Organic control of Bemisia tabaci Genn. on Capsicum annuum with entomopathogenic fungi raw secondary metabolites
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Abstract. Soesanto L, Fatihah B, Manan A, Mugiastuti E, Prihaningsih N. 2020. Organic control of Bemisia tabaci Genn. on Capsicum annuum with entomopathogenic fungi raw secondary metabolites. Biodiversitas 21: xxxx. Control of whitefly with entomopathogenic fungi raw secondary metabolites and their correlation was investigated under control condition. The in vitro test used randomize completely design consisted of five treatments (raw secondary metabolites of Beauveria bassiana B16 and B10, Metarhizium anisopliae M16, Lecanicillium lecanii L16, and no treatments) and repeated five times. The in planta one used Latin square design consisted of five treatments and repeated five times. Variables observed were the mortality of whitefly imago, chitinolytic index, incubation period, viral disease intensity, plant height and total leaves per plant. The results showed that all treatment of raw secondary metabolites of entomopathogenic fungi caused mortality in the B. tabaci imago by 77.8% (B. bassiana B16); 71.5% (B. bassiana B10); 66.7% (M. anisopliae M16); and 59.5% (L. lecanii L16). All raw secondary metabolites of entomopathogenic fungi reduce the intensity of viral diseases by 79.98% (B. bassiana B16); 74.00% (B. bassiana B10); 72.23% (L. lecanii L16); and 55.41% (M. anisopliae M16). The correlation between B. tabaci mortality due to raw secondary metabolites of entomopathogenic fungi with the viral disease intensity is very close and opposite. Every 1% increase in pest mortality causes decrease in viral intensity by 1.346%.
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References
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El-bassiony AM, Fawzy ZF, Abd El-Samad EH, Riad GS. 2010. Growth, yield and fruit quality of sweet pepper plants (Capsicum annuum L.) as affected by potassium fertilization. J Ame Sci 6 (12): 722–730.
Fernandes EG, Valério HM, Feltrin T, Sand STV. 2012. Variability in the production of extracellular enzymes by entomopathogenic fungi grown on different substrates. Brazilian Journal of Microbiology 43: 827–833.
Gerling D, Motro U, Horowitz R. 1980. Dynamics of Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae) attacking cotton in the coastal plain of Israel. Bulletin of Entomological Research 70 (2): 213–219. https://doi.org/10.1017/S000748530000746X.
Haedar N, Natsir H, Fahruddin, Aryanti W. 2017. Production and characterization of chitinase enzymes from chitinolytic bacteria from Anadara granosa shellfish. J Ilm Alam Ling 8 (15): 14-21.
Han JH, Jin BR, Kim JJ, Lee SY. 2014. Virulence of entomopathogenic fungi Metarhizium anisopliae and Paecilomyces fumosoroseus for the microbial control of Spodoptera exigua. Mycobiology 42 (4): 385–390. https://doi.org/10.5941/MYCO.2014.42.4.385.
He Y, Zhao J, Zheng Y, Weng Q, Biondi A, Desneux N, Wu K. 2013. Assessment of potential sublethal effects of various insecticides on key biological traits of the tobacco whitefly, Bemisia tabaci. International Journal of Biological Sciences 9 (3): 246–255. https://doi.org/10.7150/ijbs.5762.
Horowitz AR, Antignus Y, Gerling D. 2011. Management of Bemisia tabaci Whiteflies: The Whitefly, Bemisia tabaci (Homoptera: Aleyrodidae) Interaction with Geminivrus-Infected Host Plants. (W. M. O. Thompson, Ed.). National Agricultural Research Intitute, USA. Retrieved from http://www.springer.com/10.1007/978-94-007-1524-0.
Keyhani NO. 2018. Lipid biology in fungal stress and virulence: Entomopathogenic fungi. Fungal Biology 122 (6): 420–429. https://doi.org/10.1016/j.funbio.2017.07.003.
Kim JJ, Jeong G, Han JH, Lee S. 2013. Biological Control of Aphid Using Fungal Culture and Culture Filtrates of Beauveria bassiana. Mycobiology 41 (4): 221–224. https://doi.org/10.5941/MYCO.2013.41.4.221.
