Molecular identification of endophytic fungi from torch ginger (Etlingera elatior) antagonist to phytopathogenic fungi
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Abstract. Lutfia A, Munir E, Yurnaliza. 2020. Molecular identification of endophytic fungi from torch ginger (Etlingera elatior) antagonist to phytopathogenic fungi. Biodiversitas 21: 2681-2689. Medicinal plants are valuable sources in exploration of endophytic microorganisms. The utilization of culturable endophytes, particularly endophytic fungi in pharmacological aspects has been reported in many literature. Zingiberaceae, being known as one of medicinal plant families, is commonly used in tropical countries, e.g Indonesia to treat health disorders and ailments. However, little information has been reported upon their associative endophytic fungi that may be used as biocontrol agents against phytopathogenic fungi. Efforts to elaborate on the symbiotic relationship between endophytic fungi and host to explain the antifungal ability from endophytes are presented in this study. Six fungal morphotypes were recovered from the rhizome fragment of torch ginger (Etlingera elatior (Jack) RM Smith) sampled from Sibayak forest, North Sumatra, Indonesia. All isolates displayed potential antifungal activities against Fusarium oxysporum, Ganoderma boninense, and Rigidoporus lignosus as representative phytopathogens in a dual culture plate assay. All fungal morphotypes were identified based on their 18S rDNA-ITS regions. Molecular identification revealed that most isolates were related to Trichoderma spp. while one isolate was identified as Pestaliotopsis sp. The endophytic assemblage of mostly Trichoderma strains in our study may reveal a mutual relationship of these soil fungi as root colonizer displaying biocontrol properties against phytopathogenic fungi to host.
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References
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J. Mol. Biol. 215: 403-410.
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
Anees M, Tronsmo A, Edel-Hermann V, Hjeljord LG, Heraud C, Steinberg C. 2010. Characterization of field isolates of Trichoderma antagonistic against Rhizoctonia solani. Fungal Biol 114 (9): 691-701.
Auliani A, Fitmawati F, Sofiyanti N. 2014. Studi etnobotani famili Zingiberaceae dalam kehidupan masyarakat lokal di Kecamatan Siak Hulu Kabupaten Kampar. Jurnal Online Mahasiswa FMIPA 1 (2): 526-533.
Bezerra JDP, Nascimento CCF, Barbosa RN, Silva DCV, Svedese VM, Silva-Nogueira EB, Gomes BS, Paiva LM, Souza-Motta CM. 2015. Endophytic fungi from medicinal plant Bauhinia forficata: diversity and biotechnological potential. Braz J Microbiol 57: 49-57.
Bissett J, Gams W, Jaklitsch W, Samuels GJ. 2015. Accepted Trichoderma names in the year 2015. IMA Fungus 6 (2): 263-295.
Bivi MR, Farhana MSN, Khairulmazmi A, Idris A. 2010. Control of Ganoderma boninense?: a causal agent of basal stem rot disease in oil palm with endophyte bacteria in vitro. Int J Agr Biol 12: 833-839.
Cheah, HL, Lim V, Sandai D. 2014. Inhibitors of the glyoxylate cycle enzyme ICL1 in Candida albicans for potential use as antifungal agents. PLoS ONE 9 (4): 1-8.
Deshmukh SK, Verekar SA, Bhave SV. 2014. Endophytic fungi: a reservoir of antibacterials. Front Microbiol 5: 1-43.
Dzurhinina IS, Kopchinskiy AG, Komon M, Bissett J, Szakacs G, Kubicek CP. 2005. An oligonucleotide barcode for species identification in Trichoderma and Hypocrea. Fungal Gen Biol 42: 813-828.
Edgar RC. 2004. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32 (5): 1792-1797.
Felsenstein J. 2009. Confidence limits on phylogenies?: an approach using the bootstrap. Evolution 39 (4): 783-791.
