New emerging entomopathogenic fungi isolated from soil in South Sumatra (Indonesia) and their filtrate and conidial insecticidal activity against Spodoptera litura
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Abstract. Herlinda S, Efendi RA, Suharjo R, Hasbi, Setiawan A, Elfita, Verawaty M. 2020. New emerging entomopathogenic fungi isolated from soil in South Sumatra (Indonesia) and their filtrate and conidial insecticidal activity against Spodoptera litura. Biodiversitas 21: 5102-5113. This study was carried out to confirm identity of Beauveria bassiana and Metarhizium anisopliae using sequence analysis of Internal Transcribed Spacer (ITS) region as well as the two unknown isolates of EPF and to investigate their filtrate and conidial insecticidal activity against S. litura larvae. The EPF species were identified based on morphological characters and molecular analysis. Their culture filtrate and conidial bioassays were performed on S. litura larvae. The species found were Penicillium citrinum (BKbTp), Talaromyces diversus (MSwTp1), B. bassiana (BSwTd4), and M. anisopliae (MSwTp3) and have been deposited in the GenBank. All EPF species have high insecticidal activity against S. litura larvae. The highest larvae mortality caused by filtrate was found on P. citrinum (98.67%) and not significantly different from those of T. diversus (96%), but significantly different from B. bassiana (86.67%) and M anisopliae (82.67%). The highest larvae mortality caused by the conidia was also occurred to P. citrinum (98.67%) which was not significantly different from those of T. diversus (97.33%), B. bassiana (86.67%), and M. anisopliae (86.67%). The LT50 caused by T. diversus filtrate was the shortest (6.19 days) and not significantly different from those caused by P. citrinum (6.62 days). The shortest LT50 caused by conidia was found on P. citrinum (5.45 days). Therefore, the conidia and filtrate of P. citrinum, a new emerging entomopathogenic fungus, has the highest insecticidal activity. P. citrinum has the potential to be developed into commercial mycoinsecticides.
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References
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Ayudya DR, Herlinda S, Suwandi S. 2019. Insecticidal activity of culture filtrates from liquid medium of Beauveria bassiana isolates from South Sumatra (Indonesia) wetland soil against larvae of Spodoptera litura. Biodiversitas 20: 2101–2109. https://doi.org/10.13057/biodiv/d200802
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Bugti GA, Bin W, Na C, Feng LH. 2018. Pathogenicity of Beauveria bassiana strain 202 against sap-sucking insect pests. Plant Prot. Sci. 54: 111–117. https://doi.org/10.17221/45/2017-PPS
Chen Z, Xu L, Yang F, Ji G, Yang J, Wang J. 2014. Efficacy of Metarhizium anisopliae isolate MAX-2 from Shangri-la, China under desiccation stress. BBMC Microbiol: 14, 1–8. https://doi.org/http://www.biomedcentral.com/1471-2180/14/4
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Foo K, Seelan JSS, Dawood MM. 2017. Microfungi associated with Pteroptyx bearni (Coleoptera: Lampyridae) eggs and larvae from Kawang River, Sabah (Northern Borneo). Insects 8: 1–12. https://doi.org/10.3390/insects8030066
Gustianingtyas M, Herlinda S, Suwandi, Suparman, Hamidson H, Hasbi, Setiawan A, Verawaty M, Elfita, Arsi. 2020. Toxicity of entomopathogenic fungal culture filtrate of lowland and highland soil of South Sumatra (Indonesia) against Spodoptera litura larvae. Biodiversitas 21: 1839–1849. https://doi.org/10.13057/biodiv/d210510
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Luo Z, Ren H, Mousa JJ, Rangel DEN, Zhang Y, Bruner SD, Keyhani NO. 2017. The PacC transcription factor regulates secondary metabolite production and stress response, but has only minor effects on virulence in the insect pathogenic fungus Beauveria bassiana. Environ. Microbiol. 19: 788–802. https://doi.org/10.1111/1462-2920.13648
Maketon M, Amnuaykanjanasin A, Kaysorngup A. 2014. A rapid knockdown effect of Penicillium citrinum for control of the mosquito Culex quinquefasciatus in Thailand. World J. Microbiol. Biotechnol. 30: 727–736. https://doi.org/10.1007/s11274-013-1500-4
