Skip to main content
Springer Nature Link
Log in

Evolutionary distinction between the geographical isolates of Beauveria bassiana from Iran and their efficacy against Helicoverpa armigera

  • Original Research Article
  • Published:
International Journal of Tropical Insect Science Aims and scope Submit manuscript

Abstract

Beauveria bassiana is a cosmopolitan and soil-borne fungus EPF which is widely used as a biological insecticide. Regarding the remarkable intraspecific variability amongst the B. bassiana isolates, for the first time, the evolutionary distinction between the geographical isolates of entomopathogenic fungi (EPF), Beauveria bassiana, belonging to two distinct geographical areas of Iran have been examined for taxonomic affiliation and their evolutionary distinction to other isolates. In total, 400 soil samples were randomly collected from different cultivated and non-cultivated areas of Khosroshahr and Jiroft region. Insect baiting technique was used to isolate entomopathogenic fungi from the soil. Six well-supported clades within the Beauveria were resolved in the ITS-rDNA phylogenies. Native Beauveria bassiana isolates were determined to be non-monophyletic and consist of three clades named A1, A2, and A3. No correlation was recorded between the geographical origins of the isolates and the topology of the phylogenetic tree. Results suggest that compared to other clades, the members in the clade A1 are representative of a genealogically distinct group of B. bassiana, presumably with higher fitness cause better establishment and persistence in different environments. From both geographical regions, six B. bassiana isolates belonging to phylogenetically distinct clades were subjected to bioassay against the larva of the Helicoverpa armigera as a major pest of cotton in Iran. Although the virulence of the isolates differed significantly, no obvious relationship was detected between the virulence of the isolates and their phylogenetic relatedness. Jiroft isolates showed lower virulence against larvae than did fungi from Khosroshar.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

Availability of data and materials

All data generated or analyzed in this study are available in this published manuscript.

References

  • Abbott, W. S. (1925). A method of computing the effectiveness of an insecticide. J Econ Entomol 18(2):265-267

  • Archer DB, Dyer PS (2004) From genomics to post-genomics in Aspergillus. Curr Opin Microbiol 7:499–504

    Article  CAS  PubMed  Google Scholar 

  • Bedding RA, Akhurst RJ (1975) A simple technique for the detection of insect parasitic rhabditid nematodes in soil. Nematologica 21:109–110

    Article  Google Scholar 

  • Bell-Pedersen D, Cassone VM, Earnest DJ, Golden SS, Hardin PE, Thomas TL, Zoran MJ (2005) Circadian rhythms from multiple oscillators: Lessons from diverse organisms. Nat Rev Genet 6:544–556

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Borkovich KA, Alex LA, Yarden O, Freitag M, Turner GE, Read ND, Plesofsky N (2004) Lessons from the genome sequence of Neurospora Crassa: tracing the path from genomic blueprint to multicellular organism. Microbiol Mol Biol Rev 68:1–108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bridge PD, Spooner BM, Roberts P (2005) The impact of molecular data in fungal systematics. Adv Bot Res 42:33–67. https://doi.org/10.1016/S0065-2296(05)42002-9

    Article  CAS  Google Scholar 

  • Bruns T, Shefferson R (2004) Evolutionary studies of ectomycorrhizal fungi: Recent advances and future directions. Can J Bot 82:1122–1132. https://doi.org/10.1139/b04-021

    Article  CAS  Google Scholar 

  • Bustamante DE, Oliva M, Leiva S, Mendoza JE, Bobadilla L, Angulo G, Calderon MS (2019) Phylogeny and species delimitations in the entomopathogenic genus Beauveria (Hypocreales, Ascomycota), including the description of B. peruviensis sp. nov. MycoKeys 58. https://doi.org/10.3897/mycokeys.58.35764

  • Castrillo LA, Griggs MH, Liu H, Bau LS, Vandenberg JD (2010) Assessing deposition and persistence of Beauveria bassiana GHA (Ascomycota: Hypocreales) applied for control of the emerald ash borer, Agrilus planipennis (Coleoptera: Buprestidae), in a commercial tree nursery. Biol Control 45:61–67

    Article  Google Scholar 

  • Chaverri P, Liu M, Hodge KT (2008) A monograph of the entomopathogenic genera Hypocrella, Moelleriella, and Samuelsia gen. nov. (Ascomycota, Hypocreales, Clavicipitaceae), and their aschersonia-like anamorphs in the Neotropics. Stud Mycol 60:1–66. https://doi.org/10.3114/sim.2008.60.01

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen WH, Man L, Huang ZX, Yang GM, Han YF, Liang JD, Liang ZQ (2018) Beauveria majiangensis, a new entomopathogenic fungus from Guizhou, China. Phytotaxa 333:243–250. https://doi.org/10.11646/phytotaxa.333.2.8C