Fernando O, Nursyahra, Rizki. (2008). studi pemanfaatan tumbuhan familia Zingiberaceae yang berkhasiat obat di Kecamatan Luhak Nan Duo Kabupaten Pasaman Barat. Pendidikan Biologi 4 (2): 1-5.
Ginting RCB, Sukarno N, Widyastuti U, Darusman LK, Kanaya S. 2013. Diversity of endophytic fungi from red ginger (Zingiber officinale rosc.) plant and their inhibitory effect to Fusarium oxysporum plant pathogenic fungi. HAYATI J Biosci 20 (3): 127-137.
Gorfer M, Blumhoff M, Klaubauf S, Urban A, Inselsbacher E, Bandian D, Mitter B, Sessitsch A, Wanek W, Strauss J. 2011. Community profiling and gene expression of fungal assimilatory nitrate reductases in agricultural soil. ISME J 5 (11): 1771-1783.
Gveroska B. 2013. Relationships of Trichoderma spp. quantity in soil to reducing the dampingoff in tobacco seedlings. Bulg J Agri Sci 19 (4): 666-674.
Habsah M, Amran M, Mackeen MM, Lajis NH, Kikuzaki H, Nakatani N, Rahman AA, Ghafar, Ali AM. 2000. Screening of Zingiberaceae extracts for antimicrobial and antioxidant activities. J Ethnopharmacol 72 (3): 403-410.
Hall TA. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41: 95-98.
Hanada RE, Pomella AWV, Costa HS, Bezerra JZ, Loguercio LL, Pereira JO. 2010. Endophytic fungal diversity in Theobroma cacao (Cacao) and T. grandiflorum (Cupuaçu) trees and their potential for growth promotion and biocontrol of black-pod disease. Fungal Biol 114 (11-12): 901-910.
Hartanto S, Fitmawati, Sofiyanti N. 2014. Studi etnobotani famili Zingiberaceae dalam kehidupan masyarakat lokal di Kecamatan Pangean Kabupaten Kuantan Singingi, Riau. Biosaintifika 6 (2): 98-108.
Higginbotham S, Wong WR, Linington RG, Spadafora C, Iturrado L, Arnold AE. 2014. Sloth hair as a novel source of fungi with potent anti-parasitic, anti-cancer and anti-bacterial bioactivity. PLos ONE 9 (1). https://doi.org/10.1371/journal.pone.0084549.
Hosseyni-Moghaddam MS, Soltani J. 2014. Bioactivity of endophytic Trichoderma fungal species from the plant family Cupressaceae. Ann Microbiol 64 (2): 753-761.
Hu J, Zhou Y, Chen K, Li J, Wei Y, Wang Y, Wu Y, Ryder MH, Yang H, Denton MD. 2019. Large-scale Trichoderma diversity was associated with ecosystem, climate and geographic location. Environ Microbiol. https://doi.org/10.1111/1462-2920.1479.
Juwita T, Puspitasari IM, Levita J. 2018. Torch Ginger (Etlingera elatior): a review on its botanical aspects, phytoconstituents and pharmacological activities. Pak J Biol Sci 21 (4): 151-165.
Kaul S, Gupta S, Ahmed M, Dhar MK. 2012. Endophytic fungi from medicinal plants: a treasure hunt for bioactive metabolites. Phytochem Rev 11 (4): 487-505.
Kimura M. 1980. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16: 111-120.
Kopchinskiy, A., Komo?, M., Kubicek, C. P. & Druzhinina, I. S. (2005. TrichoBLAST: a multilocus database for Trichoderma and Hypocrea identifications. Mycol Res 109 (6): 658-660.
Kumar K, Amaresan N, Bhagat S, Madhuri K, Srivastava RC. 2012. Isolation and characterization of Trichoderma spp. for antagonistic activity against root rot and foliar pathogens. Indian J Microbiol 52 (2): 137-144.
Lachumy SJT, Sasidharan S, Sumathy S, Zakaria Z. 2010. Pharmacological activity, phytochemical analysis and toxicity of methanol extract of Etlingera elatior (Torch Ginger) flowers. Asian Pac J Trop Dis 3 (10): 769-774.
