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Tolerance of entomopathogenic fungi to ultraviolet radiation: a review on screening of strains and their formulation

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Abstract

Ultraviolet radiation from sunlight is probably the most detrimental environmental factor affecting the viability of entomopathogenic fungi applied to solar-exposed sites (e.g., leaves) for pest control. Most entomopathogenic fungi are sensitive to UV radiation, but there is great inter- and intraspecies variability in susceptibility to UV. This variability may reflect natural adaptations of isolates to their different environmental conditions. Selecting strains with outstanding natural tolerance to UV is considered as an important step to identify promising biological control agents. However, reports on tolerance among the isolates used to date must be analyzed carefully due to considerable variations in the methods used to garner the data. The current review presents tables listing many studies in which different methods were applied to check natural and enhanced tolerance to UV stress of numerous entomopathogenic fungi, including several well-known isolates of these fungi. The assessment of UV tolerance is usually conducted with conidia using dose-response methods, wherein the UV dose is calculated simply by multiplying the total irradiance by the period (time) of exposure. Although irradiation from lamps seldom presents an environmentally realistic spectral distribution, laboratory tests circumvent the uncontrollable circumstances associated with field assays. Most attempts to increase field persistence of microbial agents have included formulating conidia with UV protectants; however, in many cases, field efficacy of formulated fungi is still not fully adequate for dependable pest control.

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References

  • Alves RT, Bateman RP, Prior C, Leather SR (1998) Effects of simulated solar radiation on conidial germination of Metarhizium anisopliae in different formulations. Crop Prot 17(8):675–679

    Article  CAS  Google Scholar 

  • Behle RW, Compton DL, Laszlo JA, Shapiro-Ilan DI (2009) Evaluation of soyscreen in an oil-based formulation for uv protection of Beauveria bassiana conidia. J Econ Entomol 102(5):1759–1766

    Article  CAS  PubMed  Google Scholar 

  • Bidochka MJ, Kamp AM, Lavender TM, Dekoning J, Croos JNA (2001) Habitat association in two genetic groups of the insect-pathogenic fungus Metarhizium anisopliae: Uncovering cryptic species? Appl Environ Microbiol 67:1335–1342

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Braga GUL, Flint SD, Messias CL, Anderson AJ, Roberts DW (2001a) Effect of UV-B on conidia and germlings of the entomopathogenic hyphomycete Metarhizium anisopliae. Mycol Res 105:874–882

    Article  Google Scholar 

  • Braga GUL, Flint SD, Messias CL, Anderson AJ, Roberts DW (2001b) Effects of UVB irradiance on conidia and germinants of the entomopathogenic hyphomycete Metarhizium anisopliae: A study of reciprocity and recovery. Photochem Photobiol 73(2):140–146

    Article  CAS  PubMed  Google Scholar 

  • Braga GUL, Flint SD, Miller CD, Anderson AJ, Roberts DW (2001c) Both solar UVA and UVB radiation impair conidial culturability and delay germination in the entomopathogenic fungus Metarhizium anisopliae. Photochem Photobiol 74:734–739

    Article  CAS  PubMed  Google Scholar 

  • Braga GUL, Flint SD, Miller CD, Anderson AJ, Roberts DW (2001d) Variability in response to UV-B among species and strains of Metarhizium anisopliae isolates from sites at latitudes from 61°N to 54°S. J Invertebr Pathol 78:98–108

    Article  CAS  PubMed  Google Scholar 

  • Braga GUL, Rangel DEN, Fernandes ÉKK, Flint SD, Roberts DW (2015) Molecular and physiological effects of environmental UV radiation on fungal conidia. Curr Genet In Press. doi:10.1007/s00294-015-0483-0

  • Braga GUL, Rangel DEN, Flint SD, Anderson AJ, Roberts DW (2006) Conidial pigmentation is important to tolerance against solar-simulated radiation in the entomopathogenic fungus Metarhizium anisopliae. Photochem Photobiol 82:418–422

