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Tolerance and Bioaccumulation of Copper by the Entomopathogen Beauveria bassiana (Bals.-Criv.) Vuill. Exposed to Various Copper-Based Fungicides

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Abstract

This work evaluates for the first time the relationships between copper-tolerance, -solubilization and -bioaccumulation in the entomopathogen Beauveria bassiana exposed to Bordeaux mixture, copper oxychloride or copper hydroxide. Bordeaux mixture was highly detrimental to fungus, by inhibiting the growth totally at the recommended dose (RD) and 2×RD. Copper hydroxide and copper oxychloride were found to be less toxic, reducing fungus growth, sporulation and conidial germination in an average of 29  %, 30 % and 58 %, respectively. These two copper forms were the easiest to solubilize, to precipitate and the most accumulated by B. bassiana, suggesting the involvement of all these processes on fungus copper-tolerance.

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References

  • Agrios GN (2005) Plant Pathology, 5th edn. Elsevier Academic Press, New York

    Google Scholar 

  • Akello J, Dubois T, Coyne D, Kyamanywa S (2009) The effects of Beauveria bassiana dose and exposure duration on colonization and growth of tissue cultured banana (Musa sp.) plants. Biol Control 49:6–10

    Article  Google Scholar 

  • Bååth E (1991) Tolerance of copper by entomogenous fungi and the use of copper-amended media for isolation of entomogenous fungi from soil. Mycol Res 95:1140–1152

    Article  Google Scholar 

  • Baptista P, Ferreira S, Soares E, Coelho V, Bastos M (2009) Tolerance and stress response of Macrolepiota procera to nickel. J Agric Food Chem 57:7145–7152

    Article  CAS  Google Scholar 

  • Cervantes C, Gutierrez-Crona F (1994) Copper resistance mechanisms in bacteria and fungi. FEMS Microbiol Rev 14:121–138

    Article  CAS  Google Scholar 

  • Clausen CA, Green F (2003) Oxalic acid overproduction by copper-tolerant brown-rot basidiomycetes on southern yellow pine treated with copper-based preservatives. Int Biodeterior Biodegrad 51:139–144

    Article  CAS  Google Scholar 

  • Durán J, Carballo M, Hidalgo E (2004) Efecto de fungicidas sobre la germinación y el crecimiento de Beauveria bassiana. Manejo Integrado de Plagas y Agroecología. Costa Rica 71:73–78

    Google Scholar 

  • Figueiredo E, Soares ME, Baptista P, Castro M, Bastos ML (2007) Validation of an electrothermal atomization atomic absorption spectrometry method for quantification of total chromium and chromium(VI) in wild mushrooms and underlying soils. J Agric Food Chem 55:7192–7198

    Article  CAS  Google Scholar 

  • Fomina M, Alexandre IJ, Hillier S, Gadd GM (2004) Zinc phosphate and pyromorphite solubilization by soil plant-symbiotic fungi. Geomicrobiol J 21:351–366

    Article  CAS  Google Scholar 

  • Fomina MA, Burford EP, Gadd GM (2005a) Toxic metals and fungal communities. In: Dighton J, White JF, Oudemans P (eds) The Fungal Community: Its Organization and Role in the Ecosystem. Taylor & Francis, CRC Press, USA, pp 733–758

    Chapter  Google Scholar 

  • Fomina M, Hillier S, Charnock JM, Melville K, Alexander IJ, Gadd GM (2005b) Role of oxalic acid overexcretion in transformations of toxic metal minerals by Beauveria caledonica. Appl Environ Microbiol 71:371–381

    Article  CAS  Google Scholar 

  • Gadd GM (1993) Interaction of fungi with toxic metals. New Phytol 124:25–60

    Article  CAS  Google Scholar 

  • Gharied MM (2002) Biosorption and solubilization of copper oxychloridefungicide by Aspergillus niger and the influence of calcium. Biodegradation 13:191–199

    Article  Google Scholar 

  • Gharied MM, Ali IM, El-Shoura AA (2004) Transformation of copper oxychloride fungicide into copper oxalate by tolerant fungi and the effect of nitrogen source on tolerance. Biodegradation 15:49–57

    Article  Google Scholar 

  • Gisi U, Sierotzki H (2008) Fungicide modes of action and resistance in downy mildews. Eur J Plant Pathol 122:157–167

    Article  CAS  Google Scholar 

  • Jaros-Su J, Groden E, Zhang J (1999) Effects of selected fungicides and timing of fungicide application on Beauveria bassiana-induced mortality of the colorado potato beetle (Coleoptera: Chrysomelidae). Biol Control 15:259–269

    Article  Google Scholar 

  • Kouassi M, Coderre D, Todorova SI (2003) Effects of the timing of applications on the incompatability of three fungicides and one isolate of the entomopathogenic fungus Beauveria bassiana (Balsamo) Vuillemin (Deuteromycotina). J Appl Entomol 127:421–426

