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Morphological and molecular identification of four isolates of the entomopathogenic fungal genus Akanthomyces and their effects against Bemisia tabaci on cucumber

Published online by Cambridge University Press:  18 May 2021

Fereshteh Broumandnia ,
Ali Rajabpour Open the ORCID record for Ali Rajabpour [Opens in a new window] ,
Mohamad Hamed Ghodoum Parizipour  and
Fatemeh Yarahmadi
Fereshteh Broumandnia
Affiliation:
Department of Plant Protection, Faculty of Agriculture, Agricultural Sciences and Natural Resources University of Khuzestan, Mollasani, Ahvaz, Iran
Ali Rajabpour*
Affiliation:
Department of Plant Protection, Faculty of Agriculture, Agricultural Sciences and Natural Resources University of Khuzestan, Mollasani, Ahvaz, Iran
Mohamad Hamed Ghodoum Parizipour
Affiliation:
Department of Plant Protection, Faculty of Agriculture, Agricultural Sciences and Natural Resources University of Khuzestan, Mollasani, Ahvaz, Iran
Fatemeh Yarahmadi
Affiliation:
Department of Plant Protection, Faculty of Agriculture, Agricultural Sciences and Natural Resources University of Khuzestan, Mollasani, Ahvaz, Iran
*
Author for correspondence: Ali Rajabpour, Email: [email protected]; [email protected]
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Abstract

The cotton whitefly, Bemisia tabaci Gen. (Hem., Aleyrodidae), is a key pest of many vegetables. Entomopathogenic fungi are promising microbial control agents against B. tabaci, but limited information is available concerning indigenous Iranian isolates. In this study, three isolates of Akanthomyces lecanii (PAL6, PAL7, and PAL8) and one isolate of A. muscarius (AGM5) were obtained from citrus hemipteran pests, Pulvinaria aurantii Cock. and Aphis gossypii Glover, in Mazandaran province, northern Iran. The isolates were then morphologically and molecularly identified. The efficacies of five different agar media for vegetative growth and conidiation of each isolate were determined. Potato dextrose agar was the medium on which the fungal mycelia developed at a relatively high rate. However, the highest rate of conidiation was found on Sabouraud dextrose agar. To determine the effects of the isolates on B. tabaci, a dose–response bioassay was carried out to estimate lethal concentration (LC50) and lethal time (LT50) values of each fungal isolate to second instar nymphs. The mean LC50 values of A. lecanii isolates ranged from 4.22 × 106 to 7.35 × 1013 conidia ml−1 at 5 to 7 days after the treatment. For A. muscarius, the values varied from 9.2 × 104 to 8.7 × 1010 conidia ml−1 at 5 to 7 days after the treatment. The lowest and the highest mean LC50 values were observed for A. mucarius (AGM5) and A. lecanii (isolate PAL6), respectively. The mean LT50 values of A. lecanii and A. muscarius isolates were 7.1–9.0 and 4.9–7.2 days, respectively. The LT50 values of A. muscarius were significantly lower than the other isolates. Overall, all isolates, especially A. muscarius (AGM5), exhibited appropriate potential as a biological control agent against B. tabaci.