    Article  CAS  PubMed  Google Scholar 

  • Braga GUL, Rangel DEN, Flint SD, Miller CD, Anderson AJ, Roberts DW (2002) Damage and recovery from UV-B exposure in conidia of the entomopathogens Verticillium lecanii and Aphanocladium album. Mycologia 94:912–920

    Article  PubMed  Google Scholar 

  • Caldwell MM, Flint SD (1997) Uses of biological spectral weighting functions and the need of scaling for the ozone reduction problem. Plant Ecol 128:66–79

    Article  Google Scholar 

  • Chase AR, Osborne LS, Ferguson VM (1986) Selective isolation of the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae from an artificial potting medium. Fla Entomol 69(2):285–292

    Article  Google Scholar 

  • Cohen E, Joseph T (2009) Photostabilization of Beauveria bassiana conidia using anionic dyes. Appl Clay Sci 42(3–4):569–574. doi:10.1016/j.clay.2008.03.013

    Article  CAS  Google Scholar 

  • Cohen E, Joseph T, Kahana F, Magdassi S (2003) Photostabilization of an entomopathogenic fungus using composite clay matrices. Photochem Photobiol 77(2):180–185

    Article  CAS  PubMed  Google Scholar 

  • Faria MR, Wraight SP (2007) Mycoinsecticides and mycoacaricides: A comprehensive list with worldwide coverage and international classification of formulation types. Biol Control 43(3):237–256. doi:10.1016/j.biocontrol.2007.08.001

    Article  Google Scholar 

  • Fang WG, Fernandes EKK, Roberts DW, Bidochka MJ, Leger RJS (2010) A laccase exclusively expressed by Metarhizium anisopliae during isotropic growth is involved in pigmentation, tolerance to abiotic stresses and virulence. Fungal Genet Biol 47(7):602–607. doi:10.1016/j.fgb.2010.03.011

    Article  CAS  PubMed  Google Scholar 

  • Fargues J, Goettel MS, Smits N, Ouedraogo A, Vidal C, Lacey LA, Lomer CJ, Rougier M (1996) Variability in susceptibility to simulated sunlight of conidia among isolates of entomopathogenic hyphomycetes. Mycopathologia 135:171–181

    Article  CAS  PubMed  Google Scholar 

  • Fargues JF, Rougier M, Goujet R, Smits N, Coustere C, Itier B (1997) Inactivation of conidia of Paecilomyces fumosoroseus by near-ultraviolet (UVB and UVA) and visible radiation. J Invertebr Pathol 69:70–78

    Article  CAS  PubMed  Google Scholar 

  • Fernandes EKK, Angelo IC, Rangel DEN, Bahiense TC, Moraes AML, Roberts DW, Bittencourt VREP (2011) An intensive search for promising fungal biological control agents of ticks, particularly Rhipicephalus microplus. Vet Parasitol 182:307–318

    Article  PubMed  Google Scholar 

  • Fernandes EKK, Bittencourt VREP, Roberts DW (2012) Perspectives on the potential of entomopathogenic fungi in biological control of ticks. Exp Appl Acarol 130:300–305

    Google Scholar 

  • Fernandes ÉKK, Moraes AML, Pacheco RS, Rangel DEN, Miller MP, Bittencourt VREP, Roberts DW (2009) Genetic diversity among Brazilian isolates of Beauveria bassiana: Comparisons with non-Brazilian isolates and other Beauveria species. J Appl Microbiol 107:760–774. doi:10.1111/j.1365-2672.2009.04258.x

    Article  CAS  PubMed  Google Scholar 

  • Fernandes ÉKK, Rangel DEN, Moraes AML, Bittencourt VREP, Roberts DW (2007) Variability in tolerance to UV-B radiation among Beauveria spp. isolates. J Invertebr Pathol 96:237–243. doi:10.1016/j.jip.2007.05.007

    Article  CAS  PubMed  Google Scholar 

  • Huang BF, Feng MG (2009) Comparative tolerances of various Beauveria bassiana isolates to UV-B irradiation with a description of a modeling method to assess lethal dose. Mycopathologia 168(3):145–152. doi:10.1007/s11046-009-9207-7