Manter DK, Vivanco, JM. 2007. Use of the ITS Primers, ITS1F and ITS4, to characterize fungal abundance and diversity in mixed-template samples by qPCR and length heterogeneity analysis. J Microbiol Methods 71 (1): 7-14.
Mukesh S, Vipul K, Shahid M, Sonika P, Singh A. 2016. Trichoderma - a potential and effective bio fungicide and alternative source against notable phytopathogens: a review. Afr J Agr Res 11 (5): 310-316.
Nei M, Kumar S. 2000. Molecular Evolution and Phylogenetics. New York: Oxford University Press.
Oliveira BR, Crespo MTB, Romao MVS, Benoliel MJ, Samson RA, Pereira VJ. 2013. New insights concerning the occurrence of fungi in water sources and their potential pathogenicity. Water Res 47 (16): 6338-6347.
Park Y, Mishra RC, Yoon S, Kim H, Park C, Seo S, Bae H. 2019. Endophytic Trichoderma citrinoviride isolated from mountain-cultivated ginseng (Panax ginseng) has great potential as a biocontrol agent against ginseng pathogens. J Ginseng Res. 43 (3): 408-420.
Punnawich Y, Montree I, Warin I, Kan C. 2009. Antifungal effects of Thai medicinal plants against Colletotrichum gloeosporioides Penz. Philipp Agric Sci 92 (3): 265-270.
Sharma P. 2011. Complexity of Trichoderma-Fusarium interaction and manifestation of biological control. Aust J Crop Sci 5 (8): 1027-1038.
Shi X, Wang D, Li X, Li L, Meng L, Li X, Pi Y, Zhou X, Wang B. 2017. Antimicrobial polyketides from: Trichoderma koningiopsis QA-3, an endophytic fungus obtained from the medicinal plant Artemisia argyi. RSC Advances 81 (7): 51335-51342.
Silalahi M, Nisyawati. 2018. The ethnobotanical study of edible and medicinal plants in the home garden of Batak Karo sub-ethnic in North Sumatra, Indonesia. Biodiversitas 19 (1): 229-238.
Silalahi M, Supriatna J, Walujo EK, Nisyawati. 2015. Local knowledge of medicinal plants in sub-ethnic Batak Simalungun of North Sumatra, Indonesia. Biodiversitas 16 (1): 44-54.
Siregar, ES, Pasaribu N. 2008. Inventarisasi jenis-jenis Zingiberaceae di Hutan Sibayak Sumatera Utara. Jurnal Penelitian MIPA 2 (1): 22-24.
Strobel G. 2003. Endophytes as sources of bioactive products. Microb Infect 5 (6): 535-544.
Strobel G, Daisy B. 2003. Bioprospecting for microbial endophytes and their natural products. Microbiol Mol Biol Rev 67 (4): 491-502.
Sung WS, Lee DG. 2010. Antifungal action of chlorogenic acid against pathogenic fungi, mediated by membrane disruption. Pure Appl Chem 82 (1): 219-226.
Suryanto D, Yeldi N, Munir E. 2016. Antifungal activity of endophyte bacterial isolates from torch ginger (Etlingera elicitor (Jack.) R. M. Smith)) root to some pathogenic fungal isolates. Int J Pharmtech Res 9 (8): 340-347.
Uzma F, Konappa NM, Chowdappa S. 2016. Diversity and extracellular enzyme activities of fungal endophytes isolated from medicinal plants of Western Ghats, Karnataka. Egypt J Basic App Sci 3 (4): 335-342.
Venieraki A, Dimou D, Katinakis P. 2017. Endophytic fungi residing in medicinal plants have the ability to produce the same or similar pharmacologically active secondary metabolites as their hosts. Hell Plant Prot J 10 (2): 51-66.
