Skip to main content
Log in

The functions of glutathione peroxidase in ROS homeostasis and fruiting body development in Hypsizygus marmoreus

  • Applied genetics and molecular biotechnology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Glutathione peroxidase (GPX) is one of the most important antioxidant enzymes for maintaining reactive oxygen species (ROS) homeostasis. Although studies on fungi have suggested many important physiological functions of GPX, few studies have examined the role of this enzyme in Basidiomycetes, particularly its functions in fruiting body developmental processes. In the present study, GPX-silenced (GPxi) strains were obtained by using RNA interference. The GPxi strains of Hypsizygus marmoreus showed defects in mycelial growth and fruiting body development. In addition, the results indicated essential roles of GPX in controlling ROS homeostasis by regulating intracellular H2O2 levels, maintaining GSH/GSSG balance, and promoting antioxidant enzyme activity. Furthermore, lignocellulose enzyme activity levels were reduced and the mitochondrial phenotype and mitochondrial complex activity levels were changed in the H. marmoreus GPxi strains, possibly in response to impediments to mycelial growth and fruiting body development. These findings indicate that ROS homeostasis has a complex influence on growth, fruiting body development, GSH/GSSG balance, and carbon metabolism in H. marmoreus.

Key points

ROS balance, energy metabolism, fruiting development.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Data availability

The data and material of this manuscript were available.

References

  • Aguirre J, Ríos-Momberg M, Hewitt D, Hansberg W (2005) Reactive oxygen species and development in microbial eukaryotes. Trends Microbiol 13:111–118

    Article  CAS  PubMed  Google Scholar 

  • Averyanov AA, Lapikova VP (1990) Activated oxygen as a possible factor in the autoinhibition of spore germination of the fungus Pyricularia oryzae. Biochem-Moscow 55(10):1397–1402

    Google Scholar 

  • Barros MH, McStay GP (2020) Modular biogenesis of mitochondrial respiratory complexes. Mitochondrion 50:94–114

    Article  CAS  PubMed  Google Scholar 

  • Breitenbach M, Weber M, Rinnerthaler M, Karl T, Breitenbach-Koller L (2015) Oxidative stress in fungi: its function in signal transduction, interaction with plant hosts, and lignocellulose degradation. Biomolecules 5:318–342

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baudouin-Cornu P, Lagniel G, Kumar C, Huang ME, Labarre J (2012) Glutathione degradation is a key determinant of glutathione homeostasis. J Biol Chem 287(7):4552–4561

    Article  CAS  PubMed  Google Scholar 

  • D’Autréaux B, Toledano MB (2007) ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat Rev Mol Cell Biol 8:813–824

    Article  PubMed  CAS  Google Scholar 

  • Brigelius-Flohe R (1999) Tissue-specific functions of individual glutathione peroxidases. Free Radic Biol Med 27(9–10):951–965

    Article  CAS  PubMed  Google Scholar 

  • Branco V, Coppo L, Solá S, Lu J, Rodrigues CMP, Holmgren A, Carvalho C (2017) Impaired cross-talk between the thioredoxin and glutathione systems is related to ASK-1 mediated apoptosis in neuronal cells exposed to mercury. Redox Biol 13:278–287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blokhina O, Virolainen E, Fagerstedt KV (2003) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot 91:179–194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bissaro B, Varnai A, Rohr AK, Eijsink VGH (2018) Oxidoreductase and reactive oxygen species in conversion of lignocellulosic biomass. Microbiol Mol Biol Res 82(4):e00029–e00018

    CAS  Google Scholar 

  • Chen H, Hao HB, Wang H, Wang Q, Chen MJ, Feng ZY, Ye M, Zhang JJ (2018) Hydrogen-rich water mediates redox regulation of the antioxidant system, mycelial regeneration and fruiting body development in Hypsizygus marmoreus. Fungal Biol 122:310–321

    Article  CAS  PubMed  Google Scholar 

  • Chen H, Hao HB, Han CC, Wang H, Wang Q, Chen MJ, Juan JX, Feng ZY, Zhang JJ (2020) Exogenous L-ascorbic acid regulates the antioxidant system to increase the regeneration of damaged mycelia and induce the development of fruiting bodies in Hypsizygus marmoreus. Fungal Biol 124:551–561

    Article  CAS  PubMed  Google Scholar 

  • Carberry S, Molloy E, Hammel S, O’Keeffe G, Jones GW, Kavanagh K, Doyle S (2012) Gliotoxin effects on fungal growth: mechanisms and exploitation. Fungal Genet Biol 49:302–312

