Epiphytic yeasts from Piperaceae as biocontrol agents for foot rot of black pepper caused by Phytophthora capsici
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Abstract. Safitri D, Wiyono S, Soekarno BPW, Achmad. 2021. Epiphytic yeasts from Piperaceae as biocontrol agents for foot rot of black pepper caused by Phytophthora capsici. Biodiversitas 22: 1895-1901. Phytophthora capsici, is a causative agent of footrot disease, is the primary pathogen in black pepper (Piper nigrum L.). Footrot disease may cause a loss of 67% black pepper production. Yeast as a biocontrol is a promising technique to control foot rot disease. This study aimed to isolate, characterize yeasts from several species of Piper and determine their effectiveness against foot rot disease. Epiphytic yeasts were isolated from roots, stems, and leaves of Piper nigrum, P. retrofractum, and P. ornatum. The epiphytic yeasts were tested for their antagonistic activity against P. capsici as biocontrol agents. The antagonistic activity was observed through antibiosis mechanisms, volatile organic compound production, hyperparasitism, and the production of ?1-1,3 glucanase enzyme. A total of 48 epiphytic yeasts were isolated from Piper species. There were five isolates with high antibiosis activity in vitro, i.e. EPT23, E62, EPT63, EPT69, EPT70, and identified through molecular identification as Rhodotorula glutinis, Cryptococcus magnus, Filobasidium globisporum, R. mucilaginosa, H. oryzae, respectively. The selected yeast showed biocontrol activity against foot rot disease ranged from 56.7 to 80.0%.
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References
REFERENCES
Adam DJ. 2004. Fungal cell wall chitinases and glucanases [review]. Microbiol. 150: 2029-2035.
Agrios GN. 2005. Plant Pathology 4th ed. Academic Press, Toronto.
Altschul S, Gish W, Miller W, Myers E, Lipman D. 1990. Basic local alignment search tool. Journal of Molecular Biology. 215(3):403–410.
Aravind R, Kumar A, Eapen SJ, Ramana. 2009. Endophytic bacterial flora in root and stem tissues of black pepper (Piper nigrum L.) genotype: Isolation, identification and evaluation against Phytophthora capsici. J. Microbiol. 48(1):58-64.
Assis SMP, Mariano RLR. 1999. Antagonisme of yeast to Xanthomonas campestris pv. campestris on cabbage phylloplane in field. Rev Microbiol. 30(3):191-195.
Buzzini P, Gasparetti C, Turchetti B, Cramarossa M, Vaughan-Martini A, Martini A, Pagnoni UM, Feroti L. 2005. Production of volatile organic compounds ( VOC) by yeasts isolated from the ascocarps of black (Tuber melanosporum Vitt.) and white (Tuber magnatum Pico.) truffles. Archives of Microbiology. 184:187–193.
Chan Z, Tian S. 2005. Interaction of antagonistic yeasts against postharvest pathogens of apple fruit and possible mode of action. Postharvest Biol Technol. 36:215–223.
[Ditjenbun] Direktorat Jenderal Tanaman Perkebunan. 2016. Statistik perkebunan lada Indonesia. [Internet]. [Dowloaded 2016 Oct 16]. Tersedia pada: http://ditjenbun. pertanian.go.id.
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Di Francesco A, Ugolini L, Lazzeri L, Mari M. 2014. Production of volatile organic compounds by Aureobasidium pullulans as a potential mechanism of action against postharvest fruit pathogens. Biological Control. doi:10.1016/j.biocontrol.2014.10.004.
Di-Francesco A, Roberti R, Martini C, Baraldi E, Mari M. 2015. Activities of Aureobasidium pullulans cell filtrates against Monilinia laxa of peaches. Microbiol Res. 181:61–67.
Di-Francesco A, Ugolini L, Lazzeri L, Mari M. 2014. Production of volatile organic compounds by Aureobasidium pullulans as a potential mechanism of action against postharvest fruit pathogens. Biol Control. Doi: https://doi.org/10.1016/j. biocontrol.2014.10.004.
Doxey AC, MW Yaish BA Moffatt, M Griffith and BJ MCConkey. 2007. Functional divergence in the Arabidopsis ?-1.3 glucanase gene familu inferred by phylogenetic reconstruction of expression state. Molecular Biology and Evolution.
Ginting C, Maryono T. 2012. Efikasi Trichoderma harzianum dengan berbagai bahan organik dalam pengendalian penyakit busuk pangkal batang pada lada. J. HPT Tropika. 11(2):147-156.
