Adipokinetic Hormones Enhance the Efficacy of the Entomopathogenic Fungus Isaria fumosorosea in Model and Pest Insects
Abstract
:1. Introduction
2. Results
2.1. Effect of Isaria on Mortality
2.2. Effect of Isaria on AKH Transcript Abundance
2.3. Effect of Isaria on Carbon Dioxide Production and Metabolic Levels
3. Discussion
3.1. Effect of Isaria and Externally Applied AKHs on Mortality and Metabolism
3.2. Effect of Isaria on the Synthesis of Intrinsic AKHs
4. Materials and Methods
4.1. Insects and Their Rearing
4.2. Entomopathogenic Fungus Isaria fumosorosea
4.3. Insect Treatment and Dissection
4.4. Expression of Akh Genes
4.4.1. Isolation of RNA and cDNA Synthesis
4.4.2. Quantification of Akh Gene Expressions
4.5. Quantification of AKHs
4.6. Metabolic Rate Determination
4.7. Statistical Analyses and Data Presentation
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Meyling, N.V.; Lübeck, M.; Buckley, E.P.; Eilenberg, J.; Rehner, S.A. Community composition, host range and genetic structure of the fungal entomopathogen Beauveria in adjoining agricultural and seminatural habitats. Mol. Ecol. 2009, 18, 1282–1293. [Google Scholar] [CrossRef] [PubMed]
- Zimmermann, G. The entomopathogenic fungi Isaria farinosa (formerly Paecilomyces farinosus) and the Isaria fumosorosea species complex (formerly Paecilomyces fumosoroseus): Biology, ecology and use in biological control. Biocontrol Sci. Technol. 2008, 18, 865–901. [Google Scholar] [CrossRef]
- Wize, M.C. Die durch Pilze hervorgerufenen Krankheiten des Rübenrusselka fers (Cleonus punctiventris Germ.) mit besonderer Berucksichtigung neuer Arten. In Bulletin International de l’Académie des Sciences de Cracovie, Classe des Sciences Mathématique et Naturelles; Polska Akademia Umiejętności: Cracovie, Poland, 1904; Bulletin Number 713727. [Google Scholar]
- Deshpande, M.V. Mycopesticide production by fermentation: Potential and challenges. Crit. Rev. Microbiol. 1999, 25, 229–243. [Google Scholar] [CrossRef]
- Ali, S.; Huang, Z.; Ren, S. Production of cuticle degrading enzymes by Isaria fumosorosea and their evaluation as a biocontrol agent against diamondback moth. J. Pest Sci. 2010, 83, 361–370. [Google Scholar] [CrossRef]
- Lord, J.C.; Anderson, S.; Stanley, D.W. Eicosanoids mediate Manduca sexta cellular response to the fungal pathogen Beauveria bassiana: A role for the lipoxygenase pathway. Arch. Insect Biochem. Physiol. 2002, 51, 46–54. [Google Scholar] [CrossRef] [PubMed]
- Jackson, M.A.; Payne, A.R.; Odelson, D.A. Liquid-culture production of blastospores of the bioinsecticidal fungus Paecilomyces fumosoroseus using portable fermentation equipment. J. Ind. Microbiol. Biotechnol. 2004, 31, 149–154. [Google Scholar] [CrossRef] [PubMed]
- Weng, Q.; Zhang, X.; Chen, W.; Hu, Q. Secondary metabolites and the risks of Isaria fumosorosea and Isaria farinosa. Molecules 2019, 24, 664. [Google Scholar] [CrossRef] [Green Version]
- Gäde, G.; Hoffmann, K.H.; Spring, J.H. Hormonal regulation in insects: Facts, gaps, and future directions. Physiol. Rev. 1997, 77, 963–1032. [Google Scholar] [CrossRef]
- Van der Horst, D.J.; Van Marrewijk, W.J.A.; Diederen, H.B. Adipokinetic hormones of insect: Release, signal transduction, and responses. Int. Rev. Cytol. 2001, 211, 179–240. [Google Scholar]