Vu D, Groenewald M, de Vries M, Gehrmann T, Stielow B, Eberhardt U, Al-Hatmi A, Groenewald JZ, Cardinali G, Houbraken J, Bouekhout T, Crous PW, Robert V, Verkley GJM. .2019. Large-scale generation and analysis of filamentous fungal DNA barcodes boosts coverage for kingdom fungi and reveals thresholds for fungal species and higher taxon delimitation. Stud Mycol 92: 135-154.
Wei JG, Xu T, Guo LD, Liu AR, Zhang Y, Pan XH. 2007. Endophytic Pestaliotopsis species associated with plants of Podocarpaceae, Theaceae and Taxaceae in Southern China. Fungal Divers 24: 55-74.
Yurnaliza Y, Aryantha INP, Esyanti RR, Susanto A. 2014. Antagonistic activity assessment of fungal endophytes from oil palm tissues against Ganoderma boninense Pat. Plant Pathol J 13 (4): 257-267.
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
Anees M, Tronsmo A, Edel-Hermann V, Hjeljord LG, Heraud C, Steinberg C. 2010. Characterization of field isolates of Trichoderma antagonistic against Rhizoctonia solani. Fungal Biol 114 (9): 691-701.
Auliani A, Fitmawati F, Sofiyanti N. 2014. Studi etnobotani famili Zingiberaceae dalam kehidupan masyarakat lokal di Kecamatan Siak Hulu Kabupaten Kampar. Jurnal Online Mahasiswa FMIPA 1 (2): 526-533.
Bezerra JDP, Nascimento CCF, Barbosa RN, Silva DCV, Svedese VM, Silva-Nogueira EB, Gomes BS, Paiva LM, Souza-Motta CM. 2015. Endophytic fungi from medicinal plant Bauhinia forficata: diversity and biotechnological potential. Braz J Microbiol 57: 49-57.
Bissett J, Gams W, Jaklitsch W, Samuels GJ. 2015. Accepted Trichoderma names in the year 2015. IMA Fungus 6 (2): 263-295.
Bivi MR, Farhana MSN, Khairulmazmi A, Idris A. 2010. Control of Ganoderma boninense?: a causal agent of basal stem rot disease in oil palm with endophyte bacteria in vitro. Int J Agr Biol 12: 833-839.
Cheah, HL, Lim V, Sandai D. 2014. Inhibitors of the glyoxylate cycle enzyme ICL1 in Candida albicans for potential use as antifungal agents. PLoS ONE 9 (4): 1-8.
Deshmukh SK, Verekar SA, Bhave SV. 2014. Endophytic fungi: a reservoir of antibacterials. Front Microbiol 5: 1-43.
Dzurhinina IS, Kopchinskiy AG, Komon M, Bissett J, Szakacs G, Kubicek CP. 2005. An oligonucleotide barcode for species identification in Trichoderma and Hypocrea. Fungal Gen Biol 42: 813-828.
Edgar RC. 2004. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32 (5): 1792-1797.
Felsenstein J. 2009. Confidence limits on phylogenies?: an approach using the bootstrap. Evolution 39 (4): 783-791.
Fernando O, Nursyahra, Rizki. (2008). studi pemanfaatan tumbuhan familia Zingiberaceae yang berkhasiat obat di Kecamatan Luhak Nan Duo Kabupaten Pasaman Barat. Pendidikan Biologi 4 (2): 1-5.
Ginting RCB, Sukarno N, Widyastuti U, Darusman LK, Kanaya S. 2013. Diversity of endophytic fungi from red ginger (Zingiber officinale rosc.) plant and their inhibitory effect to Fusarium oxysporum plant pathogenic fungi. HAYATI J Biosci 20 (3): 127-137.
Gorfer M, Blumhoff M, Klaubauf S, Urban A, Inselsbacher E, Bandian D, Mitter B, Sessitsch A, Wanek W, Strauss J. 2011. Community profiling and gene expression of fungal assimilatory nitrate reductases in agricultural soil. ISME J 5 (11): 1771-1783.