    Article  CAS  PubMed  Google Scholar 

  • Drakulic T, Temple MD, Guido R, Jarolim S, Breitenbach M, Attfield PV, Dawes IW (2005) Involvement of oxidative stress response genes in redox homeostasis, the level of reactive oxidative species, and ageing in Saccharomyces cerevisiae. FEMS Yeast Res 5:1215–1228

    Article  CAS  PubMed  Google Scholar 

  • Gyongyosi N, Nagy D, Makara K, Ella K, Kaldi K (2013) Reactive oxygen species can modulate circadian phase and period in Neurospora crassa. Free Radic Biol Med 58:134–143

    Article  CAS  PubMed  Google Scholar 

  • Hansberg W, Degroot H, Sies H (1993) Reactive oxygen species associated with cell-differentiation in Neurospora crassa. Free Radical Bio Med 14(3):287–293

    Article  CAS  Google Scholar 

  • Holmgren A, Johansson C, Berndt C, Lönn ME, Hudemann C, Lillig CH (2005) Thiol redox control via thioredoxin and glutaredoxin systems. Biochem Soc Trans 33:1375–1377

    Article  CAS  PubMed  Google Scholar 

  • Huang K, Czymmek KJ, Caplan J, Sweigard JA, Donofrio NM (2011) HYR1-mediated detoxification of reactive oxygen species is required for full virulence in the rice blast fungus. PLoS Pathog 7:e1001335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harada A, Yoneyama S, Doi SC, Aoyama M (2003) Changes in contents of free amino acids and soluble carbohydrates during fruit-body development of Hypsizygus marmoreus. Food Chem 83:343–347

    Article  CAS  Google Scholar 

  • Hansberg W, Aguirre J (1990) Hyperoxidant states cause microbial cell differentiation by cell isolation from dioxygen. J Tgeor Biol 142:201–221

    Article  CAS  Google Scholar 

  • Jones DP, Liang Y (2009) Measuring the poise of thiol/disulfide couples in vivo. Free Radic Biol Med 47:1329–1338

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kowalec P, Grynberg M, Pajak B, Socha A, Winiarska K, Fronk J, Kurlandzka A (2015) Newly identified protein Imi1 affects mitochondrial integrity and glutathione homeostasis in Saccharomyces cerevisiae. FEMS Yeast Res 15:fov048

    Article  PubMed  CAS  Google Scholar 

  • Lam SK, Ng TB (2001) Hypsin, a novel thermostable ribosome-inactivating protein with antifungal and antiproliferative activities from fruiting bodies of the edible mushroom Hypsizigus marmoreus. Biochem Bioph Res Co 285:1071–1075

    Article  CAS  Google Scholar 

  • Leuthner B, Aichinger C, Oehmen E, Koopmann E, Müller O, Müller P, Kahmann R, Bölker M, Schreier PH (2005) A H2O2-producing glyoxal oxidase is required for filamentous growth and pathogenicity in Ustilago maydis. Mol Gen Genomics 272:639–650

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-DeltaC(T)) method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Liu GQ, Qiu XH, Cao L, Han RC (2018) Scratching stimuli of mycelia influence fruiting body production and ROS-scavenging gene expression of Cordyceps militaris. Mycobiol 46(4):382–387

    Article  Google Scholar 

  • Luikenhuis S, Perrone G, Dawes IW, Grant CM (1998) The yeast Saccharomyces cerevisiae contains two glutaredoxin genes that are required for protection against reactive oxygen species. Mol Biol Cell 9:1081–1091

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li CY, Shi L, Chen DD, Ren A, Gao T, Zhao MW (2015) Functional analysis of the role of glutathione peroxidase (GPx) in the ROS signaling pathway, hyphal branching and the regulation of ganoderic acid biosynthesis in Ganoderma lucidum. Fungal Genet Biol 82:168–180

    Article  CAS  PubMed  Google Scholar 

  • Liu M, Song XL, Zhang JJ, Zhang C, Gao Z, Li SS, Jing HJ, Ren ZZ, Wang SX, Jia L (2017) Protective effects on liver, kidney and pancreas of enzymatic- and acidic-hydrolysis of polysaccharides by spent mushroom compost (Hypsizigus marmoreus). Sci Rep 7:43212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meister A, Anderson ME (1983) Glutathione. Annu Rev Biochem 52:711–760

    Article  CAS  PubMed  Google Scholar 

  • Min B, Kim S, Oh YL, Kong WS, Park H, Cho HJ, Jang KY, Kim JG, Choi IG (2018) Genomic discovery of the hypsin gene and biosynthetic pathways for terpenoids in Hypsizygus marmoreus. BMC Genomics 19:789