Hartati S. 2015. Khamir sebagai agens biokontrol antraknosa (Colletotrichum acutatum J.H. Simmonds) pada cabai pascapanen. [Dissertation]. Institut Pertanian Bogor. Bogor [Indonesian]
Huang, R., G.Q. Li, J. Zhang, L. Yang, H.J. Che, D.H. Jiang, & H.C. Huang. 2011. Disease Control and Pest Management Control of Postharvest Botrytis Fruit Rot of Strawberry by Volatile Organic Compounds of Candida intermedia. Phytopathology 101: 859?869.
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Inacio J, Ludwig W, Spencer-Martins I, Fonseca A. 2010. Assessment of phylloplane yeasts on selected Mediterranean plants by FISH with group and species-specific oligonucleotide probes. FEMS Microbiol Ecol. 71(1):61–72.
Isaeva OV, Glushakova AM, Garbuz SA, Kachalkin AV, Chernov IY. 2010. Endophytic yeast fungi in plant storage tissues. Biol Bull. 37(1):26-34.
Kachalkin AV, Yurkov AM. 2012. Yeast communities in Sphagnum phyllosphere along the temperature-moisture ecocline in the boreal forest-swamp ecosystem and description of Candida sphagnicola sp. nov. Antonie van Leeuwenhoek. 102 :29-43.
Kroon LPNM, Bakker FT, Van den Bosch GMB, Bonants PJM, Flier WG. 2004. Phylogenetic analysis of Phytophthora species base on mitochondrial and nuclear DNA sequence. Fungal Genetic and Biology. 41:766-782.
Lozano GL, Holt J, Ravel J, Rasko DA, Thomas MG, Handelsman J. 2016. Draft genome sequence of biocontrol agent Bacillus cereus UW85. Genome Announc 4:1-2
Manohara D, Wahyuno D, Noveriza R. 2005. Penyakit busuk pangkal batang lada dan strategi pengendaliannya. Perkembangan Teknologi Tanaman Rempah dan Obat. 17(2):41-51.
Manohara D. 2007. Bercak daun phytophthora sebagai sumber inokulum penyakit busuk pangkal batang lada (Piper nigrum). Bul. Littro. 18(2):177–187.
Nguyen VL. 2015. Spread of Phytophthora capsici in black pepper (Piper nigrum) in Vietnam. J Aut Scient ResPub Inc. 7(8):506-513.
Nishiyama Y, S Kuga and S sato. 2001. Role of the putative membrane-bound putative endo ? -D-1,4-glucanase KORINGAN in cell elongation and cellulose synthesis in Arabidobsis.Plant Cell Physiology. 42:251-263.
Sansone, G., Rezza, V. Calvente, D. Benuzzi. M.I.S. de Tosetti. 2005. Control of Boutrytis cinerea strains resistant of iprodione in apple with rhodotorulic acid and yeast. Post harvest biology and technology. 35:245-251.
Schaad NW, Jones JB, Chun W. 2001. Plant Pathogenic Bacteria 3rd Edition. Minnesota (US): American Phytophatological Society Press.
Scott JH, Schekman R. 1980. Lyticase: Endoglucanase and protease activities that act together in yeast cell lysis. J. Bacteriol. 142(2):414–423.
Shetty NP, Jensen JD, Knudsen A, Finnie C, Geshi N, Blennow A,Collinge DB, Jergensen HJL. 2009. Effects of ?-1,3-glucan from Septoria tritici on structural defence responses in wheat. J Experiment Bot. 60(15): 4287-4300.
Silva GAD, Bernardi TL, Schaker PDC, Menegotto M, Valente P. Rapid yeast DNA extraction by boiling and freeze-thawing without using chemical reagents and DNA purification. Brazilian Archives of Biology and Technology. 55(2):319-327.
Suardana IW, Utama IH, Wibowo WH. 2014. Identifikasi Escherichia coli O157:H7 dari feses ayam dan uji profil hemolisisnya pada media agar darah. J Med Vet Indones 8: 1-5.
Wahyuno, Manohara D, Ningsih SD, Setijono. 2010. Pengembangan varietas unggul lada tahan penyakit busuk pangkal batang yang disebabkan oleh Phytophthora capsici. Litbang Pertanian. 29(3):86-95.