    Article  PubMed  Google Scholar 

  • Hunt TR, Moore D, Higgins PM, Prior C (1994) Effect of sunscreens, irradiance and resting periods on the germination of Metarhizium flavoviride conidia. Entomophaga 39(3–4):313–322

    Article  Google Scholar 

  • Ignoffo CM, Garcia C (1992) Influence of conidial color on inactivation of several entomogenous fungi (hyphomycetes) by simulated sunlight. Environ Entomol 21:913–917

    Article  Google Scholar 

  • Inglis GD, Goettel MS, Johnson DL (1995) Influence of ultraviolet-light protectants on persistence of the entomopathogenic fungus. Beauveria bassiana. Biol Control 5(4):581–590

    Article  Google Scholar 

  • Inglis GD, Johnson DL, Goettel MS (1997a) Effects of temperature and sunlight on mycosis (Beauveria bassiana) (Hyphomycetes: Sympodulosporae) of grasshoppers under field conditions. Environ Entomol 26(2):400–409

    Article  Google Scholar 

  • Inglis GD, Johnson DL, Goettel MS (1997b) Field and laboratory evaluation of two conidial batches of Beauveria bassiana (Balsamo) Vuillemin against grasshoppers. Can Entomol 129(1):171–186

    Article  Google Scholar 

  • Jaronski ST (2010) Ecological factors in the inundative use of fungal entomopathogens. Biocontrol 55(1):159–185. doi:10.1007/s10526-009-9248-3

    Article  Google Scholar 

  • Le Grand M, Cliquet S (2013) Impact of culture age on conidial germination, desiccation and UV tolerance of entomopathogenic fungi. Biocontrol Sci Techn 23(7):847–859

    Article  Google Scholar 

  • Lee JY, Kang SW, Yoon CS, Kim JJ, Choi DR, Kim SW (2006) Verticillium lecanii spore formulation using UV protectant and wetting agent and the biocontrol of cotton aphids. Biotechnol Lett 28:1041–1045

    Article  CAS  PubMed  Google Scholar 

  • Leland JE, Behle RW (2005) Coating Beauveria bassiana with lignin for protection from solar radiation and effects on pathogenicity to lygus lineolaris (Heteroptera: Miridae). Biocontrol Sci Techn 15(3):309–320. doi:10.1080/09583150400016936

    Article  Google Scholar 

  • Milner RJ, Huppatz RJ, Swaris SC (1991) A new method for assessment of germination of metarhizium conidia. J Invertebr Pathol 57:121–123

    Article  Google Scholar 

  • Moore D, Bridge PD, Higgins PM, Bateman RP, Prior C (1993) Ultra-violet radiation damage to Metarhizium flavoviride conidia and the protection given by vegetable and mineral oils and chemical sunscreens. Ann Appl Biol 122:605–616

    Article  CAS  Google Scholar 

  • Morley Davies J, Moore D, Prior C (1996) Screening of Metarhizium and Beauveria spp. conidia with exposure to simulated sunlight and a range of temperatures. Mycol Res 100:31–38

    Article  Google Scholar 

  • Nascimento É, da Silva SH, Marques ER, Roberts DW, Braga GUL (2010) Quantification of cyclobutane pyrimidine dimers induced by UVB radiation in conidia of the fungi Aspergillus fumigatus, Aspergillus nidulans, Metarhizium acridum and Metarhizium robertsii. Photochem Photobiol 86:1259–1266

    Article  CAS  PubMed  Google Scholar 

  • Ottati-de-Lima EL, Filho AB, Almeida JEM, Gassen MH, Wenzel IM, Almeida AMB, Zapellini LO (2012) Liquid production of entomopathogenic fungi and ultraviolet radiation and temperature effects on produced propagules. Arq Inst Biol 81(4):342–350

    Article  Google Scholar 

  • Polar P, Moore D, Kairo MTK, Ramsubhag A (2008) Topically applied myco-acaricides for the control of cattle ticks: Overcoming the challenges. Exp Appl Acarol 46(1–4):119–148. doi:10.1007/s10493-008-9170-x

