Abstract
In the present investigation, hyperparasitic interaction between B. bassiana, TM (MH590235) and P. xylostella was studied through scanning electron microscopy and chromatographic techniques. Dose–mortality responses showed an increase in mortality of larva with an increase in spore concentration. The LC50 value for B. bassiana isolate TM (MH590235) was 2.4 × 107 spores mL−1. The ditrophic interaction between B. bassiana and P. xylostella after 24 h revealed the adherence of conidia on stemmata, sensory setae, maxillary palpi and legs. After 48 h post-infection (hpi), germination of the conidia and appressorium formation was observed. Formation of hyphae and initiation of fungal networking was observed at 72 hpi. Complete ramification by mycelia and conidiogenesis of B. bassiana was observed over the mycosed cadaver after 168 hpi. Subsequently, typical sympodial conidiophores of B. bassiana bearing secondary spores were also observed. The metabolome profile of healthy larvae of P. xylostella revealed the presence of non-volatile organic compounds (NVOCs) like docosene, nonadecene, palmitic acid and heneicosane. However, the NVOC profile was different in the P. xylostella larvae hyperparasitized by B. bassiana. The metabolites present in the infected cadaver were phthalate esters, hydroxyquebrachamine and lactones.
Similar content being viewed by others
References
Abbott WS (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18(2):265–267
Alali S, Mereghetti V, Faoro F, Bocchi S, Al Azmeh F, Montagna M (2019) Thermotolerant isolates of Beauveria bassiana as potential control agent of insect pest in subtropical climates. PloS one 14(2):e0211457
Ankersmit GW (1953) DDT-resistance in Plutella maculipennis (Curt.) (Lep.) in Java. Bull Entomol Res 44(3):421–425. https://doi.org/10.1017/S0007485300025530
AVRDC (2019) Proceedings of Eighth International Conference on Management of the Diamondback moth and other crucifer insect pests, 4–8 March 2019, Shanhua, Tainan, Taiwan, p 42. https://doi.org/10.2201/wvc.66831
Barta M (2018) In planta bioassay on the effects of endophytic Beauveria strains against larvae of horse-chestnut leaf miner (Cameraria ohridella). Biol Control 121:88–98. https://doi.org/10.1016/j.biocontrol.2018.02.013
Batcho A, Ali M, Samuel AO, Shehzad K, Rashid B (2018) Comparative study of the effects of five Beauveria bassiana (Balsamo) Vuillemin (Ascomycota: Hypocreales) strains on cabbage moth Plutella xylostella (L.) (Lepidoptera: Plutellidae). Cogent Environ Sci 4(1):1477542. https://doi.org/10.1080/23311843.2018.1477542
Bhutia YD, Jain N, Ahmed F, Sharma M, Singh R, Kumar S, Mendki MJ, Kumar P, Vijayaraghavan R (2010) Acute and sub-acute toxicity of an insect pheromone, N-heneicosane and combination with insect growth regulator, diflubenzuron, for establishing no observed adverse effect level (NOAEL). Indian J Exp Biol 48:744–751. http://hdl.handle.net/123456789/9742
Bidochka MJ, Kamp AM, De Cross JNA (2000) Insect pathogenic fungi: from genes to populations. In: Kronstad JW (ed) Fungal pathology. Kluwer Academic Press, pp 171–193
Boomsma JJ, Jensen AB, Meyling NV, Eilenberg J (2014) Evolutionary interaction networks of insect pathogenic fungi. Annu Rev Entomol 59:467–485. https://doi.org/10.1146/annurev-ento-011613-162054
Butt TM, Coates CJ, Dubovskiy IM, Ratcliffe NA (2016) Entomopathogenic fungi: new insights into host-pathogen interactions. In: Lovett B, St Leger RJ (eds) Genetics and molecular biology of entomopathogenic fungi. Academic Press, USA, pp 307–364