Weller DM. 2007. Pseudomonas biocontrol agents of soilborne pathogens: Looking back over 30 years. Phytopathology 97:250-256.
Whipps JM, Hand P, Pink D, Bending GD. 2008. Phyllosphere microbiology with special reference to diversity and plant genotype. Appl Microbiology 105: 1744-1755.
Wilia, W., Widodo, S. Wiyono. 2012. Potensi khamir untuk mengendalikan penyakit antraknosa (Colletotrichum acutatum L.) pada tanaman cabai. Bioplantae. 1(4): 291-298.
Adam DJ. 2004. Fungal cell wall chitinases and glucanases [review]. Microbiol. 150: 2029-2035.
Agrios GN. 2005. Plant Pathology 4th ed. Academic Press, Toronto.
Altschul S, Gish W, Miller W, Myers E, Lipman D. 1990. Basic local alignment search tool. Journal of Molecular Biology. 215(3):403–410.
Aravind R, Kumar A, Eapen SJ, Ramana. 2009. Endophytic bacterial flora in root and stem tissues of black pepper (Piper nigrum L.) genotype: Isolation, identification and evaluation against Phytophthora capsici. J. Microbiol. 48(1):58-64.
Assis SMP, Mariano RLR. 1999. Antagonisme of yeast to Xanthomonas campestris pv. campestris on cabbage phylloplane in field. Rev Microbiol. 30(3):191-195.
Buzzini P, Gasparetti C, Turchetti B, Cramarossa M, Vaughan-Martini A, Martini A, Pagnoni UM, Feroti L. 2005. Production of volatile organic compounds ( VOC) by yeasts isolated from the ascocarps of black (Tuber melanosporum Vitt.) and white (Tuber magnatum Pico.) truffles. Archives of Microbiology. 184:187–193.
Chan Z, Tian S. 2005. Interaction of antagonistic yeasts against postharvest pathogens of apple fruit and possible mode of action. Postharvest Biol Technol. 36:215–223.
[Ditjenbun] Direktorat Jenderal Tanaman Perkebunan. 2016. Statistik perkebunan lada Indonesia. [Internet]. [Dowloaded 2016 Oct 16]. Tersedia pada: http://ditjenbun. pertanian.go.id.
[Ditjenbun] Direktorat Jenderal Tanaman Perkebunan. 2016. Statistik perkebunan lada Indonesia. [Internet]. [Downloaded 2016 Okt 16]. Tersedia pada: http://ditjenbun. pertanian.go.id.
Di Francesco A, Ugolini L, Lazzeri L, Mari M. 2014. Production of volatile organic compounds by Aureobasidium pullulans as a potential mechanism of action against postharvest fruit pathogens. Biological Control. doi:10.1016/j.biocontrol.2014.10.004.
Di-Francesco A, Roberti R, Martini C, Baraldi E, Mari M. 2015. Activities of Aureobasidium pullulans cell filtrates against Monilinia laxa of peaches. Microbiol Res. 181:61–67.
Di-Francesco A, Ugolini L, Lazzeri L, Mari M. 2014. Production of volatile organic compounds by Aureobasidium pullulans as a potential mechanism of action against postharvest fruit pathogens. Biol Control. Doi: https://doi.org/10.1016/j. biocontrol.2014.10.004.
Doxey AC, MW Yaish BA Moffatt, M Griffith and BJ MCConkey. 2007. Functional divergence in the Arabidopsis ?-1.3 glucanase gene familu inferred by phylogenetic reconstruction of expression state. Molecular Biology and Evolution.
Ginting C, Maryono T. 2012. Efikasi Trichoderma harzianum dengan berbagai bahan organik dalam pengendalian penyakit busuk pangkal batang pada lada. J. HPT Tropika. 11(2):147-156.
Hartati S. 2015. Khamir sebagai agens biokontrol antraknosa (Colletotrichum acutatum J.H. Simmonds) pada cabai pascapanen. [Dissertation]. Institut Pertanian Bogor. Bogor [Indonesian]
Huang, R., G.Q. Li, J. Zhang, L. Yang, H.J. Che, D.H. Jiang, & H.C. Huang. 2011. Disease Control and Pest Management Control of Postharvest Botrytis Fruit Rot of Strawberry by Volatile Organic Compounds of Candida intermedia. Phytopathology 101: 859?869.