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mu DS, Li CY, Zhang XC, Li XB, Shi L, Ren A, Zhao MW (2014) Functions of the nicotinamide adenine dinucleotide phosphate oxidase family in Ganoderma lucidum: an essential role in ganoderic acid biosynthesis regulation, hyphal branching, fruiting body development, and oxidative-stress resistance. Environ Microbiol 16:1709–1728

    Article  CAS  PubMed  Google Scholar 

  • Morgan B, Ezeriņa D, Amoako TNE, Riemer J, Seedorf M, Dick TP (2013) Multiple glutathione disulfide removal pathways mediate cytosolic redox homeostasis. Nat Chem Biol 9:119–127

    Article  CAS  PubMed  Google Scholar 

  • Mailloux RJ, Treberg JR (2016) Protein S-glutathionlyation links energy metabolism to redox signaling in mitochondria. Redox Biol 8:110–118

    Article  CAS  PubMed  Google Scholar 

  • Meister A (1995) Mitochondrial changes associated with glutathione deficiency. Biochim Biophys Acta 1271:35–42

    Article  PubMed  Google Scholar 

  • Moraitis C, Curran BPG (2010) Differential effects of hydrogen peroxide and ascorbic acid on the aerobic thermosensitivity of yeast cells grown under aerobic and anoxic conditions. Yeast 27:103–114

    CAS  PubMed  Google Scholar 

  • Muthukumar K, Rajakumar S, Sarkar MN, Nachiappan V (2011) Glutathione peroxidase3 of Saccharomyces cerevisiae protects phospholipids during cadmium-induced oxidative stress. Antion Leeuw Int J G 99(4):761–771

    Article  CAS  Google Scholar 

  • Pollegioni L, Tonin F, Rosini E (2015) Lignin-degrading enzymes. FEBS J 282:1190–1213

    Article  CAS  PubMed  Google Scholar 

  • Perna V, Meyer AS, Holck J, Eltis LD, Eijsink VGH, Agger JW (2020) Laccase-catalyzed oxidation of lignin induces production of H2O2. ACS Sustainable Chen Eng 8:831–841

    Article  CAS  Google Scholar 

  • Ren A, Liu R, Miao ZG, Zhang X, Cao PF, Chen TX, Li CY, Shi L, Jiang AL, Zhao MW (2017) Hydrogen-rich water regulates effects of ROS balance on morphology, growth and secondary metabolism via glutathione peroxidase in Ganoderma lucidum. Environ Microbiol 19(2):566–583

    Article  CAS  PubMed  Google Scholar 

  • Ströher E, Millar AH (2012) The biological roles of glutaredoxins. Biochem J 446:333–348

    Article  PubMed  CAS  Google Scholar 

  • Schafer FQ, Buettner GR (2001) Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic Biol Med 30:1191–1212

    Article  CAS  PubMed  Google Scholar 

  • Sideri M, Georgiou CD (2000) Differentiation and hydrogen peroxide production in Sclerotium rolfsii are induced by the oxidizing growth factors, light and iron. Mycologia 92(6):1033–1042

    Article  CAS  Google Scholar 

  • 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 285:6118–6126

    Article  CAS  PubMed  Google Scholar 

  • Turrens JF (2003) Mitochondrial formation of reactive oxygen species. J Physiol 552:335–344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsuchida K, Aoyagi Y, Odani S, Mita T, Isemura M (1995) Isolation of a novel collagen-binding protein from the mushroom, Hypsizigus marmoreus, which inhibits the Lewis lung carcinoma cell adhesion to type IV collagen. J Biol Chem 270:1481–1484

    Article  CAS  PubMed  Google Scholar 

  • Ursini F, Maiorino M, Brigelius-Flohe R, Aumann KD, Roveri A, Schomburg D, Flohe L (1995) Diversity of glutathione peroxidases. Methods Enzymol 252:38–53

    Article  CAS  PubMed  Google Scholar 

  • Xiong CH, Xia YL, Zheng P, Wang CS (2013) Increasing oxidative stress tolerance and subculturing stability of Cordyceps militaris by overexpression of a glutathione peroxidase gene. Appl Microbiol Biotechnol 97:2009–2015

    Article  CAS  PubMed  Google Scholar 

  • Yang SL, Yu PL, Chung KR (2016) The glutathione peroxidase-mediated reactive oxygen species resistance, fungicide sensitivity and cell wall construction in the citrus fungal pathogen Alternaria alternata. Environ Microbiol 18(3):923–935

