Skip to main content

Phenotypic and molecular insights into heat tolerance of formulated cells as active ingredients of fungal insecticides

Applied Microbiology and Biotechnology volume 104, pages 5711–5724 (2020)Cite this article

Abstract

Formulated conidia of insect-pathogenic fungi, such as Beauveria and Metarhizium, serve as the active ingredients of fungal insecticides but are highly sensitive to persistent high temperatures (32–35 °C) that can be beyond their upper thermal limits especially in tropical areas and during summer months. Fungal heat tolerance and inter- or intra-specific variability are critical factors and limitations to field applications of fungal pesticides during seasons favoring outbreaks of pest populations. The past decades have witnessed tremendous advances in improving fungal pesticides through selection of heat-tolerant strains from natural isolates, improvements and innovations in terms of solid-state fermentation technologies for the production of more heat-tolerant conidia, and the use of genetic engineering of candidate strains for enhancing heat tolerance. More recently, with the entry into a post-genomic era, a large number of signaling and effector genes have been characterized as important sustainers of heat tolerance in both Beauveria and Metarhizium, which represent the main species used as fungal pesticides worldwide. This review focuses on recent advances and provides an overview into the broad molecular basis of fungal heat tolerance and its multiple regulatory pathways. Emphases are placed on approaches for screening of heat-tolerant strains, methods for optimizing conidial quality linked to virulence and heat tolerance particularly involving cell wall architecture and optimized trehalose/mannitol contents, and how molecular determinants can be exploited for genetic improvement of heat tolerance and pest-control potential. Examples of fungal pesticides with different host spectra and their appropriateness for use in apiculture are given.

Key points

• Heat tolerance is critical for field stability and efficacy of fungal insecticides.

• Inter- and intra-specific variability exists in insect-pathogenic fungi.

• Optimized production technology and biotechnology can improve heat tolerance.

• Fungal heat tolerance is orchestrated by multiple molecular pathways.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

References

  • Bischoff JF, Rehner SA, Humber RA (2009) A multilocus phylogeny of the Metarhizium anisopliae lineage. Mycologia 101:512–530

    CAS  PubMed  Google Scholar 

  • Braga GUL, Rangel DEN, Fernandes EKK, Flint SD, Roberts DW (2015) Molecular and physiological effects of environmental UV radiation on fungal conidia. Curr Genet 61:405–425

    CAS  PubMed  Google Scholar 

  • Butt TM, Coates CJ, Dubovskiy IM, Ratcliffe NA (2016) Entomopathogenic fungi: new insights into host-pathogen interactions. Adv Genet 94:307–364

    CAS  PubMed  Google Scholar 

  • Cai Q, Wang JJ, Fu B, Ying SH, Feng MG (2018a) Gcn5-dependent histone H3 acetylation and gene activity is required for the asexual development and virulence of Beauveria bassiana. Environ Microbiol 20:1484–1497

    CAS  PubMed  Google Scholar 

  • Cai Q, Tong SM, Shao W, Ying SH, Feng MG (2018b) Pleiotropic effects of the histone deacetylase Hos2 linked to H4-K16 deacetylation, H3-K56 acetylation and H2A-S129 phosphorylation in Beauveria bassiana. Cell Microbiol 20:e12839

    PubMed  Google Scholar 

  • Cao YQ, Du MJ, Luo S, Xia YX (2014) Calcineurin modulates growth, stress tolerance, and virulence in Metarhizium acridum and its regulatory network. Appl Microbiol Biotechnol 98:8253–8265

    CAS  PubMed  Google Scholar 

  • Chen X, Liu YZ, Keyhani NO, Xia YX, Cao YQ (2017) The regulatory role of the transcription factor Crz1 in stress tolerance, pathogenicity, and its target gene expression in Metarhizium acridum. Appl Microbiol Biotechnol 101:5033–5043

    CAS  PubMed  Google Scholar 

  • Chen Y, Zhu J, Ying SH, Feng MG (2014a) Three mitogen-activated protein kinases required for cell wall integrity contribute greatly to biocontrol potential of a fungal entomopathogen. PLoS One 9:e87948

    PubMed  PubMed Central  Google Scholar 

  • Chen Y, Zhu J, Ying SH, Feng MG (2014b) The GPI-anchored protein Ecm33 is vital for conidiation, cell wall integrity and multi-stress tolerance of two filamentous entomopathogens but not for virulence. Appl Microbiol Biotechnol 98:5517–5529

    CAS  PubMed  Google Scholar 

  • Clancy LM, Jones R, Cooper AL, Griffith GW, Santer RD (2018) Dose-dependent behavioural fever responses in desert locusts challenged with the entomopathogenic fungus Metarhizium acridum. Sci Rep 8:14222