    Article  CAS  Google Scholar 

  • Loria RS, Galaini S, Roberts DW (1983) Survival of the entomopathogenic fungus Beauveria bassiana as influenced by fungicides. Environ Entomol 12:1724–1726

    Google Scholar 

  • Majchrowicz I, Poprawski TJ (1993) Effects in vitro of nine fungicides on growth of entomopathogenic fungi. Biocontrol Sci Tech 3:321–336

    Article  Google Scholar 

  • Oliveira I, Pereira JA, Bento A, Baptista P (2010) Viability of Beauveria bassiana isolates after storage under several preservation methods. Ann of Microbiol 61:339–344

    Article  Google Scholar 

  • Oliveira I, Pereira JA, Lino-Neto T, Bento A, Baptista P (in press) Fungal diversity associated to the olive moth, Prays oleae Bernard: a survey for potential entomopathogenic fungi. Microb Ecol

  • Olmert I, Kenneth RG (1974) Sensitivity of the entomopathogenic fungi Beauveria bassiana, Verticillium lecanii, Verticillium sp. to fungicides and insecticides. Environ Entomol 3:33–38

    CAS  Google Scholar 

  • Ownley BH, Griffin MR, Klingeman WE, Gwinn KD, Moulton JK, Pereira RM (2008) Beauveria bassiana: Endophytic colonization and plant disease control. J Invertebr Pathol 98:267–270

    Article  CAS  Google Scholar 

  • Popowska-Nowak E, Sosak-Oewiderska B, Bajan C, Bieñkowski P (2004) Response of isolates of entomopathogenic fungus Metarhizium anisopliae to heavy metal pollution and their accumulative abilities. Chem InZ Ekol 11:71

    CAS  Google Scholar 

  • Rachappa V, Lingappa S, Patil RK (2007) Effect of agrochemicals on growth and sporulation of Metarhizium Anisopliae (Metschnikoff) Sorokin Karnataka. J Agric Sci 20:410–413

    Google Scholar 

  • Shah FA, Ansari MA, Watkins J, Phelps Z, Cross J, Butt TM (2009) Influence of commercial fungicides on the germination, growth and virulence of four species of entomopathogenic fungi. Biocontrol Sci Technol 19:743–753

    Article  Google Scholar 

  • Shapiro-Ilan DI, Reilly CC, Hotchkiss MW, Wood BW (2002) The potential for enhanced fungicide resistance in Beauveria bassiana through strain discovery and artificial selection. J Invertebr Pathol 81:86–93

    Article  CAS  Google Scholar 

  • Soares ME, Pereira JA, Bastos L (2006) Validation of a method to quantify copper and other metals in olive fruit by ETAAS. Application to the residual metal control after olive tree treatments with different copper formulations. J Agric Food Chem 54:3923–3928

    Article  CAS  Google Scholar 

  • Tamai MA, Alves SB, Lopes RB, Faion M, Padulla LFL (2002) Toxicidade de produtos fitossanitários para Beauveria bassiana. Arq Inst Biol 69:89–96

    Google Scholar 

  • Todorova SI, Coderre D, Duchesne RM, Côté JC (1998) Compatibility of Beauveria bassiana with selected fungicides and herbicides. Environ Entomol 27:427–433

    CAS  Google Scholar 

  • White Tj, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis M, Gelfand D, Shinsky J, White Tj (eds) PCR Protocols: A guide to methods and applications, Academic Press, San Diego, pp. 315–322

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Acknowledgments

Authors are grateful to Fundação para a Ciência e Tecnologia (FCT) for financial support (Project PTCD/AGR-AAM/102600/2008).

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Authors and Affiliations

  1. CIMO/School of Agriculture, Polytechnic Institute of Bragança, Campus de Santa Apolónia, Apartado 1172, 5301-854, Bragança, Portugal

    Fátima Martins, Ivo Oliveira, José Alberto Pereira & Paula Baptista

  2. REQUIMTE/Serviço de Toxicologia, Faculdade de Farmácia, Universidade do Porto, R. Aníbal Cunha 164, 4099-030, Porto, Portugal

    Maria Elisa Soares & Maria de Lourdes Bastos

Authors
  1. Fátima Martins
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  2. Maria Elisa Soares
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  3. Ivo Oliveira
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  4. José Alberto Pereira
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  5. Maria de Lourdes Bastos
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  6. Paula Baptista
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Correspondence to Paula Baptista.

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Martins, F., Soares, M.E., Oliveira, I. et al. Tolerance and Bioaccumulation of Copper by the Entomopathogen Beauveria bassiana (Bals.-Criv.) Vuill. Exposed to Various Copper-Based Fungicides. Bull Environ Contam Toxicol 89, 53–60 (2012). https://doi.org/10.1007/s00128-012-0628-5

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  • DOI: https://doi.org/10.1007/s00128-012-0628-5

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