Applied Microbiology and Biotechnology

, Volume 102, Issue 12, pp 4995–5004 | Cite as

Antioxidant enzymes and their contributions to biological control potential of fungal insect pathogens

Mini-Review

Abstract

Filamentous fungal insect pathogens represent a source of biological insecticides and acaricides formulated using intact cells, such as conidia or other spores. These mycoinsecticides infect arthropod pests through cuticular penetration. In field application, formulated fungal cells are exposed to environmental stresses, including solar UV irradiation, high temperature, and applied chemical herbicides and fungicides, as well as stress from host immune defenses. These stresses often result in accumulation of toxic reactive oxygen species (ROS), generating oxidative stress to the fungal cells and hence affecting the efficacy and persistency of fungi formulated for pest control. In response, fungi have evolved effective antioxidant mechanisms that include enzyme families that act as ROS scavengers, e.g., superoxide dismutases, catalases, peroxidases, thioredoxins /thioredoxin reductases, and glutaredoxins/glutathione reductases. Over two dozen antioxidant enzymes dispersed in different families have been characterized in Beauveria bassiana in recent years. This mini-review focuses on the progress detailed in the studies of these enzymes and provides an overview of their antioxidant activities and contributions to conidial thermotolerance, UV resistance and virulence. These activities are crucial for the biological control potential of mycoinsecticide formulation and have significantly advanced our understanding of how these organisms work. Several potent antioxidant genes have been exploited for successful genetic engineering of entomopathogenic fungi aimed at enhancing their potential against arthropod pests.

Keywords

Entomopathogenic fungi Antioxidant machinery ROS decomposition Stress tolerance Virulence 

Notes

Funding information

This work was financially supported by the Ministry of Science and Technology of the People’s Republic of China (Grant No.: 2017YFD0201202) and the National Natural Science Foundation of China (Grant No.: 31772218).

Compliance with ethical standards

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.