    PubMed  PubMed Central  Google Scholar 

  • Davari A, Skinner M, Parker BL (2018) Cell electrofusion to improve efficacy and thermotolerance of the entomopathogenic fungus, Beauveria bassiana. J Appl Microbiol 125:1482–1493

    CAS  PubMed  Google Scholar 

  • de Crecy E, Jaronski S, Lyons B, Lyons T, Keyhani NO (2009) Directed evolution of a filamentous fungus for thermotolerance. BMC Biotechnol 9:74

    PubMed  PubMed Central  Google Scholar 

  • Du YR, Jin K, Xia YX (2018) Involvement of MaSom1, a downstream transcriptional factor of cAMP/PKA pathway, in conidial yield, stress tolerances, and virulence in Metarhizium acridum. Appl Microbiol Biotechnol 102:5611–5623

    CAS  PubMed  Google Scholar 

  • Elbein AD, Pan YT, Pastuszak I, Carroll D (2003) New insights on trehalose: a multifunctional molecule. Glycobiology 13:17–27

    Google Scholar 

  • Elliot SL, Blanford S, Thomas MB (2002) Host-pathogen interactions in a varying environment: temperature, behavioural fever and fitness. Proc Roy Soc B-Biol Sci 269:1599–1607

    Google Scholar 

  • Etxebeste O, Garzia A, Espeso EA, Ugalde (2010) Aspergillus nidulans asexual development: making the most of cellular modules. Trends Microbiol 18:569–576

    CAS  PubMed  Google Scholar 

  • Faria M, Waright SP (2002) Biological control of Bemisia tabaci with fungi. Crop Prot 20:767–778

    Google Scholar 

  • Feng MG, Poprawski TJ, Khachatourians GG (1994) Production, formulation and application of the entomopathogenic fungus Beauveria bassiana for insect control: current status. Biocontrol Sci Tech 4:3–34

    Google Scholar 

  • Fernandes EKK, Rangel DEN, Moraes AML, Bittencourt VREP, Roberts DW (2008) Cold activity of Beauveria and Metarhizium, and thermotolerance of Beauveria. J Invertebr Pathol 98:69–78

    PubMed  Google Scholar 

  • Fernandes EKK, Keyser CA, Chong JP, Rangel DEN, Miller MP, Roberts DW (2010) Characterization of Metarhizium species and varieties based on molecular analysis, heat tolerance and cold activity. J Appl Microbiol 108:115–128

    CAS  PubMed  Google Scholar 

  • Fernandes EKK, Rangel DEN, Braga GUL, Roberts DW (2015) Tolerance of entomopathogenic fungi to ultraviolet radiation: a review on screening of strains and their formulation. Curr Genet 61:427–440

    CAS  PubMed  Google Scholar 

  • Francis RM, Nielsen SL, Kryger P (2013) Varroa-virus interaction in collapsing honey bee colonies. PLoS One 8:e57540

    CAS  PubMed  PubMed Central  Google Scholar 

  • Genersch E, von der OheW KH, Schroeder A, Otten C, Büchler R, Berg S, Ritter W, Muehlen W, Gisder S, Meixner M, Liebig G, Rosenkranz P (2010) The German bee monitoring project: a long term study to understand periodically high winter losses of honey bee colonies. Apidologie 41:332–352

    CAS  Google Scholar 

  • Guan Y, Wang DY, Ying SH, Feng MG (2015) A novel Ras GTPase (Ras3) regulates conidiation, multi-stress tolerance and virulence by acting upstream of Hog1 signaling pathway in Beauveria bassiana. Fungal Genet Biol 82:85–94

    CAS  PubMed  Google Scholar 

  • Guan Y, Wang DY, Ying SH, Feng MG (2016) Miro GTPase controls mitochondrial behavior affecting stress tolerance and virulence of a fungal insect pathogen. Fungal Genet Biol 93:1–9

    CAS  PubMed  Google Scholar 

  • Huang SS, He ZJ, Zhang SW, Keyhani NO, Song YL, Yang Z, Jiang YH, Zhang WL, Pei Y, Zhang YJ (2015) Interplay between calcineurin and the Slt2 MAP-kinase in mediating cell wall integrity, conidiation and virulence in the insect fungal pathogen Beauveria bassiana. Fungal Genet Biol 83:78–91

    PubMed  Google Scholar 

  • Huarte-Bonnet C, Juarez MP, Pedrini N (2015) Oxidative stress in entomopathogenic fungi grown on insect-like hydrocarbons. Curr Genet 61:289–297

    CAS  PubMed  Google Scholar 

  • Jaronski ST (2010) Ecological factors in the inundative use of fungal entomopathogens. BioControl 55:159–185

    Google Scholar 

  • Jin K, Ming Y, Xia YX (2012) MaHog1, a Hog1-type mitogen-activated protein kinase gene, contributes to stress tolerance and virulence of the entomopathogenic fungus Metarhizium acridum. Microbiol-SGM 158:2987–2926