- Kodrík, D. Adipokinetic hormone functions that are not associated with insect flight. Physiol. Entomol. 2008, 33, 171–180. [Google Scholar] [CrossRef]
- Kodrík, D.; Bednářová, A.; Zemanová, M.; Krishnan, N. Hormonal regulation of response to oxidative stress in insects—An update. Int. J. Mol. Sci. 2015, 16, 25788–25816. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kim, S.K.; Rulifson, E.J. Conserved mechanisms of glucose sensing and regulation by Drosophila corpora cardiaca cells. Nature 2004, 431, 316–320. [Google Scholar] [CrossRef] [PubMed]
- Kodrík, D.; Plavšin, I.; Velki, M.; Stašková, T. Enhancement of insecticide efficacy by adipokinetic hormones. In Insecticides: Occurrence, Global Threats and Ecological Impact, 1st ed.; Montgomery, J., Ed.; Nova Science Publishers Inc.: New York, NY, USA, 2015; pp. 77–91. [Google Scholar]
- Goldsworthy, G.J.; Kodrík, D.; Comley, R.; Lightfoot, M. A quantitative study of the adipokinetic hormone of the firebug, Pyrrhocoris apterus. J. Insect Physiol. 2002, 48, 1103–1108. [Google Scholar] [CrossRef] [Green Version]
- Goldsworthy, G.J.; Chandrakant, S.; Opoku-Ware, K. Adipokinetic hormone enhances nodule formation and phenoloxidase activation in adult locusts injected with bacterial lipopolysaccharide. J. Insect Physiol. 2003, 49, 795–803. [Google Scholar] [CrossRef] [Green Version]
- Goldsworthy, G.J.; Mullen, L.M.; Opoku-Ware, K.; Chandrakant, S. Interactions between the endocrine end immune systems in locusts. Physiol. Entomol. 2003, 28, 54–61. [Google Scholar] [CrossRef] [Green Version]
- Gautam, U.K.; Bohatá, A.; Shaik, H.A.; Zemek, R.; Kodrík, D. Adipokinetic hormone promotes infection with entomopathogenic fungus Isaria fumosorosea in the cockroach Periplaneta americana. Comp. Biochem. Physiol. C 2020, 229, 108677. [Google Scholar] [CrossRef]
- Ibrahim, E.; Hejníková, M.; Shaik, H.A.; Doležel, D.; Kodrík, D. Adipokinetic hormone activities in insect body infected by entomopathogenic nematode. J. Insect Physiol. 2017, 98, 347–355. [Google Scholar] [CrossRef]
- Ibrahim, E.; Dobeš, P.; Kunc, M.; Hyršl, P.; Kodrík, D. Adipokinetic hormone and adenosine interfere with nematobacterial infection and locomotion in Drosophila melanogaster. J. Insect Physiol. 2018, 107, 167–174. [Google Scholar] [CrossRef]
- Shaik, H.A.; Mishra, A.; Kodrík, D. Beneficial effect of adipokinetic hormone on neuromuscular paralysis in insect body elicited by braconid wasp venom. Comp. Biochem. Physiol. C 2017, 196, 11–18. [Google Scholar] [CrossRef]
- Kodrík, D.; Bártů, I.; Socha, R. Adipokinetic hormone (Pyrap-AKH) enhances the effect of a pyrethroid insecticide against the firebug Pyrrhocoris apterus. Pest Manag. Sci. 2010, 66, 425–431. [Google Scholar] [CrossRef]
- Velki, M.; Kodrík, D.; Večeřa, J.; Hackenberger, B.K.; Socha, R. Oxidative stress elicited by insecticides: A role for the adipokinetic hormone. Gen. Comp. Endocrinol. 2011, 172, 77–84. [Google Scholar] [CrossRef] [PubMed]
- Plavšin, I.; Stašková, T.; Šerý, M.; Smýkal, V.; Hackenberger, H.K.; Kodrík, D. Hormonal enhancement of insecticide efficacy in Tribolium castaneum: Oxidative stress and metabolic aspects. Comp. Biochem. Physiol. C 2015, 170, 19–27. [Google Scholar] [CrossRef] [PubMed]