Mancillas-Paredes J, Hernández-Sánchez H, Jaramillo-Flores ME, García-Gutiérrez C. 2019. Proteases and chitinases induced in Beauveria bassiana during infection by Zabrotes subfasciatus. Southwest. Entomol 44: 125–137. https://doi.org/10.3958/059.044.0114
Mascarin GM, Jackson MA, Kobori NN, Behle RW, Delalibera Júnior Í. 2015. Liquid culture fermentation for rapid production of desiccation tolerant blastospores of Beauveria bassiana and Isaria fumosorosea strains. J. Invertebr. Pathol. 127: 11–20. https://doi.org/10.1016/j.jip.2014.12.001
Mathew AJ, Jayachandran K, Mathew J. 2010. Endophytic Penicillium citrinum Thom. from Scoparia dulcis Linn. Indian J. Microbiol. 50: 99–102. https://doi.org/10.1007/s12088-010-0065-2
Mazid S, Kalita JC, Rajkhowa RC. 2016. Biocontrol potential of Penicillium citrinum and Penicillium chrysogenum against red spider mite, Oligonychus coffeae Nietner infesting tea. J. Entomol. Res. https://doi.org/10.5958/0974-4576.2016.00008.6
Ngangambe MH, Mwatawala MW. 2020. Effects of entomopathogenic fungi (EPFs) and cropping systems on parasitoids of fall armyworm (Spodoptera frugiperda) on maize in eastern central, Tanzania. Biocontrol Sci. Technol. 30: 1–13. https://doi.org/10.1080/09583157.2020.1726878
Safitri A, Herlinda S, Setiawan A. 2018. Entomopathogenic fungi of soils of freshwater swamps, tidal lowlands, peatlands, and highlands of South Sumatra, Indonesia. Biodiversitas 19: 2365–2373. https://doi.org/10.13057/biodiv/d190647
Sharma L, Oliveira I, Torres L, Marques G. 2018. Entomopathogenic fungi in Portuguese vineyards soils: suggesting a ‘Galleria-Tenebrio-bait method’ as bait-insects Galleria and Tenebrio significantly underestimate the respective recoveries of Metarhizium (robertsii) and Beauveria (bassiana). MycoKeys 23: 1–23. https://doi.org/10.3897/mycokeys.38.26970
Siaga E, Lakitan B, Hasbi H, Bernas SM, Widuri LI, Kartika K. 2019. Floating seedbed for preparing rice seedlings under unpredictable flooding occurrence at tropical riparian wetland. Bulg. J. Agric. Sci. 25: 326–336.
Soesanto L, Mugiastuti E, Manan A. 2019. Raw secondary metabolites application of two Trichoderma harzianum isolates towards vascular streak dieback on cocoa seedlings. Pelita Perkeb. 35, 22–32. https://doi.org/10.22302/iccri.jur.pelitaperkebunan.v35i1.346
Souza ML, Sanches MM, Souza DAde, Faria M, Espinel-Correal C, Sihler W, Lopes RB. 2019. Within-host interactions of Metarhizium rileyi strains and nucleopolyhedroviruses in Spodoptera frugiperda and Anticarsia gemmatalis (Lepidoptera: Noctuidae). J. Invertebr. Pathol. 162: 10–18. https://doi.org/10.1016/j.jip.2019.01.006
Sowmya G, Ramanagouda SH, Jayappa J. 2017. Lethal and sub lethal effects of indigenous isolates of Metarhizium anisopliae (Metchnikoff) Sorokin against Spodoptera litura (Fabricius). Entomol. Zool. Stud. 5, 1154–1160.
Sumikarsih E, Herlinda S, Pujiastuti Y. 2019. Conidial density and viability of Beauveria bassiana isolates from Java and Sumatra and their virulence against Nilaparvata lugens at different temperatures. Agrivita J. Agric. Sci. 41: 335–349. http://doi.org/10.17503/agrivita.v41i2.2105
Suwandi, Ammar M, Chandra I. 2012. Application of extract compost increased yield and suppressed the diseases of ratoon rice crop in tidal swamp of Banyuasin Regency. J. Suboptimal Lands 1: 116–122. [Indonesia] https://doi.org/10.33230/JLSO.1.2.2012.15
Syamsudin TS, Faizal A, Kirana, R. 2019. Dataset on antixenosis and antibiosis of chili fruit by fruit fly (Bactrocera dorsalis) infestation Tati. Data Br. 23: 1–4. https://doi.org/10.1016/j.dib.2019.103758
Thaochan N, Sausa-Ard W. 2017. Occurrence and effectiveness of indigenous Metarhizium anisopliae against adults Zeugodacus cucurbitae (Coquillett) (Diptera: Tephritidae) in Southern Thailand. Songklanakarin J. Sci. Technol. 39: 325–334. https://doi.org/10.14456/sjst-psu.2017.35
Tompe AA, Hole UB, Kulkarni SR, Chaudhari CS, Chavan SK. 2020. Studies on seasonal incidence of leaf eating caterpillar, Spodoptera litura (Fab.) infesting capsicum under polyhouse condition. J. Entomol. Zool. Stud. 8: 761–764.