M. Wisniewski, C. Wilson, S. Droby, E. Chalutz, A. El Ghaouth, and C. Stevens. 2007. Postharvest Biocontrol: New Concepts and Applications,” in Biological Control: a Global Perspective, C. Vincent, M. S. Goettel, G. Lazarovits. CAB International. 262-273.
Inacio J, Ludwig W, Spencer-Martins I, Fonseca A. 2010. Assessment of phylloplane yeasts on selected Mediterranean plants by FISH with group and species-specific oligonucleotide probes. FEMS Microbiol Ecol. 71(1):61–72.
Isaeva OV, Glushakova AM, Garbuz SA, Kachalkin AV, Chernov IY. 2010. Endophytic yeast fungi in plant storage tissues. Biol Bull. 37(1):26-34.
Kachalkin AV, Yurkov AM. 2012. Yeast communities in Sphagnum phyllosphere along the temperature-moisture ecocline in the boreal forest-swamp ecosystem and description of Candida sphagnicola sp. nov. Antonie van Leeuwenhoek. 102 :29-43.
Kroon LPNM, Bakker FT, Van den Bosch GMB, Bonants PJM, Flier WG. 2004. Phylogenetic analysis of Phytophthora species base on mitochondrial and nuclear DNA sequence. Fungal Genetic and Biology. 41:766-782.
Lozano GL, Holt J, Ravel J, Rasko DA, Thomas MG, Handelsman J. 2016. Draft genome sequence of biocontrol agent Bacillus cereus UW85. Genome Announc 4:1-2
Manohara D, Wahyuno D, Noveriza R. 2005. Penyakit busuk pangkal batang lada dan strategi pengendaliannya. Perkembangan Teknologi Tanaman Rempah dan Obat. 17(2):41-51.
Manohara D. 2007. Bercak daun phytophthora sebagai sumber inokulum penyakit busuk pangkal batang lada (Piper nigrum). Bul. Littro. 18(2):177–187.
Nguyen VL. 2015. Spread of Phytophthora capsici in black pepper (Piper nigrum) in Vietnam. J Aut Scient ResPub Inc. 7(8):506-513.
Nishiyama Y, S Kuga and S sato. 2001. Role of the putative membrane-bound putative endo ? -D-1,4-glucanase KORINGAN in cell elongation and cellulose synthesis in Arabidobsis.Plant Cell Physiology. 42:251-263.
Sansone, G., Rezza, V. Calvente, D. Benuzzi. M.I.S. de Tosetti. 2005. Control of Boutrytis cinerea strains resistant of iprodione in apple with rhodotorulic acid and yeast. Post harvest biology and technology. 35:245-251.
Schaad NW, Jones JB, Chun W. 2001. Plant Pathogenic Bacteria 3rd Edition. Minnesota (US): American Phytophatological Society Press.
Scott JH, Schekman R. 1980. Lyticase: Endoglucanase and protease activities that act together in yeast cell lysis. J. Bacteriol. 142(2):414–423.
Shetty NP, Jensen JD, Knudsen A, Finnie C, Geshi N, Blennow A,Collinge DB, Jergensen HJL. 2009. Effects of ?-1,3-glucan from Septoria tritici on structural defence responses in wheat. J Experiment Bot. 60(15): 4287-4300.
Silva GAD, Bernardi TL, Schaker PDC, Menegotto M, Valente P. Rapid yeast DNA extraction by boiling and freeze-thawing without using chemical reagents and DNA purification. Brazilian Archives of Biology and Technology. 55(2):319-327.
Suardana IW, Utama IH, Wibowo WH. 2014. Identifikasi Escherichia coli O157:H7 dari feses ayam dan uji profil hemolisisnya pada media agar darah. J Med Vet Indones 8: 1-5.
Wahyuno, Manohara D, Ningsih SD, Setijono. 2010. Pengembangan varietas unggul lada tahan penyakit busuk pangkal batang yang disebabkan oleh Phytophthora capsici. Litbang Pertanian. 29(3):86-95.
Weller DM. 2007. Pseudomonas biocontrol agents of soilborne pathogens: Looking back over 30 years. Phytopathology 97:250-256.
Whipps JM, Hand P, Pink D, Bending GD. 2008. Phyllosphere microbiology with special reference to diversity and plant genotype. Appl Microbiology 105: 1744-1755.
Wilia, W., Widodo, S. Wiyono. 2012. Potensi khamir untuk mengendalikan penyakit antraknosa (Colletotrichum acutatum L.) pada tanaman cabai. Bioplantae. 1(4): 291-298.
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