Abstract
The tomato leafminer, Tuta absoluta (Meyrick) is an invasive pest of tomatoes spread rapidly and the damage caused by its larvae has received great attention for its management in tomato-growing regions of the world. In India, it was reported recently and spread fast throughout the whole country. To overcome this problem attempt was made to identify an entomopathogenic fungus and its pathogenicity tested against T. absoluta for sustainable pest management. In the present study, a fungus was isolated from the soil using the Galleria bait method and was characterized morphologically and with phylogenetic analysis, it turned out to be a Simplicillium obclavatum (Hypocreales: Cordycipitaceae). Its pathogenicity was evaluated against T. absoluta in the laboratory and the result showed 50.83 ± 2.29% mortality towards fourth instar larvae at 1.0 × 1010 fungal concentration after seven days of incubation. This report thus demonstrates the pathogenic nature of this newly isolated S. obclavatum from native soil and its efficay. To our understanding, this is the first report of S. obclavatum infecting T. absoluta from India.
References
Akutse KS, Subramanian S, Khamis FM, Ekesi S, Mohamed SA (2020) Entomopathogenic fungus isolates for adult Tuta absoluta (Lepidoptera: Gelechiidae) management and their compatibility with Tuta pheromone. J Appl Entomol 144(9):777–787. https://doi.org/10.1111/jen.12812
Bali GK, Singh SK, Chauhan VK, Joshi N, Bhat FA, Malla WA, Ramanujam B, Varshney R, Kour M, Pandit RS (2022a) An insight in proteome profiling of Tuta absoluta larvae after entomopathogenic fungal infection. Sci Data 9(1):1–7. https://doi.org/10.1038/s41597-022-01593-y
Bali GK, Singh SK, Maurya DK, Wani FJ, Pandit RS (2022b) Morphological and molecular identification of the entomopathogenic fungus purpureocillium lilacinum and its virulence against Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) larvae and pupae. Egypt J Biol Pest Control 32:86. https://doi.org/10.1186/s41938-022-00582-y
Biondi A, Guedes RNC, Wan FH, Desneux N (2018) Ecology, worldwide spread, and management of the invasive south american tomato pinworm, Tuta absoluta: past, present, and future. Ann Rev Entomol 63(1):239–258. https://doi.org/10.1146/annurev-ento-031616-034933
Brownbridge M, Humber RA, Parker BL, Skinner M (1993) Fungal entomopathogens recovered from Vermont forest soils. Mycologia 85(3):358–361. https://doi.org/10.1080/00275514.1993.12026285
Butt TM, Coates CJ, Dubovskiy IM, Ratcliffe NA (2016) Entomopathogenic fungi: new insights into host-pathogen interactions. Adv Genet 1(94):307–364. https://doi.org/10.1016/bs.adgen.2016.01.006
Chen RS, Huang CC, Li JC, Tsay JG (2017) Evaluation of characteristics of Simplicillium lanosoniveum on pathogenicity to aphids and in vitro antifungal potency against plant pathogenic fungi. Int J Environ Sci Agric Res 3(1):2454–1850
Chen WH, Liu C, Han YF, Liang JD, Tian WY, Liang ZQ (2019) Three novel insect-associated species of simplicillium (Cordycipitaceae, Hypocreales) from Southwest China. MycoKeys 58:83. https://doi.org/10.3897/mycokeys.58.37176
Damalas CA, Eleftherohorinos IG (2011) Pesticide exposure, safety issues, and risk assessment indicators. Int J Environ Res Public Health 8(5):1402–1419. https://doi.org/10.3390/ijerph8051402
Desneux N, Wajnberg E, Wyckhuys KA, Burgio G, Arpaia S, Narváez-Vasquez CA, González-Cabrera J, Catalán Ruescas D, Tabone E, Frandon J, Pizzol J (2010) Biological invasion of european tomato crops by Tuta absoluta: ecology, geographic expansion and prospects for biological control. J Pest Sci 83(3):197–215. https://doi.org/10.1007/s10340-010-0321-6
Desneux N, Han P, Mansour R, Arnó J, Brévault T, Campos MR et al (2021) Integrated pest management of Tuta absoluta: practicalimplementations across different world regions. J Pest Sci 95:17–39. https://doi.org/10.1007/s10340-021-01442-8
Dong QL, Lin TY, Xing XY, Chen B, Han Y (2014) Identification of a symbiotic fungus from blue-green alga and its extracellular polysaccharide. Lett Appl Microbiol 58(4):303–310. https://doi.org/10.1111/lam.12192