References

  1. Abdalla M, Dai YN, Chi CB, Cheng W, Cao DD, Zhou K, Ali W, Chen YX, Zhou CZ (2016) Crystal structure of yeast monothiol glutaredoxin Grx6 in complex with a glutathione-coordinated [2Fe-2S] cluster. Acta Crystallogr F-Struct Biol Commun 72:732–737CrossRefPubMedPubMedCentralGoogle Scholar
  2. Ali S, Huang Z, Li H, Bashir MH, Ren S (2013) Antioxidant enzyme influences germination, stress tolerance, and virulence of Isaria fumosorosea. J Basic Microbiol 53:489–497CrossRefPubMedGoogle Scholar
  3. Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53:1331–1341CrossRefPubMedGoogle Scholar
  4. Arner ES, Holmgren A (2000) Physiological functions of thioredoxin and thioredoxin reductase. Eur J Biochem 267:6102–6109CrossRefPubMedGoogle Scholar
  5. Bai Z, Harvey LM, McNeil B (2003) Elevated temperature effects on the oxidant/antioxidant balance in submerged batch cultures of the filamentous fungus Aspergillus niger B1-D. Biotechnol Bioeng 83:772–779CrossRefPubMedGoogle Scholar
  6. Broxton CN, Culotta VC (2016) SOD enzymes and microbial pathogens: surviving the oxidative storm of infection. PLoS Pathog 12:e1005295CrossRefPubMedPubMedCentralGoogle Scholar
  7. Butt TM, Coates CJ, Dubovskiy IM, Ratcliffe NA (2016) Entomopathogenic fungi: new insights into host-pathogen interactions. Adv Genet 94:307–364PubMedGoogle Scholar
  8. Cai Q, Tong SM, Shao W, Ying SH, Feng MG (2018a) 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.  https://doi.org/10.1111/cmi.12839 CrossRefGoogle Scholar
  9. Cai Q, Wang JJ, Fu B, Ying SH, Feng MG (2018b) Gcn5-dependent histone H3 acetylation and gene activity is required for the asexual development and virulence of Beauveria bassiana. Environ Microbiol 20:1484–1497.  https://doi.org/10.1111/1462-2920.14066 CrossRefPubMedGoogle Scholar
  10. Cai Q, Wang ZK, Shao W, Ying SH, Feng MG (2018c) Essential role of Rpd3-dependent lysine modification in the growth, development and virulence of Beauveria bassiana. Environ Microbiol 20:1590–1606.  https://doi.org/10.1111/1462-2920.14100 CrossRefPubMedGoogle Scholar
  11. Chantasingh D, Kitikhun S, Keyhani NO, Boonyapakron K, Thoetkiattikul H, Pootanakit K, Eurwilaichitr L (2013) Identification of catalase as an early up-regulated gene in Beauveria bassiana and its role in entomopathogenic fungal virulence. Biol Control 67:85–93CrossRefGoogle Scholar
  12. Chen Y, Zhu J, Ying SH, Feng MG (2014) Three mitogen-activated protein kinases required for cell wall integrity contribute greatly to biocontrol potential of a fungal entomopathogen. PLoS One 9:e87948CrossRefPubMedPubMedCentralGoogle Scholar
  13. Chen YX, Feng P, Shang YF, Xu YJ, Wang CS (2015) Biosynthesis of non-melanin pigment by a divergent polyketide synthase in Metarhizium robertsii. Fungal Genet Biol 81:142–149CrossRefPubMedGoogle Scholar
  14. 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 101:5033–5043CrossRefPubMedGoogle Scholar
  15. Chu ZJ, Sun HH, Ying SH, Feng MG (2017) Vital role for cyclophilin B (CypB) in asexual development, dimorphic transition and virulence of Beauveria bassiana. Fungal Genet Biol 105:8–15CrossRefPubMedGoogle Scholar
  16. Couturier J, Stroher E, Albetel AN, Roret T, Muthuramalingam M, Tarrago L, Seidel T, Tsan P, Jacquot JP, Johnson MK, Dietz KJ, Didierjean C, Rouhier N (2011) Arabidopsis chloroplastic glutaredoxin C5 as a model to explore molecular determinants for iron-sulfur cluster binding into glutaredoxins. J Biol Chem 286:27515–27527CrossRefPubMedPubMedCentralGoogle Scholar
  17. Culotta VC, Yang M, O'Halloran TV (2006) Activation of superoxide dismutases: putting the metal to the pedal. BBA-Mol Cell Res 1763:747–758Google Scholar