Legg JP, Shirima R, Tajebe LS, Guastella D, Boniface S, Jeremiah S, Nsami E, Chikoti P, Rapisarda C. 2014. Biology and management of Bemisia whitefly vectors of cassava virus pandemics in Africa. Pest Management Science 70 (10): 1446–1453. https://doi.org/10.1002/ps.3793.
Liu CP, Lin PW. 2013. Titanium dioxide nanoparticles as UV protectants for enhancing the survival of conidia of the entomopathogenic fungus. Int J Innov Biol Res 2 (1): 21–29.
Macfadyen S, Paull C, Boykin LM, De Barro P, Maruthi MN, Otim M, Kelyebi A, Vassao DG, Sseruwangi P, Tay WT, Delatte H, Seguni Z, Colvin J, Omongo CA. 2018. Cassava whitefly, Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) in East African farming landscapes: a review of the factors determining abundance. Bulletin of Entomological Research 108 (5): 565–582. https://doi.org/10.1017/S0007485318000032.
Mascarin GM, Kobori NN, Quintela ED, Delalibera I. 2013. The virulence of entomopathogenic fungi against Bemisia tabaci biotype B (Hemiptera: Aleyrodidae) and their conidial production using solid substrate fermentation. Biological Control 66 (3): 209–218. https://doi.org/10.1016/j.biocontrol.2013.05.001.
Mondal S, Baksi S, Koris A, Vatai G. 2016. Journey of enzymes in entomopathogenic fungi. Pacific Science Review A: Natural Science and Engineering 18 (2); 85-99. https://doi.org/10.1016/j.psra.2016.10.001.
Moreno-Delafuente A, Garzo E, Moreno A, Fereres A. 2013. A Plant Virus Manipulates the Behavior of Its Whitefly Vector to Enhance Its Transmission Efficiency and Spread. PLoS ONE 8 (4): e61543. https://doi.org/10.1371/journal.pone.0061543.
Mubarik NR, Mahagiani I, Anindyaputri A, Santoso S, Rusmana I. 2010. Chitinolytic bacteria isolated from chili rhizosphere: Chitinase characterization and its application as biocontrol for whitefly (Bemisia tabaci Genn.). American J Agric Biol Sci 5 (4): 430–435.
Mustafa U, Kaur G. 2008. UV-B radiation and temperature stress causes variable growth response in Metarhizium anisopliae and Beauveria bassiana isolates. The Internet Journal of Microbiology 7 (1): 1–8.
Navas-Castillo J, Fiallo-Olivé E, Sánchez-Campos S. 2011. Emerging virus diseases transmitted by whiteflies. Annual Review of Phytopathology 49 (1): 219–248. https://doi.org/10.1146/annurev-phyto-072910-095235.
Oliveira AS, Braga GUL, Rangel DEN. 2018. Metarhizium robertsii illuminated during mycelial growth produces conidia with increased germination speed and virulence. Fungal Biology 122 (6): 555–562. https://doi.org/10.1016/j.funbio.2017.12.009.
Putra G, Hadiastono T, Afandhi A, Prayogo Y. 2013. Pathogenicity of the entomopathogenic fungus Lecanicillium lecanii (Deuteromycotina: Hyphomycetes) against Bemisia tabaci (G.) as a vector of cowpea mild mottle virus (CMMV) in soybean plants. Jurnal Hama dan Penyakit Tumbuhan 1 (1): 27–39.
Rachmawaty. 2009. The comparation chitinase enzyme of Beauveria bassiana local strain South Sulawesi to Mortality Spodoptera litura. Bionature 10 (2): 60–64.
Ramanujam B, Balachander M, Roopa G, Rangeshwaran R, Karmakar P. 2011. Chitinase activity and virulence of different isolates of Beauveria bassiana, Metarhizium anisopliae and Lecanicillium spp. Journal of Biological Control 25 (3): 223-228.
Rauf S, Ali Y, Hussain S, Ullah F, Hayat A. 2018. Design of a novel filter paper based construct for rapid analysis of acetone. PLOS ONE 13 (7): e0199978. https://doi.org/10.1371/journal.pone.0199978.
Rodríguez E, Téllez MM, Janssen D. 2019. Whitefly control strategies against Tomato Leaf Curl New Delhi Virus in greenhouse zucchini. International Journal of Environmental Research and Public Health 16 (15): 2673. https://doi.org/10.3390/ijerph16152673.