    CAS  Google Scholar 

  • Kanga LHB, Jones WA, James RR (2003) Field trials using the fungal pathogen, Metarhizium anisopliae (Deuteromycetes: Hyphomycetes) to control the ectoparasitic mite, Varroa destructor (Acari: Varroidae) in honey bee, Apis mellifera (Hymenoptera: Apidae) colonies. J Econ Entomol 96:1091–1099

    PubMed  Google Scholar 

  • Keyser CA, Fernandes EKK, Rangel DEN, Roberts DW (2014) Heat-induced post-stress growth delay: a biological trait of many Metarhizium isolates reducing biocontrol efficacy? J Invertebr Pathol 120:67–73

    PubMed  Google Scholar 

  • Kim JS, Skinner M, Parker BL (2010a) Influence of whey permeate and millet as substrates on thermotolerance of Beauveria bassiana and Metarhizium anisopliae conidia during storage. Biocontrol Sci Tech 20:859–863

    Google Scholar 

  • Kim JS, Skinner M, Parker BL (2010b) Plant oils for improving thermotolerance of Beauveria bassiana. J Microbiol Biotechnol 9:1348–1350

    Google Scholar 

  • Kim JS, Skinner M, Hata T, Parker BL (2010c) Effects of culture media on hydrophobicity and thermotolerance of bb and Ma conidia, with description of a novel surfactant based hydrophobicity assay. J Invertebr Pathol 105:322–328

    PubMed  Google Scholar 

  • Kim JS, Kassa A, Skinner M, Hata T, Parker BL (2011a) Production of thermotolerant entomopathogenic fungal conidia on millet grain. J Ind Microbiol Biotechnol 38:697–704

    CAS  PubMed  Google Scholar 

  • Kim JS, Skinner M, Gouli S, Parker BL (2011b) Generating thermotolerant colonies by pairing Beauveria bassiana isolates. FEMS Microbiol Lett 32:165–172

    Google Scholar 

  • Leng YJ, Peng GX, Cao YQ, Xia YX (2011) Genetically altering the expression of neutral trehalase gene affects conidiospore thermotolerance of the entomopathogenic fungus Metarhizium acridum. BMC Microbiol 11:32

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li F, Shi HQ, Ying SH, Feng MG (2015a) WetA and VosA are distinct regulators of conidiation capacity, conidial quality, and biological control potential of a fungal insect pathogen. Appl Microbiol Biotechnol 99:10069–10081

    CAS  PubMed  Google Scholar 

  • Li F, Wang ZL, Zhang LB, Ying SH, Feng MG (2015b) The role of three calcineurin subunits and a related transcription factor (Crz1) in conidiation, multistress tolerance and virulence of Beauveria bassiana. Appl Microbiol Biotechnol 99:827–840

    CAS  PubMed  Google Scholar 

  • Li F, Shi HQ, Ying SH, Feng MG (2015c) Distinct contributions of one Fe- and two Cu/Zn-cofactored superoxide dismutases to antioxidation, UV tolerance and virulence of Beauveria bassiana. Fungal Genet Biol 81:160–171

    CAS  PubMed  Google Scholar 

  • Li J, Feng MG (2009) Intraspecific tolerance of Metarhizium anisopliae conidia to the upper thermal limits of summer with a description of a quantitative assay system. Mycol Res 113:93–99

    PubMed  Google Scholar 

  • Li J, Ying SH, Shan LT, Feng MG (2010) A new non-hydrophobic cell wall protein (CWP10) of Metarhizium anisopliae enhances conidial hydrophobicity when expressed in Beauveria bassiana. Appl Microbiol Biotechnol 85:975–984

    CAS  PubMed  Google Scholar 

  • Liu J, Wang ZK, Sun HH, Ying SH, Feng MG (2017a) Characterization of the Hog1 MAPK pathway in the entomopathogenic fungus Beauveria bassiana. Environ Microbiol 19:1808–1821

    CAS  PubMed  Google Scholar 

  • Liu J, Sun HH, Ying SH, Feng MG (2017b) The Hog1-like MAPK Mpk3 collaborates with Hog1 in response to heat shock and functions in sustaining the biological control potential of a fungal insect pathogen. Appl Microbiol Biotechnol 101:6941–6949

    CAS  PubMed  Google Scholar 

  • Liu J, Tong SM, Qiu L, Ying SH, Feng MG (2017c) Two histidine kinases can sense different stress cues for activation of the MAPK Hog1 cascade in a fungal insect pathogen. Environ Microbiol 19:4091–4102

    CAS  PubMed  Google Scholar 

  • Liu Q, Ying SH, Feng MG, Jiang XH (2009) Physiological implication of intracellular trehalose and mannitol changes in response of entomopathogenic fungus Beauveria bassiana to thermal stress. Antonie Van Leeuwenhoek 95:65–75