Dornburg A, Townsend JP, Wang Z (2017) Maximizing power in phylogenetics and phylogenomics: a perspective the illuminated by fungal big data. Adv Genet 100:1–47. https://doi.org/10.1016/Bs.Adgen.2017.09.007
EPPO (2021) https://gd.eppo.int/taxon/GNORAB/distribution. Accessed 4 Oct 2022
Guedes RN, Roditakis E, Campos MR, Haddi K, Bielza P, Siqueira HA, Tsagkarakou A, Vontas J, Nauen R (2019) Insecticide resistance in the tomato pinworm Tuta absoluta: patterns, spread, mechanisms, management and outlook. J Pest Sci 92:1329–1342. https://doi.org/10.1007/s10340-019-01086-9
Hajek AE, St. Leger RJ (1994) Interactions between fungal pathogens and insect hosts. Annu Rev Entomol 39(1):293–322. https://doi.org/10.1146/annurev.en.39.010194.001453
Han P, Bayram Y, Shaltiel-Harpaz L, Sohrabi F, Saji A et al (2019) Tuta absoluta continues to disperse in Asia: damage, ongoing management and future challenges. J Pest Sci 92(4):1317–1327. https://doi.org/10.1007/s10340-018-1062-1
Hyde KD, Xu J, Rapior S, Jeewon R, Lumyong S, Niego AGT, Abeywickrama PD, Aluthmuhandiram JV, Brahamanage RS, Brooks S, Chaiyasen A (2019) The amazing potential of fungi: 50 ways we can exploit fungi industrially. Fungal Divers 97:1–136. https://doi.org/10.1007/s13225-019-00430-9
Inglis GD, Goettel MS, Butt TM, Strasser S (2001) Use of hyphomycetous fungi for managing insect pests. In: Butt TM, Jackson C, Magan N (eds) Fungi as biocontrol agents: progress, problems, and potential. CABI Publishing, Wallingford, pp 23–69
Kornerup A, Wanscher JH (1978) Methuen handbook of color. Eyre Methuen, London
Lahiri S, Orr D (2018) Biological control in tomato production systems. Sustain Manag Arthropod Pests Tomato 253–267. https://doi.org/10.1016/b978-0-12-802441-6.00011-5
Leemon DM, Jonsson NN (2008) Laboratory studies on australian isolates of Metarhizium anisopliae as a biopesticide for the cattle tick Boophilus microplus J Invertebr Pathol 97(1):40–49. https://doi.org/10.1016/j.jip.2007.07.006
Liang X, Zhang XY, Nong XH, Wang J, Huang ZH, Qi SH (2016) Eight linear peptides from the deep-sea-derived fungus simplicillium obclavatum EIODSF 020. Tetrahedron 72(22):3092–3097. https://doi.org/10.1016/j.tet.2016.04.032
Lietti MM, Botto E, Alzogaray RA (2005) Insecticide resistance in Argentine populations of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Neotrop Entomol 34:113–119. https://doi.org/10.1590/S1519-566X2005000100016
Lim SY, Lee S, Kong HG, Lee J (2014) Entomopathogenicity of Simplicillium lanosoniveum isolated in Korea. Mycobiology 42(4):317–321
Liu F, Cai L (2012) Morphological and molecular characterization of a novel species of Simplicillium from China. Cryptogam Mycol 33(2):137–145. https://doi.org/10.7872/crym.v33.iss2.2012.137
Meyling NV (2007) Methods for isolation of entomopathogenic fungi from the soil environment. Manual for Isolation of Soil Borne Entomopathogenic Fungi 1–18
Medo J, CagáňL, (2011) Factors affecting the occurrence of entomopathogenic fungi in soils of Slovakia as revealed using two methods. Biol Control 59(2):200–208. https://doi.org/10.1016/j.biocontrol.2011.07.020
Pereyra PC, Sánchez NE (2006) Effect of two solanaceous plants on developmental and population parameters of the tomato leaf miner, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Neotrop Entomol 35:671–676. https://doi.org/10.1590/s1519-566x2006000500016
Ponti L, Gutierrez AP, de Campos MR, Desneux N, Biondi A, Neteler M (2021) Biological invasion risk assessment of Tuta absoluta: mechanistic versus correlative methods. Biol Invasions 23(12):3809–3829. https://doi.org/10.1007/s10530-021-02613-5
Rehner SA, Samuels GJ (1994) Taxonomy and phylogeny of Gliocladium analysed from nuclear large subunit ribosomal DNA sequences. Mycol Res 98(6):625–634. https://doi.org/10.1016/S0953-7562(09)80409-7
Roditakis E, Vasakis E, Grispou M, Stavrakaki M, Nauen R, Gravouil M, Bassi A (2015) First report of Tuta absoluta resistance to diamide insecticides. J Pest Sci 88(1):9–16. https://doi.org/10.1007/s10340-015-0643-5
Rombach MC, Humber RA, Evans HC (1987) Metarhizium album, a fungal pathogen of leaf-and planthoppers of rice. Trans Br Mycol Soc 88(4):451–459. https://doi.org/10.1016/S0007-1536(87)80028