  • De Hoog GS (1972) The genera Beauveria, Isaria, Tritirachium, and Acrodontium gen. nov. Stud Mycol 1:1–14

    Google Scholar 

  • De Muro MA, Elliottt S, Moore D, Parker B, Skinner M, Reid W, El Bouhssini M (2005) Molecular characterisation of Beauveria bassiana isolates obtained from overwintering sites of Sunn Pests (Eurygaster and Aelia species). Mycol Res 109:294–306. https://doi.org/10.1017/S0953756204001832

    Article  CAS  PubMed  Google Scholar 

  • Devi K, Sridevi V, Mohan C, Padmavathi J (2005) Effect of high temperature and water stress on in vitro germination and growth in isolates of the entomopathogenic fungus Beauveria bassiana (Bals.) Vuillemin. J Invertebr Pathol 88:181–189. https://doi.org/10.1016/j.jip.2005.02.001

    Article  PubMed  Google Scholar 

  • El Sheikha AF, Hu D-M (2018) How to trace the geographic origin of mushrooms? Trends Food Sci Technol 78:292–303. https://doi.org/10.1016/j.tifs.2018.06.008

    Article  CAS  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39(4):783–791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x

    Article  PubMed  Google Scholar 

  • Fraser JA, Heitman J (2004) Evolution of fungal sex chromosomes. Mol Microbiol 51:299–306

    Article  CAS  PubMed  Google Scholar 

  • Fye RE, McAda WC (1972) Laboratory studies on the development, longevity and fecundity of six lepidopter on pests of cotton in Arizona, USDA. Res Serv Tech Bull 1454(72):171903

  • Geiser D, Jimenez-Gasco MDM, Kang S, Makalowska I, Veeraraghavan N, Ward T, O’Donnell K (2004) A DNA sequence database for identifying Fusarium. Eur J Plant Pathol 110:473–479. https://doi.org/10.1023/B:EJPP.0000032386.75915.a0

    Article  CAS  Google Scholar 

  • Glare TR, Inwood AJ (1998) Morphological and genetic characterisation of Beauveria spp. from New Zealand. Mycol Res 102:250–256

    Article  Google Scholar 

  • Glare TR, Inwood AJ, van der Wielen P, Nelson T (1996a) Identification of novel starins of Beauveria and Metarhizium in New Zealand. In T. A. Jackson & T. R. Glare (Eds.). Proceedings of the 3rd International Workshop on Microbial Control of Soil Dwelling Pests 39–49

  • Glare TR, Milner RJ, Beaton CD (1996b) Variation in Metarhizium, a genus of fungal pathogens attacking Orthoptera: is phialide morphology a useful taxonomic criterion? J Orthoptera Res 5:19–27

    Article  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

  • Hanusz Z, Tarasińska J (2015) Normalization of the kolmogorov-smirnov and shapiro-wilk tests of normality. Biom Lett 52(2):85–93. https://doi.org/10.1515/bile-2015-0008

    Article  Google Scholar 

  • Humber RA (2000) Fungal Pathogens and Parasites of Insects. In F. G. Priest & M. Goodfellow (Eds.). Appl Microbial Syste. Dordrecht: Springer

  • Inglis P, Tigano M (2006) Identification and taxonomy of some entomopathogenic Paecilomyces spp. (Ascomycota) isolates using rDNA-ITS Sequences. Genet Mol Biol 29. https://doi.org/10.1590/S1415-47572006000100025

  • Johnson D, Sung GH, Hywel-Jones NL, Luangsa-Ard JJ, Bischoff JF, Kepler RM, Spatafora JW (2009) Systematics and evolution of the genus Torrubiella (Hypocreales, Ascomycota). Mycol Res 113(Pt 3):279–289. https://doi.org/10.1016/j.mycres.2008.09.008

    Article  CAS  PubMed  Google Scholar 

  • Kary NE, Alizadeh Z (2017) Effects of sub-culturing on genetic and physiological parameters in different Beauveria bassiana isolates. J Invertebr Pathol 145:62–67. https://doi.org/10.1016/j.jip.2017.03.008

    Article  CAS  PubMed  Google Scholar 

  • Kaya HK, Patricia Stock S (1997) Chapter VI - Techniques in insect nematology. In Lacey LA (ed) Manual of Techniques in Insect Pathology. Academic Press, London, pp 281–324

    Chapter  Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee JO, Shrestha B, Sung GH, Han SK, Kim TW, Sung JM (2010) Cultural characteristics and fruiting body production in cordyceps bassiana. Mycobiology 38(2):118–121. https://doi.org/10.4489/myco.2010.38.2.118

