Skip to main content
Log in

Loss of Catalase-1 (Cat-1) results in decreased conidial viability enhanced by exposure to light in Neurospora crassa

  • Original Article
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

Light is one of the most important factors inducing morphogenesis in Neurospora crassa. The reception of light triggers the generation of reactive oxygen species (ROS) including hydrogen peroxide (H2O2). Catalase-1 (Cat-1) is one of three catalases known to detoxify H2O2 into water and oxygen. We reported that the photomorphogenetic characteristics of mutants in nucleoside diphosphate kinase-1 (NDK-1), a light signal transducer, are severely affected, and NDK-1 interacted with Cat-1 in a yeast two-hybrid assay. To disclose the function of Cat-1, we created a Cat-1 loss-of-function mutant (cat-1 RIP) by the repeat induced point-mutation (RIPing) method. No Cat-1 activity was detected in the mutant strain. Forty guanines were replaced with adenines in the cat-1 gene of cat-1 RIP, which caused 30 amino acid substitutions. The mutant strain grew normally, but its conidia and mycelia were more sensitive to H2O2 than those of the wild type. The lack of Cat-1 activity also caused a significant reduction in the conidial germination rate. Furthermore, light enhanced this reduction in cat-1 RIP more than that in the wild type. Introduction of cat-1 into the mutant reversed all of these defective phenotypes. These results indicate that Cat-1 plays an important role in supporting the survival of conidia under oxidative and light-induced stress.

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

Similar content being viewed by others

References

  • Bravo J, Fita I, Gouet P, Jouve HM, Melik-Adamyan W, Murshudov GN (1997) Structure of catalase. In: Scandalios JG (ed) Oxidative stress and the molecular biology of antioxidant defenses. Cold Spring Harbor, New York, pp 407–445

    Google Scholar 

  • Cambareri EB, Jensen BC, Schabtach E, Selker EU (1989) Repeat induced G-C to A-T mutations in Neurospora. Science 244:1571–1575

    Article  PubMed  CAS  Google Scholar 

  • Church GM, Kieffer-Higgins S (1998) Multiplex DNA sequencing. Science 240:185–188

    Article  Google Scholar 

  • Davis RH, De Serres FJ (1970) Genetic and microbiological research techniques for Neurospora crassa. Methods Enzymol 71:79–143

    Article  Google Scholar 

  • Degli-Innocenti F, Russo VE (1984) Isolation of new white collar mutants of Neurospora crassa and studies on their behaviour in the blue-light-induced formation of protoperithecia. J Bacteriol 159:757–761

    PubMed  CAS  Google Scholar 

  • Diaz A, Rangel P, Montes de Oca Y, Lledias F, Hansberg W (2001) Molecular and kinetic study of catalase-1, a durable large catalase of Neurospora crassa. Free Radic Biol Med 31:1323–1333

    Article  PubMed  CAS  Google Scholar 

  • Diaz A, Horjales E, Rudino-pinera E, Arreola R, Hansberg W (2004) Unusual Cys-Tyr covalent bond in a large catalase. J Mol Biol 342:971–985

    Article  PubMed  CAS  Google Scholar 

  • Dolamns DEJGJ, Fukumura D, Jain RK (2003) Photodynamic therapy for cancer. Nat Rev 1:380–387

    Google Scholar 

  • Farr SB, Kogoma T (1991) Oxidative stress responses in Escherichia coli and Salmonella typhimurium. Microbiol Rev 55:561–585

    PubMed  CAS  Google Scholar 

  • Feldman JF (1982) Genetic approaches to circadian clocks. Annu Rev Plant Physiol 33:583–608

    Article  CAS  Google Scholar 

  • Fukamatsu Y, Yabe N, Hasunuma K (2003) Arabidopsis NDK1 is a component of ROS signaling by interacting with three catalases. Plant Cell Physiol 44:982–989

    Article  PubMed  CAS  Google Scholar 

  • Harding RW, Melles S (1984) Genetic analysis of the phototropism of Neurospora crassa perithecial beaks using white collar and albino mutants. Plant Physiol 72:996–1000

    Google Scholar 

  • Harding RW, Turner RV (1981) Photoregulation of the carotenoid biosynthetic pathways in albino and white collar mutants of Neurospora crassa. Plant Physiol 68:745–749

    PubMed  CAS  Google Scholar 

  • Iigusa H, Yoshida Y, Hasunuma K (2005) Oxygen and hydrogen peroxide enhance light-induced carotenoid synthesis in Neurospora crassa. FEBS Lett 579:4012–4016