Vijayalakshmi P, Vijayalakshmi T, Naidu LN. 2016. Evaluation of certain insecticide molecules against chillipod borer, Spodoptera litura in Andhra Pradesh. J. Res. ANGRAU 44: 26–30.
Visagie CM, Jacobs K. 2012. Three new additions to the genus Talaromyces isolated from Atlantis sandveld fynbos soils. Persoonia 28: 14–24. https://doi.org/10.3767/003158512X632455
Visagie CM, Roets F, Jacobs K. 2009. A new species of Penicillium, P. ramulosum sp. nov., from the natural environment. Mycologia 101: 888–895. https://doi.org/10.3852/08-149
White T, Bruns T, Lee S, Taylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics, in: Innis, M.A., Gelfand, D.H., Sninsky, J.J., White, T.J. (Eds.), PCR Protocols: A Guide to Methods and Applications. Academic Press Inc., New York.
Yang H, Qin CS, Chen YM, Zhang GY, Dong LH, Wan SQ. 2019. Persistence of Metarhizium (Hypocreales: Clavicipitaceae) and Beauveria bassiana (Hypocreales: Clavicipitaceae) in tobacco soils and potential as biocontrol agents of Spodoptera litura (Lepidoptera: Noctuidae). Environ. Entomol. 48: 147–155. https://doi.org/10.1093/ee/nvy161
Youssef NA. 2014. Effect of certain entomopathogenic fungi and nematode on the desert locust Schistocerca gregaria (Forskal). Ann. Agric. Sci. 59, 125–131. https://doi.org/10.1016/j.aoas.2014.06.017
Altre JA, Vandenberg JD. 2001. Factors influencing the infectivity of isolates of Paecilomyces fumosoroseus against diamondback moth, Plutella xylostella. J. Invertebr. Pathol. 78: 31–36. https://doi.org/10.1006/jipa.2001.5043
Anwar W, Khan SN, Aslam M, Haider MS, Shahid AA, Ali M. 2015. Exploring fungal flora associated with insects of cotton agroecological zones of Punjab, Pakistan. Pakistan Entomol. 37: 27–31.
Ayudya DR, Herlinda S, Suwandi S. 2019. Insecticidal activity of culture filtrates from liquid medium of Beauveria bassiana isolates from South Sumatra (Indonesia) wetland soil against larvae of Spodoptera litura. Biodiversitas 20: 2101–2109. https://doi.org/10.13057/biodiv/d200802
Borisade OA, Medina A, Magan N. 2016. Interacting temperature and water activity modulate production of destruxin a by Metarhizium anisopliae on galleria larvae-modified agar based media invitro. West African J. Appl. Ecol. 24: 31–42.
Bugti GA, Bin W, Na C, Feng LH. 2018. Pathogenicity of Beauveria bassiana strain 202 against sap-sucking insect pests. Plant Prot. Sci. 54: 111–117. https://doi.org/10.17221/45/2017-PPS
Chen Z, Xu L, Yang F, Ji G, Yang J, Wang J. 2014. Efficacy of Metarhizium anisopliae isolate MAX-2 from Shangri-la, China under desiccation stress. BBMC Microbiol: 14, 1–8. https://doi.org/http://www.biomedcentral.com/1471-2180/14/4
El-Ghany TMA. 2015. Entomopathogenic Fungi and their Role in Biological Control. Biology Department Faculty of Science Jazan University KSA, Cairo. https://doi.org/10.4172/978-1-63278-065-2-66
Fernandes EKK, Rangel DEN, Moraes AM, Bittencourt VREP, Roberts DW. 2007. Variability in tolerance to UV-B radiation among Beauveria spp. isolates. J Invertebr Pathol 96: 237?243. https://doi.org/10.1016/j.jip.2007.05.007
Foo K, Seelan JSS, Dawood MM. 2017. Microfungi associated with Pteroptyx bearni (Coleoptera: Lampyridae) eggs and larvae from Kawang River, Sabah (Northern Borneo). Insects 8: 1–12. https://doi.org/10.3390/insects8030066
Gustianingtyas M, Herlinda S, Suwandi, Suparman, Hamidson H, Hasbi, Setiawan A, Verawaty M, Elfita, Arsi. 2020. Toxicity of entomopathogenic fungal culture filtrate of lowland and highland soil of South Sumatra (Indonesia) against Spodoptera litura larvae. Biodiversitas 21: 1839–1849. https://doi.org/10.13057/biodiv/d210510