Keywords

Aleyrodidaeentomopathogenic fungiintegrated pest managementmicrobiological control
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 111 , Issue 5 , October 2021 , pp. 628 - 636
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Abdel-Raheem, MA and Al-Keridis, LA (2017) Virulence of three entomopathogenic fungi against whitefly, Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) in tomato crop. Journal of Entomology 14, 155–159.Google Scholar
Abdulle, YA, Nazir, T, Keerio, AU, Ali, H, Zaman, S, Anwar, T, Nam, TD and Qiu, D (2020) In vitro virulence of three Lecanicillium lecanii strains against the whitefly, Bemisia tabaci (Genn.) (Hemiptera: Aleyrodidae). Egyptian Journal of Biological Pest Control 30, 1–6.CrossRefGoogle Scholar
Arenal, F, Platas, G, Monte, E and Peláez, F (2000) ITS sequencing support for Epicoccum nigrum and Phoma epicoccina being the same biological species. Mycological Research 104, 301.CrossRefGoogle Scholar
Balsamo-Crivelli, G (1835) Aufstellung von zwei neuen Arten Mucedineen, Botrytis bassiana und Mucor radicans, und über die Entwickelung der ersteren Art im Seidenwurme. Linnaea 10, 609–618.Google Scholar
Banihashemi, AS, Seraj, AA, Yarahmadi, F and Rajabpour, A (2017) Effect of host plants on predation, prey preference and switching behaviour of Orius albidipennis on Bemisia tabaci and Tetranychus turkestani. International Journal of Tropical Insect Science 37, 176–182.CrossRefGoogle Scholar
Berlinger, MJ (1986) Host plant resistance to Bemisia tabaci. Agricultural Ecosystem and Environment 17, 69–82.CrossRefGoogle Scholar
Butt, TM (2002) Use of entomogenous fungi for the control of insect pests. In Kempken, F (ed.), Agricultural Applications. Heidelberg: Springer, pp. 111–134.CrossRefGoogle Scholar
Castillo, MA, Moya, P, Hernández, E and Primo-Yufera, E (2000) Susceptibility of Ceratitis capitata Wiedemann (Diptera: Tephritidae) to entomopathogenic fungi and their extracts. Biological Control 19, 274–282.CrossRefGoogle Scholar
Chiriví-Salomón, JS, Danies, G, Restrepo, S and Sanjuan, T (2015) Lecanicillium sabanense sp. nov. (Cordycipitaceae) a new fungal entomopathogen of coccids. Phytotaxa 234, 63–74.CrossRefGoogle Scholar
Cuthbertson, AG and Walters, KF (2005) Pathogenicity of the entomopathogenic fungus, Lecanicillium muscarium, against the sweetpotato whitefly Bemisia tabaci under laboratory and glasshouse conditions. Mycopathologia 160, 315–319.CrossRefGoogle ScholarPubMed
Cuthbertson, AG, Walters, KF and Northing, P (2005) The susceptibility of immature stages of Bemisia tabaci to the entomopathogenic fungus Lecanicillium muscarium on tomato and verbena foliage. Mycopathologia 159, 23–29.CrossRefGoogle ScholarPubMed
Cuthbertson, AG, Blackburn, LF, Northing, P, Luo, W, Cannon, RJ and Walters, KF (2008) Further compatibility tests of the entomopathogenic fungus Lecanicillium muscarium with conventional insecticide products for control of sweetpotato whitefly, Bemisia tabaci on poinsettia plants. Insect Science 15, 355–360.CrossRefGoogle Scholar
Cuthbertson, AGS, Blackburn, LF, Northing, P, Luo, W, Cannon, RJC and Walters, KFA (2010) Chemical compatibility testing of the entomopathogenic fungus Lecanicillium muscarium to control Bemisia tabaci in glasshouse environment. International Journal of Environmental Science and Technology 7, 405–409.CrossRefGoogle Scholar
De Barro, PJ, Liu, SS, Boykin, LM and Dinsdale, AB (2011) Bemisia tabaci: a statement of species status. Annual Review of Entomology 56, 1–19.CrossRefGoogle ScholarPubMed
Espinosa, DJL, da Silva, IHS, Duarte, RT, Gonçalves, KC and Polanczyk, RA (2019) Potential of entomopathogenic fungi as biological control agents of whitefly (Bemisia tabaci biotype b) (Genn.) (Hemiptera: Aleyrodidae). Journal of Experimental Agriculture International 38, 1–8.CrossRefGoogle Scholar
Faria, M and Wraight, SP (2001) Biological control of Bemisia tabaci with fungi. Crop Protection 20, 767–778.CrossRefGoogle Scholar