Charnley AK, St. Leger RJ. (1991) The role of cuticle-degrading enzymes in fungal pathogenesis in insects. In: Cole JT, Hoch HC (eds) The fungal spore and disease initiation in plants and animals. Springer, Boston, pp 267–286. https://doi.org/10.1007/978-1-4899-2635-7_12
Correa-Cuadros JP, Sáenz-Aponte A, Rodríguez-Bocanegra MX (2016) In vitro interaction of Metarhizium anisopliae Ma9236 and Beauveria bassiana Bb9205 with Heterorhabditis bacteriophora HNI0100 for the control of Plutella xylostella. Springerplus 5(1):2068. https://doi.org/10.1186/s40064-016-3745-5
Doss RP, Oliver JE, Proebsting WM, Potter SW, Kuy S, Clement SL, Williamson RT, Carney JR, DeVilbiss ED (2000) Bruchins: Insect-derived plant regulators that stimulate neoplasm formation. Proc Natl Acad Sci 97(11):6218–6223. https://doi.org/10.1073/pnas.110054697
Ferron P (1978) Biological control of insect pests by entomogenous fungi. Annu Rev Entomol 23:409–442. https://doi.org/10.1146/annurev.en.23.010178.002205
Finney D (1971) Probit analysis. Cambridge University Press
Gabarty A, Salem HM, Fouda MA, Abas AA, Ibrahim AA (2014) Pathogenicity induced by the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae in Agrotis ipsilon (Hufn.). J Radiat Res Appl Sc 7(1):95–100. https://doi.org/10.1016/j.jrras.2013.12.004
Gomez-Vidal S, Lopez-Llorca LV, Jansson HB, Salinas J (2006) Endophytic colonization of date palm (Phoenix dactylifera L.) leaves by entomopathogenic fungi. Micron 37:624–632. https://doi.org/10.1016/j.micron.2006.02.003
Grove JF, Pople M (1980) The insecticidal activity of beauvericin and the enniatin complex. Mycopathologia 70(2):103–105. https://doi.org/10.1007/BF00443075
Güerri-Agulló B, Gómez-Vidal S, Asensio L, Barranco P, Lopez-Llorca LV (2010) Infection of the red palm weevil (Rhynchophorus ferrugineus) by the entomopathogenic fungus Beauveria bassiana: a SEM study. Microsc Res Tech 73(7):714–725. https://doi.org/10.1002/jemt.20812
Gurunathan A, Senguttuvan J, Paulsamy S (2016) Evaluation of mosquito repellent activity of isolated oleic acid, eicosyl ester from Thalictrum javanicum. Indian J Pharm Sci 78(1):103–110
Holder DJ, Keyhani NO (2005) Adhesion of the entomopathogenic fungus Beauveria (Cordyceps) bassiana to substrates. Appl Environ Microbiol 71:5260–5266. https://doi.org/10.1128/AEM.71.9.5260-5266.2005
Kadhim MJ, Mohammed GJ, Hussein H (2016) Analysis of bioactive metabolites from Candida albicans using (GC-MS) and evaluation of antibacterial activity. Int J Pharm Clinical Res 8(7):655–670
Krishnakumar NK, Srinivasan K, Suman CL, Ramachander PR (1986) Optimum control strategy of cabbage pests from a chemical control trial. Progress Hortic 18:1040110
Leger RJS, Butt TM, Goettel MS, Staples RC, Roberts DW (1989) Production in vitro of appressoria by the entomopathogenic fungus Metarhizium anisopliae. Exp Mycol 13(3):274–288. https://doi.org/10.1016/0147-5975(89)90049-2
Lohse R, Jakobs-Schönwandt D, Vidal S, Patel AV (2015) Evaluation of new fermentation and formulation strategies for a high endophytic establishment of Beauveria bassiana in oilseed rape plants. Biol Control 88:26–36. https://doi.org/10.1016/j.biocontrol.2015.05.002
Lopez-Llorca LV, Olivares-Bernabeu C, Salinas J, Jansson HB, Kolattukudy PE (2002) Pre-penetration events in fungal parasitism of nematode eggs. Mycol Res 106:499–506. https://doi.org/10.1017/S0953756202005798