Soesanto L. 2017. Introduction to Biological Pesticides: Addendum to Secondary Metabolites of Biological Agents. PT Raja Graffindo Persada, Jakarta. [Indonesian].
Supriadi RD, Susila AD, Sulistyono E. 2018. Penetapan kebutuhan air tanaman aabai merah (Capsicum annuum L.) dan cabai rawit (Capsicum frutescens L.). Jurnal Hortikultura Indonesia 9 (1): 38–46. https://doi.org/10.29244/jhi.9.1.38-46.
Suryadi Y, Priyatno TP, Samudra IM, Susilowati DN, Lawati N, Kustaman E. 2016. Pemurnian parsial dan karakterisasi kitinase asal jamur entomopatogen Beauveria bassiana isolat BB200109. Jurnal AgroBiogen 9 (2): 77. https://doi.org/10.21082/jbio.v9n2.2013.p77-84.
Wang L, Huang J, You M, Liu B. 2004. Time-dose-mortality modelling and virulence indices for six strains of Lecanicillium lecanii against sweetpotato whitefly, Bemisia tabaci (Gennadius). JEN 128 (7): 494–500. https://doi.org/10.1111/j.1439-0418.2004.00879.
Widariyanto R, Pinem MI, Zahara F. 2017. Pathogenicity of some entomophatogen’s fungus (Lecanicillium lecanii, Metarhizium anisopliae, and Beauveria bassiana) to Aphis glycineson Soybean. Jurnal Agroekoteknologi 5 (2): 8–16.
Yao F-L, Zheng Y, Huang X-Y, Ding X-L, Zhao J-W, Desneux N, He Y-X, Weng Q-Y. 2017. Dynamics of Bemisia tabaci biotypes and insecticide resistance in Fujian province in China during 2005–2014. Scientific Reports 7 (1): 40803. https://doi.org/10.1038/srep40803.
Yin X, Gourdriaan J, Lantinga EA, Vos J, Spiertz HJ. 2003. A flexible sigmoid function of determinate growth. Annals of Botany 91 (3): 361–371. https://doi.org/10.1093/aob/mcg029.
Yun H-G, Kim D-J, Gwak W-S, Shin T-Y, Woo S-D. 2017. Entomopathogenic fungi as dual control agents against both the pest Myzus persicae and phytopathogen Botrytis cinerea. Mycobiology 45 (3): 192–198. https://doi.org/10.5941/MYCO.2017.45.3.192.
Alavo TBC, Sermann H, Bochow H. 2002. Virulence of strains of the entomopathogenic fungus Verticillium Lecanii to phids: strain improvement. Archives of Phytopathology and Plant Protection 34 (6): 379–398. https://doi.org/10.1080/716061669.
Arogundade O, Balogun OS, Akinyemi SOS, Kumar PL. 2015. Surveys of virus diseases on pepper (Capsicum spp.) in South-west Nigeria. African Journal of Biotechnology 14 (48): 3198–3205. https://doi.org/10.5897/AJB2015.14803.
De Barro PJ, Liu S-S, Boykin LM, Dinsdale AB. 2011. Bemisia tabaci?: A statement of species status. Annual Review of Entomology 56 (1): 1–19. https://doi.org/10.1146/annurev-ento-112408-085504.
El-bassiony AM, Fawzy ZF, Abd El-Samad EH, Riad GS. 2010. Growth, yield and fruit quality of sweet pepper plants (Capsicum annuum L.) as affected by potassium fertilization. J Ame Sci 6 (12): 722–730.
Fernandes EG, Valério HM, Feltrin T, Sand STV. 2012. Variability in the production of extracellular enzymes by entomopathogenic fungi grown on different substrates. Brazilian Journal of Microbiology 43: 827–833.
Gerling D, Motro U, Horowitz R. 1980. Dynamics of Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae) attacking cotton in the coastal plain of Israel. Bulletin of Entomological Research 70 (2): 213–219. https://doi.org/10.1017/S000748530000746X.
Haedar N, Natsir H, Fahruddin, Aryanti W. 2017. Production and characterization of chitinase enzymes from chitinolytic bacteria from Anadara granosa shellfish. J Ilm Alam Ling 8 (15): 14-21.