  18. Discola KF, de Oliveira MA, Cussiol JRR, Monteiro G, Barcena JA, Porras P, Padilla CA, Guimaraes BG, Netto LES (2009) Structural aspects of the distinct biochemical properties of glutaredoxin 1 and glutaredoxin 2 from Saccharomyces cerevisiae. J Mol Biol 385:889–901CrossRefPubMedGoogle Scholar
  19. Dong WX, Ding JL, Gao Y, Peng YJ, Feng MG, Ying SH (2017) Transcriptomic insights into the alternative splicing-mediated adaptation of the entomopathogenic fungus Beauveria bassiana to host niches: autophagy-related gene 8 as an example. Environ Microbiol 19:4126–4139CrossRefPubMedGoogle Scholar
  20. Faria M, Wraight SP (2002) Biological control of Bemisia tabaci with fungi. Crop Prot 20:767–778CrossRefGoogle Scholar
  21. de Faria MR, Wraight SP (2007) Mycoinsecticides and Mycoacaricides: a comprehensive list with worldwide coverage and international classification of formulation types. Biol Control 43:237–256CrossRefGoogle Scholar
  22. Feng MG, Poprawski TJ, Khachatourians GG (1994) Production, formulation and application of the entomopathogenic fungus Beauveria bassiana for insect control: current status. Biocontrol Sci Technol 4:3–34CrossRefGoogle Scholar
  23. Forlani L, Juarez MP, Lavarias S, Pedrini N (2014) Toxicological and biochemical response of the entomopathogenic fungus Beauveria bassiana after exposure to deltamethrin. Pest Manag Sci 70:751–756CrossRefPubMedGoogle Scholar
  24. Fridovich I (1983) Superoxide radical: an endogenous toxicant. Annu Rev Pharmacol Toxicol 23:239–257CrossRefPubMedGoogle Scholar
  25. Gallogly MM, Starke DW, Leonberg AK, Ospina SM, Mieyal JJ (2008) Kinetic and mechanistic characterization and versatile catalytic properties of mammalian glutaredoxin 2: implications for intracellular roles. Biochemistry 47:11144–11157CrossRefPubMedPubMedCentralGoogle Scholar
  26. Gao Q, Jin K, Ying SH, Zhang YJ, Xiao GH, Shang YF, Duan ZB, Hu X, Xie XQ, Zhou G, Peng GX, Luo ZB, Huang W, Wang B, Fang WG, Wang SB, Zhong Y, Ma LJ, St. Leger RJ, Zhao GP, Pei Y, Feng MG, Xia YX, Wang CS (2011) Genome sequencing and comparative transcriptomics of the model entomopathogenic fungi Metarhizium anisopliae and M. acridum. PLoS Genet 7:e1001264CrossRefPubMedPubMedCentralGoogle Scholar
  27. Greetham D, Grant CM (2009) Antioxidant activity of the yeast mitochondrial one-Cys peroxiredoxin is dependent on thioredoxin reductase and glutathione in vivo. Mol Cell Biol 29:3229–3240CrossRefPubMedPubMedCentralGoogle Scholar
  28. He ZJ, Zhang SH, Keyhani NO, Song YL, Huang SS, Pei Y, Zhang YJ (2015) A novel mitochondrial membrane protein, Ohmm, limits fungal oxidative stress resistance and virulence in the insect fungal pathogen, Beauveria bassiana. Environ Microbiol 17:4213–4238CrossRefPubMedGoogle Scholar
  29. Hernandez CEM, Guerrero IEP, Hernandez GAG, Solis ES, Guzman JCT (2010) Catalase overexpression reduces the germination time and increases the pathogenicity of the fungus Metarhizium anisopliae. Appl Microbiol Biotechnol 87:1033–1044CrossRefGoogle Scholar
  30. Huang Z, Ali S, Ren S (2012) Catalase production influences germination, stress tolerance and virulence of Lecanicillium muscarium conidia. Biocontrol Sci Techn 22:249–260CrossRefGoogle Scholar
  31. Huarte-Bonnet C, Juarez MP, Pedrini N (2015) Oxidative stress in entomopathogenic fungi grown on insect-like hydrocarbons. Curr Genet 61:289–297CrossRefPubMedGoogle Scholar
  32. Jacob RA (1995) The integrated antioxidant system. Nutr Res 15:755–766CrossRefGoogle Scholar
  33. 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 158:2987–2996CrossRefGoogle Scholar