Hernandez-Trejo A, Estrada-Drouaillet B, López-Santillán, J, Rios-Velasco C, Varela-Fuentes S, Rodríguez-Herrera R, Osorio-Hernández E. 2019. In vitro evaluation of native entomopathogenic fungi and neem (Azadiractha indica) extracts on Spodoptera frugiperda. Int. J. Exp. Bot. 4: 75–84. https://doi.org/.1037//0033-2909.I26.1.78
Johari A, Herlinda S, Irsan C, Pujiastuti Y. 2016. Phenomenon of Thrips (Thysanoptera) attack on chili plant (Capsicum annuum). Am. J. Agric. Biol. Sci. 11: 103–109. https://doi.org/10.3844/ajabssp.2016.103.109
Kumar S, Stecher G, Tamura K. 2016. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger data sets. Mol. Biol. Evol. 33: 1870–1874. https://doi.org/10.1093/molbev/msw054
Liu SF, Wang GJ, Nong XQ, Liu B, Wang MM, Li SL, Cao GC, Zhang ZH. 2017. Entomopathogen Metarhizium anisopliae promotes the early development of peanut root. Plant Prot. Sci. 53: 101–107. https://doi.org/10.17221/49/2016-PPS
Lopes RB, Souza DA, Rocha LFN, Montalva C, Luz C, Humber RA, Faria M. 2018. Metarhizium alvesii sp. nov.: A new member of the Metarhizium anisopliae species complex. J. Invertebr. Pathol. 151: 165–168. https://doi.org/10.1016/j.jip.2017.12.001
Luo Z, Ren H, Mousa JJ, Rangel DEN, Zhang Y, Bruner SD, Keyhani NO. 2017. The PacC transcription factor regulates secondary metabolite production and stress response, but has only minor effects on virulence in the insect pathogenic fungus Beauveria bassiana. Environ. Microbiol. 19: 788–802. https://doi.org/10.1111/1462-2920.13648
Maketon M, Amnuaykanjanasin A, Kaysorngup A. 2014. A rapid knockdown effect of Penicillium citrinum for control of the mosquito Culex quinquefasciatus in Thailand. World J. Microbiol. Biotechnol. 30: 727–736. https://doi.org/10.1007/s11274-013-1500-4
Mancillas-Paredes J, Hernández-Sánchez H, Jaramillo-Flores ME, García-Gutiérrez C. 2019. Proteases and chitinases induced in Beauveria bassiana during infection by Zabrotes subfasciatus. Southwest. Entomol 44: 125–137. https://doi.org/10.3958/059.044.0114
Mascarin GM, Jackson MA, Kobori NN, Behle RW, Delalibera Júnior Í. 2015. Liquid culture fermentation for rapid production of desiccation tolerant blastospores of Beauveria bassiana and Isaria fumosorosea strains. J. Invertebr. Pathol. 127: 11–20. https://doi.org/10.1016/j.jip.2014.12.001
Mathew AJ, Jayachandran K, Mathew J. 2010. Endophytic Penicillium citrinum Thom. from Scoparia dulcis Linn. Indian J. Microbiol. 50: 99–102. https://doi.org/10.1007/s12088-010-0065-2
Mazid S, Kalita JC, Rajkhowa RC. 2016. Biocontrol potential of Penicillium citrinum and Penicillium chrysogenum against red spider mite, Oligonychus coffeae Nietner infesting tea. J. Entomol. Res. https://doi.org/10.5958/0974-4576.2016.00008.6
Ngangambe MH, Mwatawala MW. 2020. Effects of entomopathogenic fungi (EPFs) and cropping systems on parasitoids of fall armyworm (Spodoptera frugiperda) on maize in eastern central, Tanzania. Biocontrol Sci. Technol. 30: 1–13. https://doi.org/10.1080/09583157.2020.1726878
Safitri A, Herlinda S, Setiawan A. 2018. Entomopathogenic fungi of soils of freshwater swamps, tidal lowlands, peatlands, and highlands of South Sumatra, Indonesia. Biodiversitas 19: 2365–2373. https://doi.org/10.13057/biodiv/d190647
Sharma L, Oliveira I, Torres L, Marques G. 2018. Entomopathogenic fungi in Portuguese vineyards soils: suggesting a ‘Galleria-Tenebrio-bait method’ as bait-insects Galleria and Tenebrio significantly underestimate the respective recoveries of Metarhizium (robertsii) and Beauveria (bassiana). MycoKeys 23: 1–23. https://doi.org/10.3897/mycokeys.38.26970
Siaga E, Lakitan B, Hasbi H, Bernas SM, Widuri LI, Kartika K. 2019. Floating seedbed for preparing rice seedlings under unpredictable flooding occurrence at tropical riparian wetland. Bulg. J. Agric. Sci. 25: 326–336.