Gveroska B. 2013. Relationships of Trichoderma spp. quantity in soil to reducing the dampingoff in tobacco seedlings. Bulg J Agri Sci 19 (4): 666-674.
Habsah M, Amran M, Mackeen MM, Lajis NH, Kikuzaki H, Nakatani N, Rahman AA, Ghafar, Ali AM. 2000. Screening of Zingiberaceae extracts for antimicrobial and antioxidant activities. J Ethnopharmacol 72 (3): 403-410.
Hall TA. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41: 95-98.
Hanada RE, Pomella AWV, Costa HS, Bezerra JZ, Loguercio LL, Pereira JO. 2010. Endophytic fungal diversity in Theobroma cacao (Cacao) and T. grandiflorum (Cupuaçu) trees and their potential for growth promotion and biocontrol of black-pod disease. Fungal Biol 114 (11-12): 901-910.
Hartanto S, Fitmawati, Sofiyanti N. 2014. Studi etnobotani famili Zingiberaceae dalam kehidupan masyarakat lokal di Kecamatan Pangean Kabupaten Kuantan Singingi, Riau. Biosaintifika 6 (2): 98-108.
Higginbotham S, Wong WR, Linington RG, Spadafora C, Iturrado L, Arnold AE. 2014. Sloth hair as a novel source of fungi with potent anti-parasitic, anti-cancer and anti-bacterial bioactivity. PLos ONE 9 (1). https://doi.org/10.1371/journal.pone.0084549.
Hosseyni-Moghaddam MS, Soltani J. 2014. Bioactivity of endophytic Trichoderma fungal species from the plant family Cupressaceae. Ann Microbiol 64 (2): 753-761.
Hu J, Zhou Y, Chen K, Li J, Wei Y, Wang Y, Wu Y, Ryder MH, Yang H, Denton MD. 2019. Large-scale Trichoderma diversity was associated with ecosystem, climate and geographic location. Environ Microbiol. https://doi.org/10.1111/1462-2920.1479.
Juwita T, Puspitasari IM, Levita J. 2018. Torch Ginger (Etlingera elatior): a review on its botanical aspects, phytoconstituents and pharmacological activities. Pak J Biol Sci 21 (4): 151-165.
Kaul S, Gupta S, Ahmed M, Dhar MK. 2012. Endophytic fungi from medicinal plants: a treasure hunt for bioactive metabolites. Phytochem Rev 11 (4): 487-505.
Kimura M. 1980. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16: 111-120.
Kopchinskiy, A., Komo?, M., Kubicek, C. P. & Druzhinina, I. S. (2005. TrichoBLAST: a multilocus database for Trichoderma and Hypocrea identifications. Mycol Res 109 (6): 658-660.
Kumar K, Amaresan N, Bhagat S, Madhuri K, Srivastava RC. 2012. Isolation and characterization of Trichoderma spp. for antagonistic activity against root rot and foliar pathogens. Indian J Microbiol 52 (2): 137-144.
Lachumy SJT, Sasidharan S, Sumathy S, Zakaria Z. 2010. Pharmacological activity, phytochemical analysis and toxicity of methanol extract of Etlingera elatior (Torch Ginger) flowers. Asian Pac J Trop Dis 3 (10): 769-774.
Manter DK, Vivanco, JM. 2007. Use of the ITS Primers, ITS1F and ITS4, to characterize fungal abundance and diversity in mixed-template samples by qPCR and length heterogeneity analysis. J Microbiol Methods 71 (1): 7-14.
Mukesh S, Vipul K, Shahid M, Sonika P, Singh A. 2016. Trichoderma - a potential and effective bio fungicide and alternative source against notable phytopathogens: a review. Afr J Agr Res 11 (5): 310-316.
Nei M, Kumar S. 2000. Molecular Evolution and Phylogenetics. New York: Oxford University Press.
Oliveira BR, Crespo MTB, Romao MVS, Benoliel MJ, Samson RA, Pereira VJ. 2013. New insights concerning the occurrence of fungi in water sources and their potential pathogenicity. Water Res 47 (16): 6338-6347.