Mangold HK (ed) (2012) Ether lipids: biochemical and biomedical aspects. Elsevier, Academic Press, London
Neves PM, Alves SB (2004) External events related to the infection process of Cornitermes cumulans (Kollar) (Isoptera: Termitidae) by the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae. Neotrop Entomol 33(1):51–56. https://doi.org/10.1590/S1519-566X2004000100010
Oizumi K, Sekine S, Fukagai M, Susukida T, Ito K (2017) Identification of bile acids responsible for inhibiting the bile salt export pump, leading to bile acid accumulation and cell toxicity in rat hepatocytes. J Pharm Sci 106(9):2412–2419. https://doi.org/10.1016/j.xphs.2017.05.017
Özçelik FG, Güven Ö (2015) Morphological and molecular characterization of natural entomopathogenic fungi. Asian J Agric Food Sci 3(2):13 (ISSN:2321–1571)
Rohlfs M, Churchill ACL (2011) Fungal secondary metabolites as modulators of interactions with insects and other arthropods. Fungal Genet Biol 48(1):23–34. https://doi.org/10.1016/j.fgb.2010.08.008
Roy HE, Steinkraus DC, Eilenberg J, Hajek AE, Pell JK (2006) Bizarre interactions and endgames: entomopathogenic fungi and their arthropod hosts. Annu Rev Entomol 51:331–357. https://doi.org/10.1146/annurev.ento.51.110104.150941
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, New York, USA
Sanjaya Y, Virginia RO, Barbara LC (2015) Infection process of entomopathogenic fungi Beauveria bassiana in the Tetrancyhus kanzawai (Kishida) (Tetranychidae: Acarina). Arthropods 4(3):90–97
Sarfraz M, Keddie AB, Dosdall LM (2005) Biological control of the diamondback moth, Plutella xylostella: a review. Biocontrol Sci Technol 15(8):763–789. https://doi.org/10.1080/09583150500136956
Scott SA, Mathews TP, Ivanova PT, Lindsley CW, Brown HA (2014) Chemical modulation of glycerolipid signaling and metabolic pathways. Biochim Biophys Acta (BBA) - Mol Cell Biol Lipids 1841(8):1060–1084. https://doi.org/10.1016/j.bbalip.2014.01.009
Selman BJ, Dayer MS, Hasan M (1997) Pathogenicity of Beauveria bassiana (Bals.) Vuill. to the larvae of diamondback moth,Plutella xylostella L.(Lep., Yponomeutidae). J Appl Entomol 121(1–5):47–49. https://doi.org/10.1111/j.1439-0418.1997.tb01369.x
Shah PA, Pell JK (2003) Entomopathogenic fungi as biological control agents. Appl Microbiol Biotechnol 61:413–423. https://doi.org/10.1007/s00253-003-1240-8
Shaker NO, Ahmed GMM, Ibrahim HYE, El-Sawy MM, Mostafa ME, Ismail HNAE (2019) Secondary Metabolites of the Entomopathogenic Fungus, Cladosporium cladosporioides and its Relation to Toxicity of Cotton Aphid, Aphis gossypii (Glov). Int J Entomol Nematol 5(1):115–120
Silva-Valda CA, Barros-Reginaldo M-E, Torres-Jorge B (2003) Suscetibilidade de Plutella xylostella (L.) (Lepidoptera: Plutellidae) aos fungos Beauveria bassiana (Bals.) Vuill. e Metarhizium anisopliae (Metsch.) Sorok. Neotrop Entomol 32(4):653–658. https://doi.org/10.1590/S1519-566X2003000400016
Srivastara N, Maurya P, Sharma P, Mohan L (2009) Prospective role of insecticides of fungal origin: review. Entomol Res 39:341–355. https://doi.org/10.1111/j.1748-5967.2009.00244.x
Strasser H, Abendstein D, Stuppner H (2000) Monitoring the distribution of secondary metabolites produced by the entomogenous fungus Beauveria brongniartii with particular reference to oosporein. Mycol Res 104(10):1227–1233
Talekar NS, Shelton AM (1993) Biology, ecology, and management of the diamondback moth. Annu Rev Entomol 38(1):275–301. https://doi.org/10.1146/annurev.en.38.010193.001423