Soesanto L, Mugiastuti E, Manan A. 2019. Raw secondary metabolites application of two Trichoderma harzianum isolates towards vascular streak dieback on cocoa seedlings. Pelita Perkeb. 35, 22–32. https://doi.org/10.22302/iccri.jur.pelitaperkebunan.v35i1.346
Souza ML, Sanches MM, Souza DAde, Faria M, Espinel-Correal C, Sihler W, Lopes RB. 2019. Within-host interactions of Metarhizium rileyi strains and nucleopolyhedroviruses in Spodoptera frugiperda and Anticarsia gemmatalis (Lepidoptera: Noctuidae). J. Invertebr. Pathol. 162: 10–18. https://doi.org/10.1016/j.jip.2019.01.006
Sowmya G, Ramanagouda SH, Jayappa J. 2017. Lethal and sub lethal effects of indigenous isolates of Metarhizium anisopliae (Metchnikoff) Sorokin against Spodoptera litura (Fabricius). Entomol. Zool. Stud. 5, 1154–1160.
Sumikarsih E, Herlinda S, Pujiastuti Y. 2019. Conidial density and viability of Beauveria bassiana isolates from Java and Sumatra and their virulence against Nilaparvata lugens at different temperatures. Agrivita J. Agric. Sci. 41: 335–349. http://doi.org/10.17503/agrivita.v41i2.2105
Suwandi, Ammar M, Chandra I. 2012. Application of extract compost increased yield and suppressed the diseases of ratoon rice crop in tidal swamp of Banyuasin Regency. J. Suboptimal Lands 1: 116–122. [Indonesia] https://doi.org/10.33230/JLSO.1.2.2012.15
Syamsudin TS, Faizal A, Kirana, R. 2019. Dataset on antixenosis and antibiosis of chili fruit by fruit fly (Bactrocera dorsalis) infestation Tati. Data Br. 23: 1–4. https://doi.org/10.1016/j.dib.2019.103758
Thaochan N, Sausa-Ard W. 2017. Occurrence and effectiveness of indigenous Metarhizium anisopliae against adults Zeugodacus cucurbitae (Coquillett) (Diptera: Tephritidae) in Southern Thailand. Songklanakarin J. Sci. Technol. 39: 325–334. https://doi.org/10.14456/sjst-psu.2017.35
Tompe AA, Hole UB, Kulkarni SR, Chaudhari CS, Chavan SK. 2020. Studies on seasonal incidence of leaf eating caterpillar, Spodoptera litura (Fab.) infesting capsicum under polyhouse condition. J. Entomol. Zool. Stud. 8: 761–764.
Vijayalakshmi P, Vijayalakshmi T, Naidu LN. 2016. Evaluation of certain insecticide molecules against chillipod borer, Spodoptera litura in Andhra Pradesh. J. Res. ANGRAU 44: 26–30.
Visagie CM, Jacobs K. 2012. Three new additions to the genus Talaromyces isolated from Atlantis sandveld fynbos soils. Persoonia 28: 14–24. https://doi.org/10.3767/003158512X632455
Visagie CM, Roets F, Jacobs K. 2009. A new species of Penicillium, P. ramulosum sp. nov., from the natural environment. Mycologia 101: 888–895. https://doi.org/10.3852/08-149
White T, Bruns T, Lee S, Taylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics, in: Innis, M.A., Gelfand, D.H., Sninsky, J.J., White, T.J. (Eds.), PCR Protocols: A Guide to Methods and Applications. Academic Press Inc., New York.
Yang H, Qin CS, Chen YM, Zhang GY, Dong LH, Wan SQ. 2019. Persistence of Metarhizium (Hypocreales: Clavicipitaceae) and Beauveria bassiana (Hypocreales: Clavicipitaceae) in tobacco soils and potential as biocontrol agents of Spodoptera litura (Lepidoptera: Noctuidae). Environ. Entomol. 48: 147–155. https://doi.org/10.1093/ee/nvy161
Youssef NA. 2014. Effect of certain entomopathogenic fungi and nematode on the desert locust Schistocerca gregaria (Forskal). Ann. Agric. Sci. 59, 125–131. https://doi.org/10.1016/j.aoas.2014.06.017
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