    CAS  PubMed  Google Scholar 

  • Liu Q, Ying SH, Li JG, Tian CG, Feng MG (2013) Insight into the transcriptional regulation of Msn2 required for conidiation, multi-stress responses and virulence of two entomopathogenic fungi. Fungal Genet Biol 54:42–51

    CAS  PubMed  Google Scholar 

  • Liu Q, Li JG, Ying SH, Wang JJ, Sun WL, Tian CG, Fend MG (2015) Unveiling equal importance of two 14-3-3 proteins for morphogenesis, conidiation, multistress tolerance and virulence of an insect pathogen. Environ Microbiol 17:1444–1462

    CAS  PubMed  Google Scholar 

  • Lovett B, St Leger RJ (2018) Genetically engineering better fungal biopesticides. Pest Manag Sci 74:781–789

    CAS  PubMed  Google Scholar 

  • Lu HL, St Leger RJ (2016) Insect immunity to entomopathogenic fungi. Adv Genet 94:251–285

    CAS  PubMed  Google Scholar 

  • Luo XD, Keyhani NO, Yu XD, He ZJ, Luo ZB, Pei Y, Zhang YJ (2012) The MAP kinase Bbslt2 controls growth, conidiation, cell wall integrity, and virulence in the insect pathogenic fungus Beauveria bassiana. Fungal Genet Biol 54:544–555

    Google Scholar 

  • Ma QS, Jin K, Peng GX, Xia YX (2015) An ENA ATPase, MaENA1, of Metarhizium acridum influences the Na+-, thermo- and UV-tolerances of conidia and is involved in multiple mechanisms of stress tolerance. Fungal Genet Biol 83:68–77

    CAS  PubMed  Google Scholar 

  • Meikle WG, Mercadier G, Holst N, Nansen C, Girod V (2007) Duration and spread of an entomopathogenic fungus, Beauveria bassiana (Deuteromycota: Hyphomycetes), used to treat varroa mites, Varroa destructor (Acari: Varroidae), in honeybee hives (Hymenoptera: Apidae). J Econ Entomol 100:1–10

    CAS  PubMed  Google Scholar 

  • Meikle WG, Mercadier G, Holst N, Girod V (2008a) Impact of two treatments of a formulation of Beauveria bassiana (Deuteromycota: Hyphomycetes) conidia on Varroa mites (Acari: Varroidae) and on honeybee (Hymenoptera: Apidae) colony health. Exp Appl Acarol 46:105–117

    PubMed  Google Scholar 

  • Meikle WG, Mercadier G, Holst N, Nansen C, Girod V (2008b) Impact of a treatment of Beauveria bassiana (Deuteromycota: Hyphomycetes) on honeybee (Hymenoptera: Apidae) colony health and on varroa mites (Acari: Varroidae). Apidologie 39:1–13

    Google Scholar 

  • Meikle WG, Mercadier G, Annas F, Holst N (2009) Effects of multiple applications of a Beauveria-based biopesticide on Varroa destructor (Acari: Varroidae) densities in honey bee (Hymenoptera: Apidae) colonies. J Apic Res 48:220–222

    CAS  Google Scholar 

  • Meikle MG, Sammataro D, Neumann P, Pflugfelder J (2012) Challenges for developing pathogen-based biopesticides against Varroa destructor (Mesostigmata: Varroidae). Apidologie 43:501–514

    Google Scholar 

  • Ming Y, Wei QL, Jin K, Xia YX (2014) MaSnf1, a sucrose non-fermenting protein kinase gene, is involved in carbon source utilization, stress tolerance, and virulence in Metarhizium acridum. Appl Microbiol Biotechnol 98:10153–10164

    CAS  PubMed  Google Scholar 

  • Ortiz-Urquiza A, Keyhani NO (2013) Action on the surface: entomopathogenic fungi versus the insect cuticle. Insects 4:357–374

    PubMed  PubMed Central  Google Scholar 

  • Ortiz-Urquiza A, Keyhani NO (2015) Stress response signaling and virulence: insights from entomopathogenic fungi. Curr Genet 61:239–249

    CAS  PubMed  Google Scholar 

  • Ortiz-Urquiza A, Luo ZB, Keyhani NO (2015) Improving mycoinsecticides for insect biological control. Appl Microbiol Biotechnol 99:1057–1068

    CAS  PubMed  Google Scholar 

  • Park HS, Yu JH (2012) Genetic control of asexual sporulation in filamentous fungi. Curr Opin Microbiol 15:669–677

    CAS  PubMed  Google Scholar 

  • Pedrini N, Ortiz-Urquiza A, Huarte-Bonnet C, Zhang S, Keyhani NO (2013) Targeting of insect epicuticular lipids by the entomopathogenic fungus Beauveria bassiana: hydrocarbon oxidation within the context of a host-pathogen interaction. Front Microbiol 4:24