    Article  PubMed  PubMed Central  Google Scholar 

  • Lomer C, Bateman R (2001) Biological control of locusts and grasshoppers. Annu Rev Entomol 46:667–702

    Article  CAS  PubMed  Google Scholar 

  • Lutzoni F, Kauff F, Cox C, McLaughlin D, Celio G, Dentinger B, Vilgalys R (2004) Assembling the fungal tree of life: Progress, classification, and evolution of subcellular traits. Am J Bot 91:1446–1480. https://doi.org/10.3732/ajb.91.10.1446

    Article  PubMed  Google Scholar 

  • Maddison DR (1991) The discovery and importance of multiple islands of most-parsimonious trees. Syst Zool 40(3):315–328. https://doi.org/10.2307/2992325

    Article  Google Scholar 

  • McKinnon AC, Glare TR, Ridgway HJ, Mendoza-Mendoza A, Holyoake A, Godsoe WK, Bufford JL (2018) Detection of the entomopathogenic fungus beauveria bassiana in the rhizosphere of wound-stressed zea mays plants. Front Microbiol 9:1161–1161. https://doi.org/10.3389/fmicb.2018.01161

    Article  PubMed  PubMed Central  Google Scholar 

  • Mondal S, Baksi S (2018) Strain-specific identification of Beauveria bassiana isolated from a novel habitat, using rDNA-based sequence analogy. Egyptian Journal of Biological Pest Control 28(1):29. https://doi.org/10.1186/s41938-018-0033-4

    Article  Google Scholar 

  • Mosallanejad H, Golami Z (2019) First report of thiodicarb resistance of the cotton bollworm, Helicoverpa armigera (Hü bner) (Lepidoptera: Noctuidae) in Iran. J Entomol Soc Iran (JESI) 39(2 #r001123):195–212. Retrieved from https://www.sid.ir/en/Journal/ViewPaper.aspx?ID=787254

  • Nilsson RH, Kristiansson E, Ryberg M, Hallenberg N, Larsson K-H (2008) Intraspecific ITS variability in the kingdom fungi as expressed in the international sequence databases and its implications for molecular species identification. Evol Bioinformatics Online 4:193–201. https://doi.org/10.4137/EBO.S653

    Article  Google Scholar 

  • Odds FC, Brown AJ, Gow NA (2004) Candida albicans genome sequence: A platform for genomics in the absence of genetics. Genome Biol 5

  • Padmavathi J, UmaDevi K, Rao CU, Reddy NN (2003) Telomere fingerprinting for assessing chromosome number, isolate typing and recombination in the entomopathogen Beauveria bassiana. Mycol Res 107(Pt 5):572–580. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/12884954

  • Regupathy A, Kranthi KP, Asokan G, Armes NJ, Rao NV, Soundarajan RP, Russel DA (1997) Mechanisms of insecticide resistance in field populations of Helicoverpa armigera in India. Paper presented at the International Conference of Integrated Approaching to Combating Resistance, Harpenden Herts, UK

  • Rehner SA, Buckley E (2005) A Beauveria phylogeny inferred from nuclear ITS and EF1-alpha sequences: evidence for cryptic diversification and links to Cordyceps teleomorphs. Mycologia 97(1):84–98. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/16389960

  • Rehner SA, Minnis AM, Sung GH, Luangsa-ard JJ, Devotto L, Humber RA (2011) Phylogeny and systematics of the anamorphic, entomopathogenic genus Beauveria. Mycologia 103(5):1055–1073. https://doi.org/10.3852/10-302

    Article  PubMed  Google Scholar 

  • Ryan MJ, Smith DR (2004) Fungal genetic resource centres and the genomic challenge. Mycology Research 108:1351–1362

    Article  Google Scholar 

  • Safavi SA (2011) Successive subculturing alters spore-bound Pr1 activity, germination and virulence of the entomopathogenic fungus Beauveria Bassiana. Biocontrol Sci Tech 21(8):883–890. https://doi.org/10.1080/09583157.2011.588317

    Article  Google Scholar 

  • Samson RA, Evans HC (1974) Notes on entomogenous fungi from Ghana II The Genus Akanthomyces. Acta Botanica Neerlandica 23:28–35

    Article  Google Scholar 

  • Seifert K, Wingfield B, Wingfield M (2011) A critique of DNA sequence analysis in the taxonomy of filamentous Ascomycetes and ascomycetous anamorphs. Can J Bot 73:760–767. https://doi.org/10.1139/b95-320

    Article  Google Scholar 

  • Sevim A, Höfte M, Demirbag Z (2012) Genetic variability of Beauveria bassiana and Metarhizium anisopliae var. anisopliae isolates obtained from the Eastern Black Sea Region of Turkey. Turk J Biol 36:255–265. https://doi.org/10.3906/biy-1009-118