Tschinkel WR (1975) A comparative study of the chemical defensive system of tenebrionid beetles: chemistry of the secretions. J Insect Physiol 21(4):753–783. https://doi.org/10.1016/0022-1910(75)90008-6
Uma Devi K, Padmavathi J, Rao CUM, Khan AAP, Mohan MC (2008) A study of host specificity in the entomopathogenic fungus Beauveria bassiana (Hypocreales, Clavicipitaceae). Biocontrol Sci Technol 18(10):975–989. https://doi.org/10.1080/09583150802450451
Urbanek RA, Suchard SJ, Steelman GB, Knappenberger KS, Sygowski LA, Veale CA, Chapdelaine MJ (2001) Potent reversible inhibitors of the protein tyrosine phosphatase CD45. J Med Chem 44(11):1777–1793. https://doi.org/10.1021/jm000447i
Vinson SB (1991) Suppression of the insect immune system by parasitic Hymenoptera. In: Pathak JPN (ed) Insect Immunity. Kluwer Academic Publishers, Dordrecht, pp 171–187
Wakil W, Yasin M, Shapiro-Ilan D (2017) Effects of single and combined applications of entomopathogenic fungi and nematodes against Rhynchophorus ferrugineus (Olivier). Sci Rep 7(1). https://doi.org/10.1038/s41598-017-05615-3
Wang K, Yin J, Shen D, Li N (2014) Anaerobic digestion of food waste for volatile fatty acids (VFAs) production with different types of inoculum: effect of pH. Bioresour Technol 161:395–401. https://doi.org/10.1016/j.biortech.2014.03.088
Wraight SP, Ramos ME, Avery PB, Jaronski ST, Vandenberg JD (2010) Comparative virulence of Beauveria bassiana isolates against lepidopteran pests of vegetable crops. J Invertebr Pathol 103(3):186–199. https://doi.org/10.1016/j.jip.2010.01.001
Xia J, Huang Z, Hu Q (2013) Histopathological study of Plutella xylostella infected by three entomopathogenic fungal species. Adv Entomol 1(2):15–19. https://doi.org/10.4236/ae.2013.12004
Zalucki MP, Shabbir A, Silva R, Adamson D, Shu-Sheng L, Furlong MJ (2012) Estimating the economic cost of one of the world’s major insect pests, Plutella xylostella (Lepidoptera: Plutellidae): just how long is a piece of string? J Econ Entomol 105:1115–1129. https://doi.org/10.1603/EC12107
Acknowledgements
The first author thanks the Department of Science and Technology, Government of India for providing an INSPIRE fellowship (IF160933). The authors express their sincere thanks to the Department of Nanoscience and Technology of Tamil Nadu Agricultural University for technical assistance for SEM.
Author information
Authors and Affiliations
Contributions
NPR: Methodology, Investigation, Formal analysis, Writing—Original draft preparation, Funding acquisition. SM: Conceptualization, Resources, Data curation, Writing—Review and Editing, Supervision, Funding acquisition. SN: Conceptualization, Resources, Visualization, Investigation, Supervision. MS: Conceptualization, Visualization.
Corresponding author
Ethics declarations
Conflict of interest
Authors declare that they have no conflict of interests.
Human and animal rights
This article does not contain any studies with human participants or animals that require ethical approval.
Informed consent
Consent from all authors regarding contributions and authorship was obtained.
Rights and permissions
About this article
Cite this article
Nithya, P.R., Manimegalai, S., Nakkeeran, S. et al. Comparative study of the ditrophic interaction between Beauveria bassiana and Plutella xylostella. 3 Biotech 11, 223 (2021). https://doi.org/10.1007/s13205-021-02760-5
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s13205-021-02760-5