Feng, MG, Poprawski, TJ and Khachatourians, GG (1994) Production, formulation and application of the entomopathogenic fungus Beauveria bassiana for insect control: current status. Biocontrol Science and Technology 4, 3–34.CrossRefGoogle Scholar
Finney, DJ (1971) Probit Analysis, 3rd Edn. Cambridge, UK: Cambridge University Press.Google Scholar
Gao, L (2018) Optimization of nutritional and environmental conditions for biomass production and sporulation of entomogenous fungus Lecanicillium lecanii CA-1-G using two-stage cultivation system. Journal of Yeast and Fungal Research 9, 14–20.Google Scholar
Gao, L, Liu, XZ, Sun, MH, Li, SD and Wang, JL (2009) Use of a novel two-stage cultivation method to determine the effects of environmental factors on the growth and sporulation of several biocontrol fungi. Mycoscience 50, 317–321.CrossRefGoogle Scholar
Goettel, MS, Koike, M, Kim, JJ, Aiuchi, D, Shinya, R and Brodeur, J (2008) Potential of Lecanicillium spp. for management of insects, nematodes and plant diseases. Journal of Invertebrate Pathology 98, 256–261.CrossRefGoogle ScholarPubMed
Hillis, DM and Dixon, MT (1991) Ribosomal DNA: molecular evolution and phylogenetic inference. The Quarterly Review of Biology 66, 411–426.CrossRefGoogle ScholarPubMed
Humber, RA (1997) Fungi identification. In Lacey, L (ed.), Manual of Techniques in Insect Pathology. San Diego: Academic Press, pp. 153–185.CrossRefGoogle Scholar
Keerio, AU, Nazir, T, Abdulle, YA, Jatoi, GH, Gadhi, MA, Anwar, T, Sokea, T and Qiu, D (2020) In vitro pathogenicity of the fungi Beauveria bassiana and Lecanicillium lecanii at different temperatures against the whitefly, Bemisia tabaci (Genn.) (Hemiptera: Aleyrodidae). Egyptian Journal of Biological Pest Control 30, 1–9.CrossRefGoogle Scholar
Kepler, RM, Luangsa-ard, JJ, Hywel-Jones, NL, Quandt, CA, Sung, GH, Rehner, SA, Aime, MC, Henkel, TW, Sanjuan, T, Zare, R, Chen, MJ, Li, ZZ, Rossman, AY, Spatafora, JW and Shrestha, B (2017) A phylogenetic-based nomenclature for Cordycipitaceae (Hypocreales). Ima Fungus 8, 335–353.CrossRefGoogle Scholar
Khan, S, Guo, L, Maimaiti, Y, Mijit, M and Qiu, D (2012) Entomopathogenic fungi as microbial biocontrol agent. Molecular Plant Breeding 3, 63–79.Google Scholar
Kouvelis, VN, Sialakouma, A and Typas, MA (2008) Mitochondrial gene sequences alone or combined with ITS region sequences provide firm molecular criteria for the classification of Lecanicillium species. Mycological Research 112, 829–844.CrossRefGoogle ScholarPubMed
Kumar, CS, Jacob, TK, Devasahayam, S, D'Silva, S and Kumar, NK (2015) Isolation and characterization of a Lecanicillium psalliotae isolate infecting cardamom thrips (Sciothrips cardamomi) in India. BioControl 60, 363–373.CrossRefGoogle Scholar
Lacey, LA and Shapiro-Ilan, DI (2008) Microbial control of insect pests in temperate orchard systems: potential for incorporation into IPM. Annual Review of Entomology 53, 121–144.CrossRefGoogle ScholarPubMed
Lazreg, F, Huang, Z, Ali, S and Ren, S (2009) Effect of Lecanicillium muscarium on Eretmocerus sp. nr. furuhashii (Hymenoptera: Aphelinidae), a parasitoid of Bemisia tabaci (Hemiptera: Aleyrodidae). Journal of Pest Science 82, 27–32.CrossRefGoogle Scholar
Litwin, A, Nowak, M and Różalska, S (2020) Entomopathogenic fungi: unconventional applications. Reviews in Environmental Science and Biotechnology 19, 1–20.CrossRefGoogle Scholar
Liu, W, Xie, Y, Xue, J, Gao, Y, Zhang, Y, Zhang, X and Tan, J (2009) Histopathological changes of Ceroplastes japonicus infected by Lecanicillium lecanii. Journal of Invertebrate Pathology 101, 96–105.CrossRefGoogle ScholarPubMed
Luz, C, Mnyone, LL, Sangusangu, R, Lyimo, IN, Rocha, LF, Humber, RA and Russell, TL (2010) A new resting trap to sample fungus-infected mosquitoes, and the pathogenicity of Lecanicillium muscarium to culicid adults. Acta Tropica 116, 105–107.CrossRefGoogle ScholarPubMed
Manfrino, GR, Schuster, C, Saar, K, López Lastra, CC and Leclerque, A (2019) Genetic characterization, pathogenicity and benomyl susceptibility of Lecanicillium fungal isolates from Argentina. Journal of Applied Entomology 143, 204–213.CrossRefGoogle Scholar