- Kodrík, D.; Socha, R.; Šimek, P.; Zemek, R.; Goldsworthy, G.J. A new member of the AKH/RPCH family that stimulates locomotory activity in the firebug, Pyrrhocoris apterus (Heteroptera). Insect Biochem. Mol. Biol. 2000, 30, 489–498. [Google Scholar] [CrossRef]
- Večeřa, J.; Krishnan, N.; Mithöfer, A.; Vogele, H.; Kodrík, D. Adipokinetic hormone-induced antioxidant response in Spodoptera littoralis. Comp. Biochem. Physiol. C 2012, 155, 389–395. [Google Scholar] [CrossRef]
- Jedlička, P.; Steinbauerová, V.; Šimek, P.; Zahradníčková, H. Functional characterization of the adipokinetic hormone in the pea aphid, Acyrthosiphon pisum. Comp. Biochem. Physiol. 2012, 162, 51–58. [Google Scholar] [CrossRef]
- Goldsworthy, G.J.; Opoku-Ware, K.; Mullen, L.M. Adipokinetic hormone and the immune responses of locusts to infection. Ann. N. Y. Acad. Sci. 2005, 1040, 106–113. [Google Scholar] [CrossRef]
- Mullen, L.M.; Goldsworthy, G.J. Immune responses of locusts to challenge with the pathogenic fungus Metarhizium or high doses of laminarin. J. Insect Physiol. 2006, 52, 389–398. [Google Scholar] [CrossRef]
- Kodrík, D.; Socha, R.; Zemek, R. Topical application of Pya-AKH stimulates lipid mobilization and locomotion in the flightless bug, Pyrrhocoris apterus (L.) (Heteroptera). Physiol. Entomol. 2002, 27, 15–20. [Google Scholar] [CrossRef]
- Sajwan, S.; Sidorov, R.; Stašková, T.; Žaloudíková, A.; Takasu, J.; Kodrík, D.; Žurovec, M. Targeted mutagenesis and functional analysis of adipokinetic hormone-encoding gene in Drosophila. Insect Biochem. Mol. Biol. 2015, 61, 79–86. [Google Scholar] [CrossRef]
- Carlisle, J.; Loughton, B.G. Adipokinetic hormone inhibits protein synthesis in locusta. Nature 1979, 282, 420–421. [Google Scholar] [CrossRef]
- Kodrík, D.; Goldsworthy, G.J. Inhibition of RNA synthesis by adipokinetic hormones and brain factor(s) in adult fat body of Locusta migratoria. J. Insect Physiol. 1995, 41, 127–133. [Google Scholar] [CrossRef]
- Lemaitre, B.; Hoffmann, J. The host defense of Drosophila melanogaster. Annu. Rev. Immunol. 2007, 25, 697–743. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Candy, D.J. Adipokinetic hormones concentrations in the haemolymph of Schistocerca gregaria, measured by radioimmunoassay. Insect Biochem. Mol. Biol. 2002, 32, 1361–1367. [Google Scholar] [CrossRef]
- Kodrík, D.; Krishnan, N.; Habuštová, O. Is the titer of adipokinetic peptides in Leptinotarsa decemlineata fed on genetically modified potatoes increased by oxidative stress? Peptides 2007, 28, 974–980. [Google Scholar] [CrossRef]
- Karbusová, N.; Gautam, U.K.; Kodrík, D. Effect of natural toxins and adipokinetic hormones on the activity of digestive enzymes in the midgut of the cockroach Periplaneta americana. Arch. Insect Biochem. Physiol. 2019, 101, e21586. [Google Scholar]
- Goldsworthy, G.J. Insect adipokinetic hormones: Are they the insect glucagons. In Perspectives in Endocrinology, Proceedings of XII. International Congress of Comparative Endocrinology, Toronto, Canada, 16–21 May 1993; Davey, K.G., Peter, R.E., Tobe, S.S., Eds.; National Research Council of Canada: Ottawa, ON, Canada, 1994; pp. 486–492. [Google Scholar]