    PubMed  PubMed Central  Google Scholar 

  • Peng GX, Jin K, Liu YC, Xia YX (2015) Enhancing the utilization of host trehalose by fungal trehalase improves the virulence of fungal insecticide. Appl Microbiol Biotechnol 99:8611–8618

    CAS  PubMed  Google Scholar 

  • Peng GX, Tong SM, Zeng DY, Xia YX, Feng MG (2020) Colony heating protects honey bee populations from a risk of contact with wide-spectrum Beauveria bassiana insecticides applied in the field. Pest Manag Sci. https://doi.org/10.1002/ps.5803

  • Qiu L, Wang JJ, Ying SH, Feng MG (2015) Wee1 and Cdc25 control morphogenesis, virulence and multistress tolerance of Beauveria bassiana by balancing cell cycle-required cyclin-dependent kinase 1 activity. Environ Microbiol 17:1119–1133

    CAS  PubMed  Google Scholar 

  • Qiu L, Wei XY, Wang SJ, Wang JJ (2020) Characterization of trehalose-6-phosphate phosphatase in trehalose biosynthesis, asexual development, stress resistance and virulence of an insect mycopathogen. Pestic Biochem Physiol 163:85–192

    Google Scholar 

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

    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

    PubMed  Google Scholar 

  • Rangel DEN, Fernandes EKK, Dettenmaier SJ, Roberts DW (2010) Thermotolerance of germlings and mycelium of the insect-pathogenic fungus Metarhizium spp. and mycelial recovery after heat stress. J Basic Microbiol 50:344–350

    PubMed  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

    CAS  PubMed  Google Scholar 

  • Rangel DEN, Fernandes EKK, Anderson AJ, Roberts DW (2012) Culture of Metarhizium robertsii on salicylic-acid supplemented medium induces increased conidial thermotolerance. Fungal Biol 116:438–442

    CAS  PubMed  Google Scholar 

  • Rangel DEN, Braga GUL, Fernandes EKK, 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 61:383–404

    CAS  PubMed  Google Scholar 

  • Rangel DEN, Roberts DW (2018) Possible source of the high UV-B and heat tolerance of Metarhizium acridum (isolate ARSEF 324). J Invertebr Pathol 157:32–35

    PubMed  Google Scholar 

  • Rispail N, Soanes DM, Ant C, Czajkowski R, Grünler A, Huguet R, Perez-Nadales E, Poli A, Sartorel E, Valiante V, Yang M, Beffa R, Brakhage AA, Gow NAR, Kahmann R, Lebrun MH, Lenasi H, Perez-Martin J, Talbot NJ, Wendland J, Di Pietro A (2009) Comparative genomics of MAP kinase and calcium-calcineurin signaling components in plant and human pathogenic fungi. Fungal Genet Biol 46:287–298

    CAS  PubMed  Google Scholar 

  • Roberts DW, Campbell AS (1977) Stability of Entomopathogenic Fungi, vol. 10, Miscellaneous Publications of the Entomological Society of America, pp. 19–76

  • Roberts DW, St Leger RJ (2004) Metarhizium spp., cosmopolitan insect pathogenic fungi: mycological aspects. Adv Appl Microbiol 54:1–70

    CAS  PubMed  Google Scholar 

  • Rodríguez M, Gerding M, France A (2009) Selection of entomopathogenic fungi to control Varroa destructor (Acari: Varroidae). Chil J Agric Res 69:534–540

    Google Scholar 

  • Rosenkranz P, Aumeier P, Ziegelmann B (2010) Biology and control of Varroa destructor. J Invertebr Pathol 103:S96–S119

    PubMed  Google Scholar 

  • Ruijter GJG, Bax M, Patel H, Flitter SJ, van de Vondervoort PJI, de Vries RP, vanKuyk PA, Visser J (2003) Mannitol is required for stress tolerance in Aspergillus niger conidiospores. Eukaryot Cell 2:690–698

    CAS  PubMed  PubMed Central  Google Scholar 

  • Saibil HR (2008) Chaperone machines in action. Curr Opion Struct Biol 18:35–42

    CAS  Google Scholar 

  • Sinia A, Guzman-Novoa E (2018) Evaluation of the entomopathogenic fungi Beauveria bassiana GHA and Metarhizium anisopliae UAMH 9198 alone or in combination with thymol for the control of Varroa destructor in honey bee (Apis mellifera) colonies. J Apic Res 5:308–316

    Google Scholar 

  • Souza RKF, Azevedo RFF, Lobo AO, Rangel DEN (2014) Conidial water affinity is an important characteristic for thermotolerance in entomopathogenic fungi. Biocontrol Sci Tech 24:448–461

