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Stress tolerance and virulence of insect-pathogenic fungi are determined by environmental conditions during conidial formation

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Abstract

The virulence to insects and tolerance to heat and UV-B radiation of conidia of entomopathogenic fungi are greatly influenced by physical, chemical, and nutritional conditions during mycelial growth. This is evidenced, for example, by the stress phenotypes of Metarhizium robertsii produced on various substrates. Conidia from minimal medium (Czapek’s medium without sucrose), complex medium, and insect (Lepidoptera and Coleoptera) cadavers had high, moderate, and poor tolerance to UV-B radiation, respectively. Furthermore, conidia from minimal medium germinated faster and had increased heat tolerance and were more virulent to insects than those from complex medium. Low water-activity or alkaline culture conditions also resulted in production of conidia with high tolerance to heat or UV-B radiation. Conidia produced on complex media exhibited lower stress tolerance, whereas those from complex media supplemented with NaCl or KCl (to reduce water activity) were more tolerant to heat and UV-B than those from the unmodified complex medium. Osmotic and nutritive stresses resulted in production of conidia with a robust stress phenotype, but also were associated with low conidial yield. Physical conditions such as growth under illumination, hypoxic conditions, and heat shock before conidial production also induced both higher UV-B and heat tolerance; but conidial production was not decreased. In conclusion, physical and chemical parameters, as well as nutrition source, can induce great variability in conidial tolerance to stress for entomopathogenic fungi. Implications are discussed in relation to the ecology of entomopathogenic fungi in the field, and to their use for biological control. This review will cover recent technologies on improving stress tolerance of entomopathogenic fungi for biological control of insects.

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Acknowledgments

We wish to express great appreciation to Alene Alder-Rangel who improved the presentation of this manuscript. This work was supported by Grants of the Brazilian National Council for Scientific and Technological Development (CNPq) 473104/2008-3, 478899/2010-6, and PQ 302312/2011-0, and PQ1D 308436/2014-8 for D. E. N. R and to State of São Paulo Research Foundation (FAPESP) #2010/06374-1, 2013/50518-6 for D.E.N.R and #2012/15204-8 for G.U.L.B, and by Cooperative Agreements by D. W. R. with the US Department of Agriculture (USDA-APHIS). This review article was supported in part by a Grant from FAPESP # 2014/01229-4.

Dedication by D.E.N.R. The lead author, Drauzio Eduardo Naretto Rangel, dedicates this work to his father Drausio Taveiros Rangel born in November 26, 1932 and passed away on November 20, 2014 while the author was writing this review. Drausio Taveiros Rangel was born in Cravinhos, State of São Paulo, Brazil, in a very poor family with five children. His father died when he was 5 years old, and the family moved to the city of São Paulo. Drausio studied until the fourth grade, and he then studied carpentry in a vocational school, but made his career in typographical printing industry. In the beginning, he worked as employee, and then through his hard work, he established himself as an owner of a small typographical printing company with at least five employees. He married Maria Hilda Naretto Rangel when he was an employee of a printing company. Drausio and Maria Hilda had two sons. They lived in a small, one-bedroom house belonging to Maria Hilda’s father for 11 years, after which time the success of the printing company enabled rental of a larger family home. When D. E. N. R. was 9 years old and showed an interest in science, Drausio and Maria Hilda gave a small microscope to him, which is still in the author’s office. Three years later, they also gave science kits that were sold weekly inside a foam box at the newspaper stand. At this time (1970s), the author’s father bought weekly issues about science, history, arts, religion, etc. at the newspaper stand and collated these to form several encyclopedias. Despite their lack of formal education, Drausio and Maria Hilda read these with considerable enthusiasm, stimulating similar interest in their sons. They also took care to encourage and support their boys to obtain a university education. By this time (1980s), the printing company had grown to more than 30 employees. The motto of Drausio was do your best to avoid doing it over. Drausio Taveiros Rangel was a man with a happy disposition and kindness of heart who was also responsible and had strong work ethic. D. E. N. R. wishes to express his deepest gratitude to him.

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Authors and Affiliations

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

    Drauzio E. N. Rangel

  2. Faculdade de Ciências Farmacêuticas de Ribeirão Preto, Universidade de São Paulo, Ribeirão Prêto, SP, 14040-903, Brazil

    Gilberto U. L. Braga

  3. Instituto de Patologia Tropical e Saúde Pública, Universidade Federal de Goiás, Goiânia, GO, 74605-050, Brazil

    Éverton K. K. Fernandes

  4. Department of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, 1871, Frederiksberg, Denmark

    Chad A. Keyser

  5. Institute for Global Food Security, School of Biological Sciences, MBC, Queen’s University Belfast, Belfast, BT9 7BL, Northern Ireland, UK

    John E. Hallsworth

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

    Drauzio E. N. Rangel, Éverton K. K. Fernandes & Donald W. Roberts

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  1. Drauzio E. N. Rangel
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  2. Gilberto U. L. Braga
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  3. Éverton K. K. Fernandes
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  4. Chad A. Keyser
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  5. John E. Hallsworth
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  6. Donald W. Roberts
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Correspondence to Drauzio E. N. Rangel.

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Communicated by M. Kupiec.

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

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Rangel, D.E.N., Braga, G.U.L., Fernandes, É.K.K. et al. Stress tolerance and virulence of insect-pathogenic fungi are determined by environmental conditions during conidial formation. Curr Genet 61, 383–404 (2015). https://doi.org/10.1007/s00294-015-0477-y

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