    Article  Google Scholar 

  • Shimazu M, Mitsuhashi W, Hashimoto H (1988) Cordyceps brongniartii sp. nov., the teleomorph of Beauveria brongniartii. Transactions of the Mycological Society of Japan 29:323–330

    Google Scholar 

  • Shorey HH, Hale RL (1965) Mass-rearing of the larvae of nine noctuid species on a simple artificial medium. J Econ Entomol 58:522–524

    Article  Google Scholar 

  • Singh H, Keswani C, Ray S, Yadav S, Singh S, Singh S, Sarma B (2015) Beauveria bassiana: Biocontrol beyond lepidopteran pests

  • St Leger RJ, Frank DC, Roberts DW, Staples RC (1992) Molecular cloning and regulatory analysis of the cuticle-degrading-protease structural gene from the entomopathogenic fungus Metarhizium anisopliae. Eur J Biochem 204(3):991–1001. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/1551399

  • Sung GH, Spatafora JW, Zare R, Hodge K, Gams W (2001) A revision of verticillium sect. Prostrata. II. Phylogenetic analysis of SSU and LSU nuclear rDNA sequences from anamorphs and teleomorphs of the Clavicipitaceae. Nova Hed 72:311–328

    Article  Google Scholar 

  • Swofford D (2002). PAUP*. Phylogenetic analysis using parsimony (*and Other Methods). Version 4.0b10 (Vol. Version 4.0)

  • Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci (USA) 101:11030–11035

    Article  CAS  Google Scholar 

  • Uma Devi K, Padmavathi J, Rao UM, C., Khan, A. A. P., & Mohan, M. C. (2008) A study of host specificity in the entomopathogenic fungus Beauveria bassiana (Hypocreales, Clavicipitaceae). Biocontrol Sci Tech 18(10):975–989. https://doi.org/10.1080/09583150802450451

    Article  Google Scholar 

  • Wang-Ching H, Wen-Hsiung K (1997) A simlple method for obtaining single-spore isolates of fungi. Bot Bull Acad Sin 1997(38):41–44

    Google Scholar 

  • Wang CS, Shah FA, Patel N, Li ZZ, Butt TM (2003) Molecular investigation on strain genetic relatedness and population structure of Beauveria bassiana. Environ Microbiol 5:908–915

    Article  CAS  PubMed  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR Protocols: Genes for phylogenetics. Academic Press, San Diego, pp 315–322

    Google Scholar 

  • Zhendong H, Guangfu Y, Zhong Z, Ruiling Z (2019) Phylogenetic relationships and effectiveness of four Beauveria bassiana sensu lato strains for control of Haemaphysalis longicornis (Acari: Ixodidae). Exp Appl Acarol 77(1):83–92. https://doi.org/10.1007/s10493-018-0329-9

    Article  CAS  PubMed  Google Scholar 

  • Zhu H, Qu F, Zhu L (1993) Isolation of genomic DNA from plants, fungi and bacteria using benzyl chloride. Nucleic Acids Res 21:5279–5280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors gratefully acknowledge financial support from the Azarbaijan Shahid Madani University.

Funding

This study was funded by the Deputy of research and technology of Azarbaijan Shahid Madani University.

Author information

Authors and Affiliations

  1. Department of Plant Protection, Faculty of Agriculture, Azarbaijan Shahid Madani University, Tabriz, Iran

    Naser Eivazian Kary & Zhila Alizadeh

  2. Department of Natural Resource Sciences, McGill University, Montreal, Canada

    Gary Dunphy

Authors
  1. Naser Eivazian Kary
    View author publications

    Search author on:PubMed Google Scholar

  2. Zhila Alizadeh
    View author publications

    Search author on:PubMed Google Scholar

  3. Gary Dunphy
    View author publications

    Search author on:PubMed Google Scholar

Contributions

Naser Eivazian Kary: Conceptualization, Methodology, Validation, Investigation, Resources, Supervision, Writing- Original draft preparation, Funding acquisition, Project administration. Zhila Alizadeh: Investigation, Validation. Gary Dunphy: Writing—Review & Editing. All authors have read and approved the manuscript.

Corresponding author

Correspondence to Naser Eivazian Kary.

Ethics declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

This study does not contain any person’s data.

Competing interests

The authors declare that they have no competing interests.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kary, N.E., Alizadeh, Z. & Dunphy, G. Evolutionary distinction between the geographical isolates of Beauveria bassiana from Iran and their efficacy against Helicoverpa armigera. Int J Trop Insect Sci 42, 2083–2092 (2022). https://doi.org/10.1007/s42690-022-00729-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42690-022-00729-2

Keywords