices and Aromatic Crops 25(2):113-122.
Sriwati R, R Muarif. 2012. Characteristic symptoms of Phytophthora palmivora on cocoa leaves. Jurnal Natural 12(2) : 30-34. [Indonesian].
Sriwati R, Melnick RL, Muarif R, Strem MD, Samuels GD, Bailey BA. 2015. Trichoderma from Aceh Sumatra reduce Phytophthora lesions on pods and cacao seedlings. Biological Control 89: 33-41.
Sutton BC. 2014. Fungi. Classification of the Deuteromycetes.Encyclopedia of Food Microbiology. 2nd edition. https://doi.org/10.1016/B978-0-12-384730-0.00140-3.
Villamixar-Gallardo RA, Ortiz-Rodriguez OO, Escobar JW. 2017. Symbiotic and endophytic fungi as biocontrols against cocoa (Theobroma cacao L.) Phytopathogens. Summa Phytopathologica 43(2): 87-93.
Vyas P, Bansal A. 2018. Fungal endophytes: role in sustainable agriculture. In: Gehlot, Praveen, Singh, Joginder (eds). Fungi and their Role in Agriculture. Springer Singapore. DOI: 10.1007/978-981-13-0393-7.
Wardhany M, Adzim F. 2018. Determinant of Cocoa Export in Indonesia. Economics Development Analysis Journal 7(3): 286-293.
Watanabe T. 2010. Pictorial atlas of soil and seed fungi. Morphologies and cultured fungi and key to species. 3rd ed. CRC Press Boca Raton.
Wei F, Zhang Y, Shi Y, Feng H, Zhao L, Feng Z, Zhu H. 2019. Evaluation of the biocontrol potential of endophytic fungus Fusarium solani CEF559 against Verticillium dahliae in cotton plant. Hindawi. Biomed Research International, article ID 3187943.
Witjaksono J, Asmin. 2016. Cocoa Farming System in Indonesia and Its Sustainability Under Climate Change. Agriculture, Forestry and Fisheries 5(5): 170-180. Doi: 10.11648/j.aff.20160505.15.
Xie L, Usui E, Narisawa K. 2016. A endophytic fungus, Ramichloridium cerophilum, promotes growth of a non-mycorrhizal plant, Chinese cabbage. African Journal of Biotechnology 15(25): 1299-1305. DOI: 10.5897/AJB2016.15398.
Zheng H, Zefen Yu, Jianping Xu, Castañeda-Ruiz RF, Min Qiao. 2020. Ramichloridium endophyticum sp. nov., a novel species of endophytic fungus from Potamogeton pectinatus. International Journal of Systematic and Evolutionary Microbiology. DOI: 10.1099/ijsem.0.004190.