Marshall, RK, Lester, MT, Glare, TR and Christeller, JT (2003) The fungus, Lecanicillium muscarium, is an entomopathogen of passionvine hopper (Scolypopa australis). New Zealand Journal of Crop and Horticultural Science 31, 1–7.CrossRefGoogle Scholar
Martin, JH (1987) An identification guide to common whitefly pest species of the world (Homopt., Aleyrodidae). International Journal of Pest Management 33, 298–322.Google Scholar
Mohammadi, S, Seraj, AA and Rajabpour, A (2015) Evaluation of six cucumber greenhouse cultivars for resistance to Tetranychus turkestani (Acari: Tetranychidae). Journal of Crop Protection 4, 545–556.Google Scholar
Mohammadipour, A, Ghazavi, M, Bagdadi, A and Zare, R (2010) Efficacy of entomopathogenic fungi Lecanicillium muscarium and L. aphanocladii against Russian wheat aphid Diuraphis noxia (Mordvilko) (Homoptera: Aphididae) on the laboratory condition. p. 56 in 19th Iranian Plant Protection Congress, July 31–3 August, Tehran, Iran, Plant Protection Research Institute.Google Scholar
Oliveira, MRV, Henneberry, TE and Anderson, P (2001) History, current status, and collaborative research projects for Bemisia tabaci. Crop Protection 20, 709–723.CrossRefGoogle Scholar
Ortiz-Urquiza, A and Keyhani, NO (2013) Action on the surface: entomopathogenic fungi versus the insect cuticle. Insects 4, 357–374.CrossRefGoogle ScholarPubMed
Osborne, LS and Landa, Z (1992) Biological control of whiteflies with entomopathogenic fungi. Florida Entomologist 75, 456–456.CrossRefGoogle Scholar
Palumbo, JC, Horowitz, AR and Prabhaker, N (2001) Insecticidal control and resistance management for Bemisia tabaci. Crop Protection 20, 739–765.CrossRefGoogle Scholar
Pantou, MP, Strunnikova, OK, Shakhnazarova, VY, Vishnevskaya, NA, Papalouka, VG and Typas, MA (2005) Molecular and immunochemical phylogeny of Verticillium species. Mycological Research 109, 889–902.CrossRefGoogle ScholarPubMed
Park, H and Kim, K (2010) Selection of Lecanicillium strains with high virulence against developmental stages of Bemisia tabaci. Mycobiology 38, 210–214.CrossRefGoogle ScholarPubMed
Pedigo, LP (2002) Entomology and Pest Management. New York, USA : Iowa University Press.Google Scholar
Petch, T (1925) Studies in entomogenous fungi. IX. Aegerita. Transactions of the British Mycological Society 10, 152.182.CrossRefGoogle Scholar
Petch, T (1931) New species of fungi collected during the Whitby Foray. The Naturalist London 21, 102–103.Google Scholar
Prasad, CS and Pal, R (2014) Mass production and economics of entomopathogenic fungus, Beauveria bassiana, Metarhizium anisopliae and Verticillium lecanii on agricultural and industrial waste. Scholars Journal of Agriculture and Veterinary Sciences 1, 28–32.Google Scholar
Rehner, SA, Minnis, AM, Sung, GH, Luangsa-ard, JJ, Devotto, L and Humber, RA (2011) Phylogeny and systematics of the anamorphic, entomopathogenic genus Beauveria. Mycologia 103, 1055–1073.CrossRefGoogle ScholarPubMed
Ren, SX, Ali, S, Huang, Z and Wu, JH (2010) Lecanicillium muscarium as microbial insecticide against whitefly and its interaction with other natural enemies. Microbiology and Microbial Biotechnology 27, 339–348.Google Scholar
Robertson, JL, Russel, HK, Preisler, HK and Savin, NE (2007) Bioassays with Arthropods. Boca Raton, Florida, USA: CRC Press.CrossRefGoogle Scholar
Romero, MGY and de Romero, ER (1986) Effects of two culture media on mycelial growth and on conidia yield and germination ability of Verticillium lecanii (Zimm.) Viegas. Revista de Investigacion, Centro de Investigaciones para la Regulacion de Poblaciones de Organismos Nocivos, Argentina 4, 27–39.Google Scholar
Safaei, N, Rajabpour, A and Seraj, AA (2016) Evaluation of various diets and oviposition substrates for rearing Orius albidipennis Reuter. Entomological Society of Iran 35, 29–37.Google Scholar
Saito, T and Sugiyama, K (2005) Pathogenicity of three Japanese strains of entomopathogenic fungi against the silverleaf whitefly, Bemisia argentifolii. Applied Entomology and Zoology 40, 169–172.CrossRefGoogle Scholar