    Google Scholar 

  • Tong SM, Chen Y, Zhu J, Ying SH, Feng MG (2016a) Subcellular localization of five singular WSC domain-containing proteins and their roles in Beauveria bassiana responses to stress cues and metal ions. Env Microbiol Rep 8:295–304

    CAS  Google Scholar 

  • Tong SM, Chen Y, Ying SH, Feng MG (2016b) Three DUF1996 proteins localize in vacuoles and function in fungal responses to multiple stresses and metal ions. Sci Rep 6:20566

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tong SM, Feng MG (2019) Insights into regulatory roles of MAPK-cascaded pathways in multiple stress responses and life cycles of insect and nematode mycopathogens. Appl Microbiol Biotechnol 103:577–587

    CAS  PubMed  Google Scholar 

  • Tong SM, Wang DY, Gao BJ, Ying SH, Feng MG (2019) The DUF1996 and WSC domain-containing protein Wsc1I acts as a novel sensor of stress cues for Hog1 activation in Beauveria bassiana. Cell Microbiol 21:e13100

    CAS  PubMed  Google Scholar 

  • Tong SM, Wang DY, Cai Q, Ying SH, Feng MG (2020) Opposite nuclear dynamics of two FRH-dominated frequency proteins orchestrate non-rhythmic conidiation of Beauveria bassiana. Cells 9:626

    PubMed Central  Google Scholar 

  • Wang CS, Feng MG (2014) Advances in fundamental and applied studies in China of fungal biocontrol agents for use against arthropod pests. Biol Control 68:128–135

    Google Scholar 

  • Wang CS, Wang SB (2017) Insect pathogenic fungi: genomics, molecular interactions, and genetic improvements. Annu Rev Entomol 62:73–90

    CAS  PubMed  Google Scholar 

  • Wang DY, Tong SM, Guan Y, Ying SH, Feng MG (2019) The velvet protein VeA functions in asexual cycle, stress tolerance and transcriptional regulation of Beauveria bassiana. Fungal Genet Biol 127:1–11

    CAS  PubMed  Google Scholar 

  • Wang DY, Ren K, Tong SM, Ying SH, Feng MG (2020) Pleiotropic effects of Ubi4, a polyubiquitin precursor required for ubiquitin accumulation, conidiation and pathogenicity of a fungal insect pathogen. Environ Microbiol DOI. https://doi.org/10.1111/1462-2920.14940

  • Wang J, Zhou G, Ying SH, Feng MG (2013b) P-type calcium ATPase functions as a core regulator of Beauveria bassiana growth, conidiation and responses to multiple stressful stimuli through cross-talk with signaling networks. Environ Microbiol 15:967–979

    CAS  PubMed  Google Scholar 

  • Wang J, Liu J, Hu Y, Ying SH, Feng MG (2013c) Cytokinesis-required Cdc14 is a signaling hub of asexual development and multi-stress tolerance in Beauveria bassiana. Sci Rep 3:3086

    PubMed  PubMed Central  Google Scholar 

  • Wang J, Ying SH, Hu Y, Feng MG (2016) Mas5, a homologue of bacterial DnaJ, is indispensable for the host infection and environmental adaptation of a filamentous fungal insect pathogen. Environ Microbiol 18:1037–1047

    CAS  PubMed  Google Scholar 

  • Wang J, Ying SH, Hu Y, Feng MG (2017b) Vital role for the J-domain protein Mdj1 in asexual development, multiple stress tolerance and virulence of Beauveria bassiana. Appl Microbiol Biotechnol 101:185–195

    CAS  PubMed  Google Scholar 

  • Wang J, Zhu XG, Ying SH, Feng MG (2017c) Differential roles of six P-type calcium ATPases in sustaining intracellular Ca2+ homeostasis, asexual cycle and environmental fitness of Beauveria bassiana. Sci Rep 7:1420

    PubMed  PubMed Central  Google Scholar 

  • Wang JJ, Qiu L, Chu ZJ, Ying SH, Feng MG (2014a) The connection of protein O-mannosyltransferase family to the biocontrol potential of Beauveria bassiana, a fungal entomopathogen. Glycobiology 24:638–648

    CAS  PubMed  Google Scholar 

  • Wang JJ, Qiu L, Cai Q, Ying SH, Feng MG (2014b) Three α-1,2-mannosyltransferases contribute differentially to conidiation, cell wall integrity, multistress tolerance and virulence of Beauveria bassiana. Fungal Genet Biol 70:1–10

    PubMed  Google Scholar 

  • Wang JJ, Cai Q, Qiu L, Ying SH, Feng MG (2017a) Additive roles of two TPS genes in trehalose synthesis, conidiation, multiple stress responses and host infection of a fungal insect pathogen. Appl Microbiol Biotechnol 101:3637–3651