    Article  CAS  PubMed  Google Scholar 

  • Yang QY, Diao JW, Legrand NNG, Serwah BNA, Zhu M, Pang B, Zhang HY (2020) The protein expression profile and transcriptome characterization of Pichia caribbica induced by ascorbic acid under the oxidative stress. Biol Control 142:104164

  • Zhang BZ, Yan PS, Chen H, He J (2012) Optimization of production conditions for mushroom polysaccharides with high yield and antitumor activity. Carbohydr Polym 87:2569–2575

    Article  CAS  Google Scholar 

  • Zhang BZ, Inngjerdingen KT, Zou YF, Rise F, Michaelsen TE, Yan PS, Paulsen BS (2014a) Characterization and immunomodulating activities of exo-polysaccharides from submerged cultivation of Hypsizigus marmoreus. Food Chem 163:120–128

    Article  CAS  PubMed  Google Scholar 

  • Zhang JJ, Shi L, Chen H, Sun YQ, Zhao MW, Ren A, Chen MJ, Wang H, Feng ZY (2014b) An efficient Agrobacterium-mediated transformation method for the edible mushroom Hypsizygus marmoreus. Microbiol Res 169:741–748

    Article  CAS  PubMed  Google Scholar 

  • Zhang JJ, Chen H, Chen MJ, Wang H, Song XX, Feng ZY (2016) Construction and application of a gene silencing system using a dual promoter silencing vector in Hypsizygus marmoreus. J Basic Microbiol 56:1–9

    Article  CAS  Google Scholar 

  • Zhang JJ, Chen H, Xie MY, Chen MJ, Hao HB, Wang H, Feng ZY (2017a) Mechanism of glucose regulates the fruiting body formation in the beech culinary-medicinal mushroom, Hypsizygus marmoreus (Agaricomycetes). Int J Med Mushrooms 19(2):179–189

    Article  PubMed  Google Scholar 

  • Zheng H, Kim J, Liew M, Yan JK, Herrera O, Bok JW, Kelleher NL, Keller NP, Wang Y (2015) Redox metabolites signal polymicrobial biofilm development via the NapA oxidative stress cascade in Aspergillus. Curr Biol 25:29–37

    Article  CAS  PubMed  Google Scholar 

  • Zhang JJ, Hao HB, Chen MJ, Wang H, Feng ZY, Chen H (2017b) Hydrogen-rich water alleviates the toxicities of different stresses to mycelial growth in Hypsizygus marmoreus. AMB Express 7:107

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang JJ, Chen H, Chen MJ, Wang H, Wang Q, Song XX, Hao HB, Feng ZY (2018) Kojic acid-mediated damage responses induce mycelial regeneration in the basidiomycete Hypsizygus marmoreus. PLoS One 12(11):e0187351

    Article  CAS  Google Scholar 

  • Zámocký M, Hofbauer S, Schaffner I, Gasselhuber B, Nicolussi A, Soudi M, Pirker KF, Furtmüller PG, Obinger C (2015) Independent evolution of four heme peroxidase superfamilies. Arch Biochem Biophys 574:108–119

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zámocký M, Janeèek Š, Obinger C (2017) Fungal hybrid B heme peroxidases-unique fusions of a heme peroxidase domain with a carbohydrate-binding domain. Sci Rep 7:9393

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgments

We thank Jing Zhao for giving some helps in performing the experiments and thank the AJE company for providing the language editing help.

Code availability

The software in this manuscript was available.

Funding

This work was funded by the National Natural Science Foundation of China (Grant No. 31601802) and the earmarked fund of Shanghai Modern Edible Fungi-Industry Technology Research System (202009).

Author information

Authors and Affiliations

Authors

Contributions

Jinjing Zhang, Hui Chen, Mingjie Chen, and Zhiyong Feng conceived and designed research. Jinjing Zhang, Haibo Hao, and Xuelan Wu conducted experiments. Haibo Hao and Hui Chen contributed new reagents or analytical tools. Jinjing Zhang and Qian Wang analyzed data. Jinjing Zhang wrote the manuscript. All authors read and approved the manuscript.

Corresponding author

Correspondence to Hui Chen.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

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

Consent to participate

All authors declare that they consent to participate.

Consent for publication

All authors declare that they consent for publication.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

ESM 1

(PDF 210 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, J., Hao, H., Wu, X. et al. The functions of glutathione peroxidase in ROS homeostasis and fruiting body development in Hypsizygus marmoreus. Appl Microbiol Biotechnol 104, 10555–10570 (2020). https://doi.org/10.1007/s00253-020-10981-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-020-10981-6

Keywords

Navigation