Salazar ER, Araya JE (2001) Tomato moth, Tuta absoluta (Meyrick) response to insecticides in Arica. Chile Agric Técnica 61(4):429–435. https://doi.org/10.4067/S0365-28072001000400004
SAS Institute (2011) SAS version 9.3 system options: reference, 2nd edn. SAS Institute, Cary
Scheepmaker JWA, Butt TM (2010) Natural and released inoculum levels of entomopathogenic fungal biocontrol agents in soil in relation to risk assessment and in accordance with EU regulations. Biocontrol Sci Technol 20:503–552. https://doi.org/10.1080/09583150903545035
Skaptsov M., Smirnov S., Kutsev M., Uvarova O., Sinitsyna T., Shmakov A., Matsyura A. (2017) Pathogenicity of Simplicillium lanosoniveum to Coccus hesperidum. Ukrainian Journal of Ecology 7(4):689–691. https://doi.org/10.15421/2017_1801
Sun Z, Wu W, Zhang G (2019) Characterization of novel β-1,3-glucan recognition proteins from a tibetan Plateau ghost moth Thitarodes pui (Lepidoptera, Hepialidae). Physiol Entomol 44:20–32. https://doi.org/10.1111/phen.12272
Urbaneja A, González-Cabrera J, Arno J, Gabarra R (2012) Prospects for the biological control of Tuta absoluta in tomatoes of the Mediterranean basin. Pest Manag Sci 68(9):1215–1222. https://doi.org/10.1002/ps.3344
Vega FE, Goettel MS, Blackwell M, Chandler D, Jackson MA, Keller S, Koike M, Maniania NK, Monzón A, Ownley BH, Pell JK, Rangel DEN, Roy HE (2009) Fungal entomopathogens: new insights on their ecology. Fungal Ecol 2(4):149–159. https://doi.org/10.1016/j.funeco.2009.05.001
Wang N, Fan X, Zhang S, Liu B, He M, Chen X, Tang C, Kang Z, Wang X (2020) Identification of a Hyperparasitic Simplicillium obclavatum strain affecting the infection dynamics of Puccinia striiformis f. sp. tritici on Wheat. Front Microbiol 24(11):1277. https://doi.org/10.3389/fmicb.2020.01277
Wei DP, Wanasinghe DN, Hyde KD, Mortimer PE, Xu J, Xiao YP, Bhunjun CS, To-Anun C (2019) The genus simplicillium MycoKeys 60:69. https://doi.org/10.3897/mycokeys.60.38040
West C, Gwinn K (1993) Role of Acremonium in drought, pest, and disease tolerance grasses. In: Humne DE, Latch GCM, Easton HS (eds) Proceedings of the Second International Symposium on Acremonium/ Grass Interactions. (Palemerston North, New Zealand: Plenary papers), 131–140
White TJ, Burns T, Lee S, Taylor J (1990) Amplification and Direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protoc Guide Methods Appl 18:315–322. https://doi.org/10.1016/b978-0-12-372180-8.50042-1
Yan JF, Broughton SJ, Yang SL, Gange AC (2015) Do endophytic fungi grow through their hosts systemically? Fungal Ecol 13:53–59. https://doi.org/10.1016/j.funeco.2014.07.005
Zare R, Gams W (2008) A revision of the Verticillium fungicola species complex and its affinity with the genus lecanicillium Mycol Res 112(7):811–824. https://doi.org/10.1016/j.mycres.2008.01.019
Zare R, Gams W (2001) A revision of Verticillium section Prostrata. IV. The genus lecanicillium and simplicillium gen. nov. Nova Hedwigia 73:1–50
Zimmermann G (1986) The ‘Galleria bait method’ for detection of entomopathogenic fungi in soil. J Appl Entomol 102(5):213–215. https://doi.org/10.1111/j.1439-0418.1986.tb00912.x
Zimmermann G (2007) Review on safety of the entomopathogenic fungi Beauveria bassiana and Beauveria brongniartii Biocontrol Sci Technol 17(6):553–596. https://doi.org/10.1080/09583150701309006
Acknowledgements
Senior author is thankful to the Savitribai Phule Pune University, Pune, for providing a fellowship to conduct research work. The authors are also thankful to ICAR-National Bureau of Agriculturally Insect Resources, Bengaluru, and the Director, MACS-Agharkar Research Institute, Pune, for providing facilities and assistance throughout this study.
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Bali, G.K., Maurya, D.K., Singh, S.K. et al. Morphology, phylogeny, and pathogenicity of Simplicillium obclavatum (Hypocreales: Cordycipitaceae) against tomato leafminer, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Int J Trop Insect Sci 43, 355–361 (2023). https://doi.org/10.1007/s42690-023-00944-5
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DOI: https://doi.org/10.1007/s42690-023-00944-5