Han JH, Jin BR, Kim JJ, Lee SY. 2014. Virulence of entomopathogenic fungi Metarhizium anisopliae and Paecilomyces fumosoroseus for the microbial control of Spodoptera exigua. Mycobiology 42 (4): 385–390. https://doi.org/10.5941/MYCO.2014.42.4.385.
He Y, Zhao J, Zheng Y, Weng Q, Biondi A, Desneux N, Wu K. 2013. Assessment of potential sublethal effects of various insecticides on key biological traits of the tobacco whitefly, Bemisia tabaci. International Journal of Biological Sciences 9 (3): 246–255. https://doi.org/10.7150/ijbs.5762.
Horowitz AR, Antignus Y, Gerling D. 2011. Management of Bemisia tabaci Whiteflies: The Whitefly, Bemisia tabaci (Homoptera: Aleyrodidae) Interaction with Geminivrus-Infected Host Plants. (W. M. O. Thompson, Ed.). National Agricultural Research Intitute, USA. Retrieved from http://www.springer.com/10.1007/978-94-007-1524-0.
Keyhani NO. 2018. Lipid biology in fungal stress and virulence: Entomopathogenic fungi. Fungal Biology 122 (6): 420–429. https://doi.org/10.1016/j.funbio.2017.07.003.
Kim JJ, Jeong G, Han JH, Lee S. 2013. Biological Control of Aphid Using Fungal Culture and Culture Filtrates of Beauveria bassiana. Mycobiology 41 (4): 221–224. https://doi.org/10.5941/MYCO.2013.41.4.221.
Legg JP, Shirima R, Tajebe LS, Guastella D, Boniface S, Jeremiah S, Nsami E, Chikoti P, Rapisarda C. 2014. Biology and management of Bemisia whitefly vectors of cassava virus pandemics in Africa. Pest Management Science 70 (10): 1446–1453. https://doi.org/10.1002/ps.3793.
Liu CP, Lin PW. 2013. Titanium dioxide nanoparticles as UV protectants for enhancing the survival of conidia of the entomopathogenic fungus. Int J Innov Biol Res 2 (1): 21–29.
Macfadyen S, Paull C, Boykin LM, De Barro P, Maruthi MN, Otim M, Kelyebi A, Vassao DG, Sseruwangi P, Tay WT, Delatte H, Seguni Z, Colvin J, Omongo CA. 2018. Cassava whitefly, Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) in East African farming landscapes: a review of the factors determining abundance. Bulletin of Entomological Research 108 (5): 565–582. https://doi.org/10.1017/S0007485318000032.
Mascarin GM, Kobori NN, Quintela ED, Delalibera I. 2013. The virulence of entomopathogenic fungi against Bemisia tabaci biotype B (Hemiptera: Aleyrodidae) and their conidial production using solid substrate fermentation. Biological Control 66 (3): 209–218. https://doi.org/10.1016/j.biocontrol.2013.05.001.
Mondal S, Baksi S, Koris A, Vatai G. 2016. Journey of enzymes in entomopathogenic fungi. Pacific Science Review A: Natural Science and Engineering 18 (2); 85-99. https://doi.org/10.1016/j.psra.2016.10.001.
Moreno-Delafuente A, Garzo E, Moreno A, Fereres A. 2013. A Plant Virus Manipulates the Behavior of Its Whitefly Vector to Enhance Its Transmission Efficiency and Spread. PLoS ONE 8 (4): e61543. https://doi.org/10.1371/journal.pone.0061543.
Mubarik NR, Mahagiani I, Anindyaputri A, Santoso S, Rusmana I. 2010. Chitinolytic bacteria isolated from chili rhizosphere: Chitinase characterization and its application as biocontrol for whitefly (Bemisia tabaci Genn.). American J Agric Biol Sci 5 (4): 430–435.
Mustafa U, Kaur G. 2008. UV-B radiation and temperature stress causes variable growth response in Metarhizium anisopliae and Beauveria bassiana isolates. The Internet Journal of Microbiology 7 (1): 1–8.
Navas-Castillo J, Fiallo-Olivé E, Sánchez-Campos S. 2011. Emerging virus diseases transmitted by whiteflies. Annual Review of Phytopathology 49 (1): 219–248. https://doi.org/10.1146/annurev-phyto-072910-095235.