    CAS  PubMed  Google Scholar 

  • Wang JJ, Cai Q, Qiu L, Ying SH, Feng MG (2018b) The histone acetyltransferase Mst2 sustains the biological control potential of a fungal insect pathogen through transcriptional regulation. Appl Microbiol Biotechnol 102:1343–1355

    CAS  PubMed  Google Scholar 

  • Wang ZK, Cai Q, Tong SM, Ying SH, Feng MG (2018a) C-terminal Ser/Thr residues are vital for the regulatory role of Ste7 in the asexual cycle and virulence of Beauveria bassiana. Appl Microbiol Biotechnol 102:6973–6986

    CAS  PubMed  Google Scholar 

  • Wang ZL, Lu JD, Feng MG (2012) Primary roles of two dehydrogenases in the mannitol metabolism and multi-stress tolerance of entomopathogenic fungus Beauveria bassiana. Environ Microbiol 14:2139–2150

    CAS  PubMed  Google Scholar 

  • Wang ZL, Zhang LB, Ying SH, Feng MG (2013a) Catalases play differentiated roles in the adaptation of a fungal entomopathogen to environmental stresses. Environ Microbiol 15:409–418

    CAS  PubMed  Google Scholar 

  • Wösten HAB (2001) Hydrophobins: multipurpose proteins. Annu Rev Microbiol 55:625–646

    PubMed  Google Scholar 

  • Xie XQ, Li F, Ying SH, Feng MG (2012) Additive contributions of two manganese-cored superoxide dismutases (MnSODs) to anti-oxidation, UV tolerance and virulence of Beauveria bassiana. PLoS One 7:e30298

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ye SD, Ying SH, Chen C, Feng MG (2006) New solid-state fermentation chamber for bulk production of aerial conidia of fungal biocontrol agents on rice. Biotechnol Lett 28:799–804

    CAS  PubMed  Google Scholar 

  • Ying SH, Feng MG (2004) Relationship between thermotolerance and hydrophobin-like proteins in aerial conidia of Beauveria bassiana and Paecilomyces fumosoroseus as fungal biocontrol agents. J Appl Microbiol 97:323–331

    CAS  PubMed  Google Scholar 

  • Ying SH, Feng MG (2006) Medium components and culture conditions affect the thermotolerance of aerial conidia of fungal biocontrol agent Beauveria bassiana. Lett Appl Microbiol 43:331–335

    CAS  PubMed  Google Scholar 

  • Ying SH, Feng MG (2007) Means to mediating accumulation of hydrophobin-like proteins on the wall of Beauveria bassiana conidia for improved tolerance to thermal stress. J Gen Appl Microbiol 53:309–314

    CAS  PubMed  Google Scholar 

  • Ying SH, Feng MG (2011a) A conidial protein (CP15) of Beauveria bassiana contributes to the conidial tolerance of the entomopathogenic fungus to thermal and oxidative stresses. Appl Microbiol Biotechnol 90:1711–1720

    CAS  PubMed  Google Scholar 

  • Ying SH, Feng MG (2011b) Integration of Escherichia coli thioredoxin (trxA) into Beauveria bassiana enhances the fungal tolerance to the stresses of oxidation, heat and UV-B irradiation. Biol Control 59:255–260

    CAS  Google Scholar 

  • Ying SH, Feng MG (2019) Insight into vital role of autophagy in sustaining biological control potential of fungal pathogens against pest insects and nematodes. Virulence 10:429–437

    CAS  PubMed  Google Scholar 

  • Ying SH, Wang XH, Feng MG (2010) Characterization of a new thioredoxin (BbTrx) from entomopathogenic fungus Beauveria bassiana and its expression in response to thermal stress. Can J Microbiol 56:924–942

    Google Scholar 

  • Ying SH, Ji XP, Wang XX, Feng MG, Keyhani NO (2014) The transcriptional co-activator multiprotein bridging factor 1 from the fungal insect pathogen, Beauveria bassiana, mediates regulation of hyphal morphogenesis, stress tolerance, and virulence. Environ Microbiol 16:1879–1897

    CAS  PubMed  Google Scholar 

  • Zhang LB, Feng MG (2018) Antioxidant enzymes and their contributions to biological control potential of fungal insect pathogens. Appl Microbiol Biotechnol 102:4995–5004

    CAS  PubMed  Google Scholar 

  • Zhang LB, Tang L, Ying SH, Feng MG (2015) Subcellular localization of six thioredoxins and their antioxidant activity and contributions to biological control potential in Beauveria bassiana. Fungal Genet Biol 76:1–9

    CAS  PubMed  Google Scholar 

  • Zhang LB, Tang L, Ying SH, Feng MG (2016a) Distinct roles of cytoplasmic thioredoxin reductases Trr1 and Trr2 in the redox system involving cysteine synthesis and host infection of a fungal insect pathogen. Appl Microbiol Biotechnol 100:10363–10374