    Article  CAS  PubMed  Google Scholar 

  • Posadas JB, Angulo LM, Mini JI, Lecuona RE (2012) Natural tolerance to UV-B and assessment of photoprotectants in conidia of six native isolates of Beauveria bassiana (Bals-Criv) Vuillemin. World Appl Sci J 20(7):1024–1030

    Google Scholar 

  • Quaite FE, Sutherland BM, Sutherland JC (1992) Action spectrum for DNA damage in alfalfa lowers predicted impact of ozone depletion. Nature 358:576–578

    Article  CAS  Google Scholar 

  • Rangel DEN, Anderson AJ, Roberts DW (2006a) Growth of Metarhizium anisopliae on non-preferred carbon sources yields conidia with increased UV-B tolerance. J Invertebr Pathol 93:127–134

    Article  CAS  PubMed  Google Scholar 

  • Rangel DEN, Anderson AJ, Roberts DW (2008) Evaluating physical and nutritional stress during mycelial growth as inducers of tolerance to heat and UV-B radiation in Metarhizium anisopliae conidia. Mycol Res 112:1362–1372. doi:10.1016/j.mycres.2008.04.013

    Article  PubMed  Google Scholar 

  • Rangel DEN, Braga GUL, Anderson AJ, Roberts DW (2005a) Influence of growth environment on tolerance to UV-B radiation, germination speed, and morphology of Metarhizium anisopliae var. acridum conidia. J Invertebr Pathol 90:55–58

    Article  PubMed  Google Scholar 

  • Rangel DEN, Braga GUL, Anderson AJ, Roberts DW (2005b) Variability in conidial thermotolerance of Metarhizium anisopliae isolates from different geographic origins. J Invertebr Pathol 88:116–125. doi:10.1016/j.jip.2004.11.007

    Article  PubMed  Google Scholar 

  • Rangel DEN, Braga GUL, Fernandes ÉKK, Keyser CA, Hallsworth JE, Roberts DW (2015) Stress tolerance and virulence of insect-pathogenic fungi are determined by environmental conditions during conidial formation. Curr Genet In Press. doi:10.1007/s00294-015-0477-y

  • Rangel DEN, Braga GUL, Flint SD, Anderson AJ, Roberts DW (2004) Variations in UV-B tolerance and germination speed of Metarhizium anisopliae conidia produced on artificial and natural substrates. J Invertebr Pathol 87:77–83. doi:10.1016/j.jip.2004.06.007

    Article  PubMed  Google Scholar 

  • Rangel DEN, Butler MJ, Torabinejad J, Anderson AJ, Braga GUL, Day AW, Roberts DW (2006b) Mutants and isolates of Metarhizium anisopliae are diverse in their relationships between conidial pigmentation and stress tolerance. Journal of Invertebrate Pathology 93(3):170–182. doi:10.1016/j.jip.2006.06.008

    Article  PubMed  Google Scholar 

  • Rangel DEN, Dettenmaier SJ, Fernandes EKK, Roberts DW (2010) Susceptibility of Metarhizium spp. and other entomopathogenic fungi to dodine-based selective media. Biocontrol Sci Techn 20:375–389

    Article  Google Scholar 

  • Rangel DEN, Fernandes EKK, Braga GUL, Roberts DW (2011) Visible light during mycelial growth and conidiation of Metarhizium robertsii produces conidia with increased stress tolerance. Fems Microbiol Lett 315:81–86

    Article  CAS  PubMed  Google Scholar 

  • Rangel DEN, Roberts DW (2007) Inducing UV-B tolerance of Metarhizium anisopliae var. anisopliae conidia results in a trade-off between conidial production and conidial stress tolerance. J Anhui Agric Univ 34 (2):195-202