  34. Jiravanichpaisal P, Lee BL, Soderhall K (2006) Cell-mediated immunity in arthropods: hematopoiesis, coagulation, melanization and opsonization. Immunobiology 211:213–236CrossRefPubMedGoogle Scholar
  35. Li H, Outten CE (2012) Monothiol CGFS glutaredoxins and BolA-like proteins: [2Fe-2S] binding partners in iron homeostasis. Biochemistry 51:4377–4389CrossRefPubMedPubMedCentralGoogle Scholar
  36. Li F, Shi HQ, Ying SH, Feng MG (2015a) Distinct contributions of one Fe- and two Cu/Zn-cofactored superoxide dismutases to antioxidation, UV tolerance and virulence of Beauveria bassiana. Fungal Genet Biol 81:160–171CrossRefPubMedGoogle Scholar
  37. 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 99:827–840CrossRefPubMedGoogle Scholar
  38. Li GH, Fan AN, Peng GX, Keyhani NO, Xin JK, Cao YQ, Xia YX (2017) A bifunctional catalase-peroxidase, MakatG1, contributes to virulence of Metarhizium acridum by overcoming oxidative stress on the host insect cuticle. Environ Microbiol 19:4365–4378CrossRefPubMedGoogle Scholar
  39. Liu J, Wang ZK, Sun HH, Ying SH, Feng MG (2017) Characterization of the Hog1 MAPK pathway in the entomopathogenic fungus Beauveria bassiana. Environ Microbiol 19:1808–1821CrossRefPubMedGoogle Scholar
  40. Lovett B, St Leger RJ (2018) Genetically engineering better fungal biopesticides. Pest Manag Sci 74:781–789CrossRefPubMedGoogle Scholar
  41. Lu HL, St Leger RJ (2016) Insect immunity to entomopathogenic fungi. Adv Genet 94:251–285PubMedGoogle Scholar
  42. Mahmood DF, Abderrazak A, El Hadri K, Simmet T, Rouis M (2013) The thioredoxin system as a therapeutic target in human health and disease. Antioxid Redox Signal 19:1266–1303CrossRefPubMedGoogle Scholar
  43. Mari M, Morales A, Colell A, Garcia-Ruiz C, Fernandez-Checa JC (2009) Mitochondrial glutathione, a key survival antioxidant. Antioxid Redox Signal 11:2685–2700CrossRefPubMedPubMedCentralGoogle Scholar
  44. Mashamaite LN, Rohwer JM, Pillay CS (2015) The glutaredoxin mono- and di-thiol mechanisms for deglutathionylation are functionally equivalent: implications for redox systems biology. Biosci Rep 35:e00173CrossRefPubMedPubMedCentralGoogle Scholar
  45. Murakami K, Tsubouchi R, Fukayama M, Yoshino M (2014) Copper-dependent inhibition and oxidative inactivation with affinity cleavage of yeast glutathione reductase. Biometals 27:551–558CrossRefPubMedGoogle Scholar
  46. Mustacich D, Powis G (2000) Thioredoxin reductase. Biochem J 346:1–8CrossRefPubMedPubMedCentralGoogle Scholar
  47. Ortiz-Urquiza A, Keyhani NO (2013) Action on the surface: entomopathogenic fungi versus the insect cuticle. Insects 4:357–374CrossRefPubMedPubMedCentralGoogle Scholar
  48. Ortiz-Urquiza A, Keyhani NO (2015) Stress response signaling and virulence: insights from entomopathogenic fungi. Curr Genet 61:239–249CrossRefPubMedGoogle Scholar
  49. Ortiz-Urquiza A, Keyhani NO (2016) Molecular genetics of Beauveria bassiana infection of insects. Adv Genet 94:165–249PubMedGoogle Scholar
  50. Ortiz-Urquiza A, Luo ZB, Keyhani NO (2015) Improving mycoinsecticides for insect biological control. Appl Microbiol Biotechnol 99:1057–1068CrossRefPubMedGoogle Scholar
  51. 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 4:24CrossRefPubMedPubMedCentralGoogle Scholar
  52. Pham LN, Dionne MS, Shirasu-Hiza M, Schneider DS (2007) A specific primed immune response in Drosophila is dependent on phagocytes. PLoS Pathog 3:e26CrossRefPubMedPubMedCentralGoogle Scholar
  53. Puigpinos J, Casas C, Herrero E (2015) Altered intracellular calcium homeostasis and endoplasmic reticulum redox state in Saccharomyces cerevisiae cells lacking Grx6 glutaredoxin. Mol Biol Cell 26:104–116CrossRefPubMedPubMedCentralGoogle Scholar