Oliveira AS, Braga GUL, Rangel DEN. 2018. Metarhizium robertsii illuminated during mycelial growth produces conidia with increased germination speed and virulence. Fungal Biology 122 (6): 555–562. https://doi.org/10.1016/j.funbio.2017.12.009.
Putra G, Hadiastono T, Afandhi A, Prayogo Y. 2013. Pathogenicity of the entomopathogenic fungus Lecanicillium lecanii (Deuteromycotina: Hyphomycetes) against Bemisia tabaci (G.) as a vector of cowpea mild mottle virus (CMMV) in soybean plants. Jurnal Hama dan Penyakit Tumbuhan 1 (1): 27–39.
Rachmawaty. 2009. The comparation chitinase enzyme of Beauveria bassiana local strain South Sulawesi to Mortality Spodoptera litura. Bionature 10 (2): 60–64.
Ramanujam B, Balachander M, Roopa G, Rangeshwaran R, Karmakar P. 2011. Chitinase activity and virulence of different isolates of Beauveria bassiana, Metarhizium anisopliae and Lecanicillium spp. Journal of Biological Control 25 (3): 223-228.
Rauf S, Ali Y, Hussain S, Ullah F, Hayat A. 2018. Design of a novel filter paper based construct for rapid analysis of acetone. PLOS ONE 13 (7): e0199978. https://doi.org/10.1371/journal.pone.0199978.
Rodríguez E, Téllez MM, Janssen D. 2019. Whitefly control strategies against Tomato Leaf Curl New Delhi Virus in greenhouse zucchini. International Journal of Environmental Research and Public Health 16 (15): 2673. https://doi.org/10.3390/ijerph16152673.
Soesanto L. 2017. Introduction to Biological Pesticides: Addendum to Secondary Metabolites of Biological Agents. PT Raja Graffindo Persada, Jakarta. [Indonesian].
Supriadi RD, Susila AD, Sulistyono E. 2018. Penetapan kebutuhan air tanaman aabai merah (Capsicum annuum L.) dan cabai rawit (Capsicum frutescens L.). Jurnal Hortikultura Indonesia 9 (1): 38–46. https://doi.org/10.29244/jhi.9.1.38-46.
Suryadi Y, Priyatno TP, Samudra IM, Susilowati DN, Lawati N, Kustaman E. 2016. Pemurnian parsial dan karakterisasi kitinase asal jamur entomopatogen Beauveria bassiana isolat BB200109. Jurnal AgroBiogen 9 (2): 77. https://doi.org/10.21082/jbio.v9n2.2013.p77-84.
Wang L, Huang J, You M, Liu B. 2004. Time-dose-mortality modelling and virulence indices for six strains of Lecanicillium lecanii against sweetpotato whitefly, Bemisia tabaci (Gennadius). JEN 128 (7): 494–500. https://doi.org/10.1111/j.1439-0418.2004.00879.
Widariyanto R, Pinem MI, Zahara F. 2017. Pathogenicity of some entomophatogen’s fungus (Lecanicillium lecanii, Metarhizium anisopliae, and Beauveria bassiana) to Aphis glycineson Soybean. Jurnal Agroekoteknologi 5 (2): 8–16.
Yao F-L, Zheng Y, Huang X-Y, Ding X-L, Zhao J-W, Desneux N, He Y-X, Weng Q-Y. 2017. Dynamics of Bemisia tabaci biotypes and insecticide resistance in Fujian province in China during 2005–2014. Scientific Reports 7 (1): 40803. https://doi.org/10.1038/srep40803.
Yin X, Gourdriaan J, Lantinga EA, Vos J, Spiertz HJ. 2003. A flexible sigmoid function of determinate growth. Annals of Botany 91 (3): 361–371. https://doi.org/10.1093/aob/mcg029.
Yun H-G, Kim D-J, Gwak W-S, Shin T-Y, Woo S-D. 2017. Entomopathogenic fungi as dual control agents against both the pest Myzus persicae and phytopathogen Botrytis cinerea. Mycobiology 45 (3): 192–198. https://doi.org/10.5941/MYCO.2017.45.3.192.
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