    CAS  PubMed  Google Scholar 

  • Zhang LB, Tang L, Ying SH, Feng MG (2016b) Regulative roles of glutathione reductase and four glutaredoxins in glutathione redox, antioxidant activity and iron homeostasis of Beauveria bassiana. Appl Microbiol Biotechnol 100:5907–5917

    CAS  PubMed  Google Scholar 

  • Zhang LB, Tang L, Ying SH, Feng MG (2017) Two eisosome proteins play opposite roles in autophagic control and sustain cell integrity, function and pathogenicity in Beauveria bassiana. Environ Microbiol 19:2037–2052

    CAS  PubMed  Google Scholar 

  • Zhang SZ, Xia YX, Keyhani NO (2011) Contribution of the gas1 gene of the entomopathogenic fungus Beauveria bassiana, encoding a putative glycosylphosphatidylinositol-anchored β-1,3-glucanosyltransferase, to conidial thermotolerance and virulence. Appl Environ Microbiol 77:2676–2684

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang YJ, Zhao JH, Fang WG, Zhang JQ, Luo ZB, Zhang M, Fan YH, Pei Y (2009) Mitogen-activated protein kinase hog1 in the entomopathogenic fungus Beauveria bassiana regulates environmental stress responses and virulence to insects. Appl Environ Microbiol 75:3787–3795

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao H, Lovett B, Fang WG (2016) Genetically engineering entomopathogenic fungi. Adv Genet 94:137–163

    CAS  PubMed  Google Scholar 

  • Zhao TT, Tian HT, Xia YX, Jin K (2019) MaPmt4, a protein O-mannosyltransferase, contributes to cell wall integrity, stress tolerance and virulence in Metarhizium acridum. Curr Genet 65:1025–1040

    CAS  PubMed  Google Scholar 

  • Zhou G, Wang J, Qiu L, Feng MG (2012) A group III histidine kinase (mhk1) upstream of high-osmolarity glycerol pathway regulates sporulation, multi-stress tolerance and virulence of Metarhizium robertsii, a fungal entomopathogen. Environ Microbiol 14:817–829

    CAS  PubMed  Google Scholar 

  • Zhou G, Ying SH, Hu Y, Xiang F, Feng MG, Wang J (2018) Roles of three HSF domain-containing proteins in mediating heat-shock protein genes and sustaining asexual cycle, stress tolerance and virulence in Beauveria bassiana. Front Microbiol 9:1677

    PubMed  PubMed Central  Google Scholar 

  • Zhu J, Zhu XG, Ying SH, Feng MG (2017a) Effect of vacuolar ATPase subunit H (VmaH) on cellular pH, asexual cycle, stress tolerance and virulence in Beauveria bassiana. Fungal Genet Biol 98:52–60

    CAS  PubMed  Google Scholar 

  • Zhu XG, Chu ZJ, Ying SH, Feng MG (2017b) Lysyl-tRNA synthetase (Krs) acts a virulence factor of Beauveria bassiana by its vital role in conidial germination and dimorphic transition. Fungal Biol 121:956–965

    CAS  PubMed  Google Scholar 

  • Zhu XG, Tong SM, Ying SH, Feng MG (2018) Antioxidant activities of four superoxide dismutases in Metarhizium robertsii and their contributions to pest control potential. Appl Microbiol Biotechnol 102:9221–9230

    CAS  PubMed  Google Scholar 

Download references

Funding

Funding of this work was provided by the National Natural Science Foundation of China (Grants 31801795 and 31772218) and the Ministry of Science and Technology of the People’s Republic of China (Grant 2017YFD0201202).

Author information

Affiliations

  1. College of Agricultural and Food Science, Zhejiang A&F University, Lin’an, Hangzhou, 311300, Zhejiang, China

    Sen-Miao Tong

  2. Institute of Microbiology, College of Life Sciences, Zhejiang University, Hangzhou, 310058, Zhejiang, China

    Ming-Guang Feng

Authors
  1. Sen-Miao Tong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ming-Guang Feng
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MGF conceived a necessity of this mini-review and sent a proposal to the Editor-in-Chief for approval. SMT prepared the first draft of the manuscript. MGF reviewed and revised the manuscript. All authors read and approved the manuscript.

Corresponding authors

Correspondence to Sen-Miao Tong or Ming-Guang Feng.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

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

Verify currency and authenticity via CrossMark

Cite this article

Tong, SM., Feng, MG. Phenotypic and molecular insights into heat tolerance of formulated cells as active ingredients of fungal insecticides. Appl Microbiol Biotechnol 104, 5711–5724 (2020). https://doi.org/10.1007/s00253-020-10659-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-020-10659-z

Keywords

  • Entomopathogenic fungi
  • Thermal limits
  • Thermo-tolerance
  • Trehalose
  • Mannitol
  • Cell wall integrity
  • Stress response
  • Biological control