Salazar, O, Schneider, JH, Julian, MC, Keijer, J and Rubio, V (1999) Phylogenetic subgrouping of Rhizoctonia solani AG2 isolates based on ribosomal ITS sequences. Mycologia 91, 459–467.CrossRefGoogle Scholar
Sani, I, Ismail, SI, Abdullah, S, Jalinas, J, Jamian, S and Saad, N (2020) A review of the biology and control of whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae), with special reference to biological control using entomopathogenic fungi. Insects 11, 619.CrossRefGoogle Scholar
Shah, PA and Pell, JK (2003) Entomopathogenic fungi as biological control agents. Applied Microbiology and Biotechnology 61, 413–423.CrossRefGoogle ScholarPubMed
Shahbi, M and Rajabpour, A (2017) A fixed-precision sequential sampling plan for the potato tuberworm moth, Phthorimaea operculella Zeller (Lepidoptera: Gelechidae), on potato cultivars. Neotropical Entomology 46, 388–395.CrossRefGoogle Scholar
Sun, MH, Gao, L, Liu, XZ and Wang, JL (2009) Fungal sporulation in two-stage cultivation. Mycosystema 28, 64–72.Google Scholar
Tabadkani, SM, Askary, H, Mehrasa, A and Ashouri, A (2010) Study on pathogencity effects of the entomophagous fungi Lecanicillium muscarium on the greenhouse whitefly Trialeurodes vaporariorum. p. 89. in 19th Iranian Plant Protection Congress, July 31–3 August, Tehran, Iran, Plant Protection Research Institute.Google Scholar
Thomas, MB and Read, AF (2007) Can fungal biopesticides control malaria? Nature Reviews Microbiology 5, 377–383.CrossRefGoogle ScholarPubMed
Thompson, WMO (2011) The Whitefly, Bemisia tabaci (Homoptera: Aleyrodidae). Interaction with Gemnivirus-Infected Host Plants. Netherland: Springer.CrossRefGoogle Scholar
Throne, JE, Weaver, DK, Chew, V and Baker, JE (1995) Probit analysis of correlated data: multiple observations over time at one concentration. Journal of Economic Entomology 88, 1510–1512.CrossRefGoogle Scholar
Vuillemin, P (1912) Beauveria, nouveau genre de Verticilliacées. Bulletin de la Société Botanique de France 59, 34–40.CrossRefGoogle Scholar
Wang, L, Huang, J, You, M and Liu, B (2004) Time-dose-mortality modelling and virulence indices for six strains of Verticillium lecanii against sweetpotato whitefly, Bemisia tabaci (Gennadius). Journal of Applied Entomology 128, 494–500.CrossRefGoogle Scholar
White, TJ, Bruns, TD, Lee, S and Taylor, J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In Innis, MA, Gelfand, DH, Sninsky, JJ and White, TJ (eds), PCR Protocols. San Diego: Academic Press, pp. 315–322.Google Scholar
Wize, C (1904) Die durch Pilze hervorgerufenen Krankheiten des Rubenrusselkafers (Cleonus punctioentris Germ.) mit besonderer Beriicksichtigung neuer Arten. Bulletin international de l'Académie des sciences de Cracovie 22, 713–727.Google Scholar
Wraight, SP, Carruthers, R, Bradley, CA, Jaronski, ST, Lacey, LA, Wood, P and Galaini-Wraight, S (1998) Pathogenicity of the entomopathogenic fungi Paecilomyces spp. and Beauveria bassiana against the silverleaf whitefly, Bemisia argentifolii. Journal of Invertebrate Pathology 71, 217–226.CrossRefGoogle ScholarPubMed
Xie, T, Jiang, L, Li, J, Hong, B, Wang, X and Jia, Y (2019) Effects of Lecanicillium lecanii strain JMC-01 on the physiology, biochemistry, and mortality of Bemisia tabaci Q-biotype nymphs. PeerJ 7, e7690.CrossRefGoogle ScholarPubMed
Zare, R and Gams, W (2001) A revision of Verticillium section Prostrata. IV. The genera Lecanicillium and Simplicillium. Nova Hedwigia 73, 1–50.CrossRefGoogle Scholar
Zare, R and Gams, W (2004) A monograph of Verticillium section Prostata. Rostaniha 3, 1–188.Google Scholar
Zare, R, Gams, W and Culham, A (2000) A revision of Verticillium sect. Prostrata. I. Phylogenetic studies using ITS sequences. Nova Hedwigia 71, 465–480.CrossRefGoogle Scholar
Zhu, H and Kim, JJ (2011) Susceptibility of the tobacco whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae) biotype Q to entomopathogenic fungi. Biocontrol Science and Technology 21, 1471–1483.CrossRefGoogle Scholar
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