  • Reddy NP, Khan PAA, Devi KU, Victor JS, Sharma HC (2008) Assessment of the suitability of tinopal as an enhancing adjuvant in formulations of the insect pathogenic fungus Beauveria bassiana (Bals.)Vuillemin. Pest Manag Sci 64(9):909–915. doi:10.1002/Ps.1581

    Article  CAS  PubMed  Google Scholar 

  • Roberts DW, Campbell AA (1977) Stability of entomopathogenic fungi. In: Ignoffo CM, Hostetter DL (eds) Environmental stability of microbial insecticides. Entomological Society of America, Lanham, pp 19–76

    Google Scholar 

  • Santos MP, Dias LP, Ferreira PC, Pasin LAAP, Rangel DEN (2011) Cold activity and tolerance of the entomopathogenic fungus Tolypocladium spp. to UV-B irradiation and heat. J Invertebr Pathol 108:209–213

    Article  PubMed  Google Scholar 

  • Speare AT (1920) Further studies on Sorosporella uvella, a fungous parasite of noctuid larvae. J Agric Res 18:399–437

    Google Scholar 

  • Tuveson RW, McCoy CW (1982) Far-ultraviolet sensitivity and photoreactivation of Hirsutella thompsonii. Ann Appl Biol 101:13–18

    Article  Google Scholar 

  • Yao SL, Ying SH, Feng MG, Hatting JL (2010) In vitro and in vivo responses of fungal biocontrol agents to gradient doses of UV-B and UV-A irradiation. Biocontrol 55(3):413–422. doi:10.1007/s10526-009-9265-2

    Article  CAS  Google Scholar 

  • Zimmermann G (1982) Effect of high-temperatures and artificial sunlight on the viability of conidia of Metarhizium anisopliae. J Invertebr Pathol 40(1):36–40

    Article  Google Scholar 

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Acknowledgments

We would like to thank Alene Alder-Rangel (Univap) for help with revising the English manuscript. We thank Richard Allan Humber (USDA–ARS) for a critical review of the manuscript. This review article was supported in part by the grants: 484329/2012-0 from the Brazilian National Council for Scientific and Technological Development (CNPq), and 201210267001060 from the Foundation for Research of the State of Goiás (FAPEG) for ÉKKF. We also thank the State of São Paulo Research Foundation (FAPESP) for the grants: 2012/15204-8 for GULB, 2010/06374-1 for DENR, and CNPq for the grants: PQ 304192/2012-0 for GULB and PQ 302312/2011 for DENR. This review article was supported in part by a grant from FAPESP # 2014/01229-4, and by Cooperative Agreements between DWR and the United States Department of Agriculture (USDA–APHIS).

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Authors and Affiliations

  1. Instituto de Patologia Tropical e Saúde Pública, Universidade Federal de Goiás, Goiânia, GO, 746050-50, Brazil

    Éverton K. K. Fernandes

  2. Instituto de Pesquisa e Desenvolvimento, Universidade do Vale do Paraíba, São José dos Campos, SP, 12244-000, Brazil

    Drauzio E. N. Rangel

  3. Departamento de Análises Clínicas, Toxicológicas e Bromatológicas, Universidade de São Paulo, Ribeirão Preto, SP, 14040-903, Brazil

    Gilberto U. L. Braga

  4. Research Support Center in Natural and Synthetic Products, Faculdade de Ciências Farmacêuticas de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, SP, 14040-903, Brazil

    Gilberto U. L. Braga

  5. Department of Biology, Utah State University, Logan, UT, 84322-5305, USA

    Donald W. Roberts

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  1. Éverton K. K. Fernandes
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  2. Drauzio E. N. Rangel
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  3. Gilberto U. L. Braga
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Correspondence to Éverton K. K. Fernandes.

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Communicated by D. E. N. Rangel.

This article is part of the Special Issue “Fungal Stress Responses”.

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Fernandes, É.K.K., Rangel, D.E.N., Braga, G.U.L. et al. Tolerance of entomopathogenic fungi to ultraviolet radiation: a review on screening of strains and their formulation. Curr Genet 61, 427–440 (2015). https://doi.org/10.1007/s00294-015-0492-z

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