  54. Rietsch A, Beckwith J (1998) The genetics of disulfide bond metabolism. Annu Rev Genet 32:163–184CrossRefPubMedGoogle Scholar
  55. Roberts DW, St Leger RJ (2004) Metarhizium spp., cosmopolitan insect-pathogenic fungi: mycological aspects. Adv Appl Microbiol 54:1–70CrossRefPubMedGoogle Scholar
  56. Schouten A, Tenberge KB, Vermeer J, Stewart J, Wagemakers L, Williamson B, van Kan JA (2002) Functional analysis of an extracellular catalase of Botrytis cinerea. Mol Plant Pathol 3:227–238CrossRefPubMedGoogle Scholar
  57. Shin Y, Lee S, Ku M, Kwak MK, Kang SO (2017) Cytochrome c peroxidase regulates intracellular reactive oxygen species and methylglyoxal via enzyme activities of erythroascorbate peroxidase and glutathione-related enzymes in Candida albicans. Int J Biochem Cell Biol 92:183–201CrossRefPubMedGoogle Scholar
  58. Slade D, Radman M (2011) Oxidative stress resistance in Deinococcus radiodurans. Microbiol Mol Biol Rev 75:133–191CrossRefPubMedPubMedCentralGoogle Scholar
  59. Stroher E, Millar AH (2012) The biological roles of glutaredoxins. Biochem J 446:333–348CrossRefPubMedGoogle Scholar
  60. Tan SX, Greetham D, Raeth S, Grant CM, Dawes IW, Perrone GG (2010) The thioredoxin-thioredoxin reductase system can function in vivo as an alternative system to reduce oxidized glutathione in Saccharomyces cerevisiae. J Biol Chem 285:6118–6126CrossRefPubMedGoogle Scholar
  61. Thon M, Al-Abdallah Q, Hortschansky P, Brakhage AA (2007) The thioredoxin system of the filamentous fungus Aspergillus nidulans: impact on development and oxidative stress response. J Biol Chem 282:27259–27269CrossRefPubMedGoogle Scholar
  62. Ukai Y, Kishimoto T, Ohdate T, Izawa S, Inoue Y (2011) Glutathione peroxidase 2 in Saccharomyces cerevisiae is distributed in mitochondria and involved in sporulation. Biochem Biophys Res Commun 411:580–585CrossRefPubMedGoogle Scholar
  63. Wang CS, Feng MG (2014) Advances in fundamental and applied studies in China of fungal biocontrol agents for use against arthropod pests. Biol Control 68:128–135Google Scholar
  64. Wang CS, Wang SB (2017) Insect pathogenic fungi: genomics, molecular interactions, and genetic improvements. Annu Rev Entomol 62:73–90CrossRefPubMedGoogle Scholar
  65. 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 15:409–418CrossRefPubMedGoogle Scholar
  66. 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 15:967–979CrossRefPubMedGoogle Scholar
  67. 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 3:3086CrossRefPubMedPubMedCentralGoogle Scholar
  68. Wang JJ, Qiu L, Cai Q, Ying SH, Feng MG (2015) Transcriptional control of fungal cell cycle and cellular events by Fkh2, a forkhead transcription factor in an insect pathogen. Sci Rep 5:10108CrossRefPubMedPubMedCentralGoogle Scholar
  69. Wang JB, St Leger RJ, Wang C (2016a) Advances in genomics of entomopathogenic fungi. Adv Genet 94:67–105PubMedGoogle Scholar
  70. Wang J, Ying SH, Hu Y, Feng MG (2016b) Mas5, a homologue of bacterial DnaJ, is indispensable for the host infection and environmental adaptation of a filamentous fungal insect pathogen. Environm Microbiol 18:1037–1047CrossRefGoogle Scholar
  71. Wang J, Zhu XG, Ying SH, Feng MG (2017a) Differential roles of six P-type calcium ATPases in sustaining intracellular Ca2+ homeostasis, asexual cycle and environmental fitness of Beauveria bassiana. Sci Rep 7:1420CrossRefPubMedPubMedCentralGoogle Scholar
  72. 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 101:185–195CrossRefPubMedGoogle Scholar
  73. Wang JJ, Cai Q, Qiu L, Ying SH, Feng MG (2018) The histone acetyltransferase Mst2 sustains the biological control potential of a fungal insect pathogen through transcriptional regulation. Appl Microbiol Biotechnol 102:1343–1355CrossRefPubMedGoogle Scholar