- Kodrík, D.; Socha, R. The effect of insecticide on adipokinetic hormone titre in insect body. Pest Manag. Sci. 2005, 61, 1077–1082. [Google Scholar] [CrossRef]
- Zemek, R.; Prenerová, E.; Weyda, F. The first record of entomopathogenic fungus Paecilomyces fumosoroseus (Deuteromycota: Hyphomycetes) on the hibernating pupae of Cameraria ohridella (Lepidoptera: Gracillariidae). Entomol. Res. 2007, 37, A135–A136. [Google Scholar]
- Prenerová, E.; Zemek, R.; Weyda, F.; Volter, L. Strain of entomopathogenic fungus Isaria fumosorosea CCM 8367 (CCEFO.011.PFR) and the method of controlling insect and mite pests. U.S. Patent 08574566, 5 November 2013. [Google Scholar]
- Prenerová, E.; Zemek, R.; Weyda, F.; Volter, L. Strain of entomopathogenic fungus Isaria fumosorosea CCM 8367 (CCEFO.011.PFR) and the method for controlling insect and mite pests. EPO patent EP2313488, 29 April 2015. [Google Scholar]
- Pfaffl, M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001, 29, e45. [Google Scholar] [CrossRef]
- Jaffe, H.; Raina, A.K.; Riley, C.T.; Fraser, B.A.; Bird, T.G.; Tseng, C.M.; Zhang, Y.S.; Hayes, D.K. Isolation and primary structure of a neuropeptide hormone from Heliothis zea with hypertrehalosemic and adipokinetic activities. Biochem. Biophys. Res. Commun. 1988, 155, 344–350. [Google Scholar] [CrossRef]
- Gäde, G.; Marco, H.G.; Šimek, P.; Audsley, N.; Clark, K.D.; Weaver, R.J. Predicted versus expressed adipokinetic hormones, and other small peptides from the corpus cardiacum-corpus allatum: A case study with beetles and moths. Peptides 2008, 29, 1124–1139. [Google Scholar] [CrossRef]
- Ziegler, R.; Eckart, K.; Schwarz, H.; Keller, R. Amino acid sequence of Manduca sexta adipokinetic hormone elucidated by combined fast atom bombardment (FAB)/tandem mass spectrometry. Biochem. Biophys. Res. Commun. 1985, 133, 337–342. [Google Scholar] [CrossRef]
- Withers, P.C. Measurement of VO2, VCO2 and evaporative water loss with a flow-through mask. J. Appl. Physiol. 1977, 42, 120–123. [Google Scholar] [CrossRef] [PubMed]
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Gautam, U.K.; Hlávková, D.; Shaik, H.A.; Karaca, I.; Karaca, G.; Sezen, K.; Kodrík, D. Adipokinetic Hormones Enhance the Efficacy of the Entomopathogenic Fungus Isaria fumosorosea in Model and Pest Insects. Pathogens 2020, 9, 801. https://doi.org/10.3390/pathogens9100801
Gautam UK, Hlávková D, Shaik HA, Karaca I, Karaca G, Sezen K, Kodrík D. Adipokinetic Hormones Enhance the Efficacy of the Entomopathogenic Fungus Isaria fumosorosea in Model and Pest Insects. Pathogens. 2020; 9(10):801. https://doi.org/10.3390/pathogens9100801
Chicago/Turabian StyleGautam, Umesh Kumar, Daniela Hlávková, Haq Abdul Shaik, Ismail Karaca, Gürsel Karaca, Kazim Sezen, and Dalibor Kodrík. 2020. "Adipokinetic Hormones Enhance the Efficacy of the Entomopathogenic Fungus Isaria fumosorosea in Model and Pest Insects" Pathogens 9, no. 10: 801. https://doi.org/10.3390/pathogens9100801
APA StyleGautam, U. K., Hlávková, D., Shaik, H. A., Karaca, I., Karaca, G., Sezen, K., & Kodrík, D. (2020). Adipokinetic Hormones Enhance the Efficacy of the Entomopathogenic Fungus Isaria fumosorosea in Model and Pest Insects. Pathogens, 9(10), 801. https://doi.org/10.3390/pathogens9100801