Park Y, Mishra RC, Yoon S, Kim H, Park C, Seo S, Bae H. 2019. Endophytic Trichoderma citrinoviride isolated from mountain-cultivated ginseng (Panax ginseng) has great potential as a biocontrol agent against ginseng pathogens. J Ginseng Res. 43 (3): 408-420.
Punnawich Y, Montree I, Warin I, Kan C. 2009. Antifungal effects of Thai medicinal plants against Colletotrichum gloeosporioides Penz. Philipp Agric Sci 92 (3): 265-270.
Sharma P. 2011. Complexity of Trichoderma-Fusarium interaction and manifestation of biological control. Aust J Crop Sci 5 (8): 1027-1038.
Shi X, Wang D, Li X, Li L, Meng L, Li X, Pi Y, Zhou X, Wang B. 2017. Antimicrobial polyketides from: Trichoderma koningiopsis QA-3, an endophytic fungus obtained from the medicinal plant Artemisia argyi. RSC Advances 81 (7): 51335-51342.
Silalahi M, Nisyawati. 2018. The ethnobotanical study of edible and medicinal plants in the home garden of Batak Karo sub-ethnic in North Sumatra, Indonesia. Biodiversitas 19 (1): 229-238.
Silalahi M, Supriatna J, Walujo EK, Nisyawati. 2015. Local knowledge of medicinal plants in sub-ethnic Batak Simalungun of North Sumatra, Indonesia. Biodiversitas 16 (1): 44-54.
Siregar, ES, Pasaribu N. 2008. Inventarisasi jenis-jenis Zingiberaceae di Hutan Sibayak Sumatera Utara. Jurnal Penelitian MIPA 2 (1): 22-24.
Strobel G. 2003. Endophytes as sources of bioactive products. Microb Infect 5 (6): 535-544.
Strobel G, Daisy B. 2003. Bioprospecting for microbial endophytes and their natural products. Microbiol Mol Biol Rev 67 (4): 491-502.
Sung WS, Lee DG. 2010. Antifungal action of chlorogenic acid against pathogenic fungi, mediated by membrane disruption. Pure Appl Chem 82 (1): 219-226.
Suryanto D, Yeldi N, Munir E. 2016. Antifungal activity of endophyte bacterial isolates from torch ginger (Etlingera elicitor (Jack.) R. M. Smith)) root to some pathogenic fungal isolates. Int J Pharmtech Res 9 (8): 340-347.
Uzma F, Konappa NM, Chowdappa S. 2016. Diversity and extracellular enzyme activities of fungal endophytes isolated from medicinal plants of Western Ghats, Karnataka. Egypt J Basic App Sci 3 (4): 335-342.
Venieraki A, Dimou D, Katinakis P. 2017. Endophytic fungi residing in medicinal plants have the ability to produce the same or similar pharmacologically active secondary metabolites as their hosts. Hell Plant Prot J 10 (2): 51-66.
Vu D, Groenewald M, de Vries M, Gehrmann T, Stielow B, Eberhardt U, Al-Hatmi A, Groenewald JZ, Cardinali G, Houbraken J, Bouekhout T, Crous PW, Robert V, Verkley GJM. .2019. Large-scale generation and analysis of filamentous fungal DNA barcodes boosts coverage for kingdom fungi and reveals thresholds for fungal species and higher taxon delimitation. Stud Mycol 92: 135-154.
Wei JG, Xu T, Guo LD, Liu AR, Zhang Y, Pan XH. 2007. Endophytic Pestaliotopsis species associated with plants of Podocarpaceae, Theaceae and Taxaceae in Southern China. Fungal Divers 24: 55-74.
Yurnaliza Y, Aryantha INP, Esyanti RR, Susanto A. 2014. Antagonistic activity assessment of fungal endophytes from oil palm tissues against Ganoderma boninense Pat. Plant Pathol J 13 (4): 257-267.
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