  74. Winterbourn CC, Kettle AJ (2013) Redox reactions and microbial killing in the neutrophil phagosome. Antioxid Redox Signal 18:642–660CrossRefPubMedGoogle Scholar
  75. Wipf P, Lynch SM, Birmingham A, Tamayo G, Jimenez A, Campos N, Powis G (2004) Natural product based inhibitors of the thioredoxin-thioredoxin reductase system. Org Biomol Chem 2:1651–1658CrossRefPubMedGoogle Scholar
  76. Xiao GH, Ying SH, Zheng P, Wang ZL, Zhang SW, Xie XQ, Shang YF, Zheng HJ, Zhou Y, St Leger RJ, Zhao GP, Wang CS, Feng MG (2012) Genomic perspectives on the evolution of fungal entomopathogenicity in Beauveria bassiana. Sci Rep 2:483CrossRefPubMedPubMedCentralGoogle Scholar
  77. Xie XQ, Ying SH, Feng MG (2010a) Characterization of a new Cu/Zn-superoxide dismutase from Beauveria bassiana and two site-directed mutations crucial to its antioxidation activity without chaperon. Enzym Microb Technol 46:217–222CrossRefGoogle Scholar
  78. Xie XQ, Wang J, Huang BF, Ying SH, Feng MG (2010b) A new manganese superoxide dismutase identified from Beauveria bassiana enhances virulence and stress tolerance when overexpressed in the fungal pathogen. Appl Microbiol Biotechnol 86:1543–1553CrossRefPubMedGoogle Scholar
  79. Xie XQ, Li F, Ying SH, Feng MG (2012) Additive contributions of two manganese-cored superoxide dismutases (MnSODs) to antioxidation, UV tolerance and virulence of Beauveria bassiana. PLoS One 7:e30298CrossRefPubMedPubMedCentralGoogle Scholar
  80. Xie XQ, Guan Y, Ying SH, Feng MG (2013) Differentiated functions of Ras1 and Ras2 proteins in regulating the germination, growth, conidiation, multi-stress tolerance and virulence of Beauveria bassiana. Environ Microbiol 15:447–462CrossRefPubMedGoogle Scholar
  81. Yassine H, Kamareddine L, Osta MA (2012) The mosquito melanization response is implicated in defense against the entomopathogenic fungus Beauveria bassiana. PLoS Pathog 8:e1003029CrossRefPubMedPubMedCentralGoogle Scholar
  82. 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 76:1–9CrossRefPubMedGoogle Scholar
  83. Zhang LB, Tang L, Ying SH, Feng MG (2016a) Distinct roles of two cytoplasmic thioredoxin reductases (Trr1/2) in the redox system involving cysteine synthesis and host infection of Beauveria bassiana. Appl Microbiol Biotechnol 100:10363–10374CrossRefPubMedGoogle Scholar
  84. 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 100:5907–5917CrossRefPubMedGoogle Scholar
  85. Zhang D, Dong YJ, Yu QL, Kai Z, Zhang M, Jia C, Xiao CP, Zhang B, Zhang B, Li MC (2017a) Function of glutaredoxin 3 (Grx3) in oxidative stress response caused by iron homeostasis disorder in Candida albicans. Future Microbiol 12:1397–1412CrossRefPubMedGoogle Scholar
  86. Zhang LB, Tang L, Ying SH, Feng MG (2017b) Two eisosome proteins play opposite roles in autophagic control and sustain cell integrity, function and pathogenicity in Beauveria bassiana. Environ Microbiol 19:2037–2052CrossRefPubMedGoogle Scholar
  87. Zhao H, Lovett B, Fang W (2016) Genetically engineering entomopathogenic fungi. Adv Genet 94:137–163PubMedGoogle Scholar
  88. Zheng P, Xia YL, Xiao GH, Xiong CH, Zhang SW, Zheng HJ, Huang Y, Zhou Y, Wang SY, Zhao G-P, Liu XZ, St. Leger RJ, Wang CS (2011) Genome sequence of the insect pathogenic fungus Cordyceps militaris, a valued traditional Chinese medicine. Genome Biol 12:R116CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.School of Medicine and Biomedical SciencesHuaqiao UniversityQuanzhouChina
  2. 2.Institute of Microbiology, College of Life SciencesZhejiang UniversityHangzhouChina

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