    Article  PubMed  CAS  Google Scholar 

  • Jacobson A, Peltz SW (1996) Interrelationships of the pathways of mRNA decay and translation in eukaryotic cells. Annu Rev Biochem 65:693–739

    Article  PubMed  CAS  Google Scholar 

  • Kendrick RE, Kronenberg GHM (1994) Photomorphogenesis in plants. Kluwer, Dordrecht, Netherlands

    Google Scholar 

  • Lee B, Yoshida Y, Hasunuma K (2006) Photomorphogenetic characteristics are severely affected in nucleoside diphosphate kinase-1 (ndk-1)-disrupted mutants in Neurospora crassa. Mol Gen Genomics 275:9–17

    Article  CAS  Google Scholar 

  • Lledias F, Rangel P, Hansberg W (1998) Oxidation of catalase by singlet oxygen. J Biol Chem 273:10630–10637

    Article  PubMed  CAS  Google Scholar 

  • Lledias F, Rangel P, Hansberg W (1999) Singlet oxygen is part of a hyperoxidant state generated during spore germination. Free Radic Biol Med 26:1396–1404

    Article  PubMed  CAS  Google Scholar 

  • Loewen PC (1997) Bacterial catalases. In: Scandalios JG (ed) Oxidative stress and the molecular biology of antioxidant defenses. Cold Spring Harbor, New York, pp 273–308

    Google Scholar 

  • Massey V (2000) The chemical and biological versatility of riboflavin. Biochem Soc Trans 28:283–296

    PubMed  CAS  Google Scholar 

  • McCluskey K (2003) The Fungal Genetics Stock Center: from molds to molecules. Adv Appl Microbiol 52:245–262

    PubMed  Google Scholar 

  • Michan S, Lledias F, Baldwin JD, Natvig DO, Hansberg W (2002) Regulation and oxidation of two large monofunctional catalases. Free Radic Biol Med 33:521–532

    Article  PubMed  CAS  Google Scholar 

  • Michan S, Lledias W, Hansberg W (2003) Asexual development is increased in Neurospora crassa CAT-3 null mutant strains. Eukaryot Cell 2:798–808

    Article  PubMed  CAS  Google Scholar 

  • Mullaney EJ, Hamer JE, Roberti KA, Yelton MM, Timberlake WE (1985) Primary structure of the trpC gene from Aspergillus nidulans. Mol Gen Genet 199:37–45

    Article  PubMed  CAS  Google Scholar 

  • Navarro RE, Stringer MA, Hansberg W, Timberlade WE, Aguirre J (1996) catA, a new Aspergilus nidulans gene encoding a developmentally regulated catalase. Curr Genet 29:352–359

    PubMed  CAS  Google Scholar 

  • Noventa-Jordao MA, Couto RM, Goldman MHS, Aguirre J, Lyer S, Caplan A, Terenzi HF, Goldman GH (1999) Catalase activity is necessary for heat-shock recovery in Aspergillus nidulans germlings. Micorbiology 145:3229–3234

    CAS  Google Scholar 

  • Oda K, Hasunuma K (1997) Genetic analysis of signal transduction through light-induced protein phosphorylation in Neurospora crassa. Mol Gen Genet 256:593–601

    Article  PubMed  CAS  Google Scholar 

  • Ogura Y, Yoshida Y, Yabe N, Hasunuma K (2001) A point mutation in nucleoside diphosphate kinase results in a deficient light response for perithecial polarity in Neurospora crassa. J Biol Chem 276:21228–21234

    Article  PubMed  CAS  Google Scholar 

  • Omata Y, Lewis JB, Rotenberg S, Lockwood PE, Messer RL, Noda M, Hsu SD, Sano H, Wataha JC (2006) Intra- and extracellular reactive oxygen species generated by blue light. J Biomed Mater Res A 77(3):470–477

    PubMed  CAS  Google Scholar 

  • Parvathi C, Donald ON (1989) Evidence for three differentially regulated catalase genes in Neurospora crassa: effects of oxidative stress, heat shock, and development. J Bacteriol 171:2646–2652

    Google Scholar 

  • Peraza L, Hansberg W (2002) Neurospora crassa catalases, singlet oxygen and cell differentiation. Biol Chem 383:569–575

    Article  PubMed  CAS  Google Scholar 

  • Sargent ML, Briggs WR (1967) The effects of blue light on a circadian rhythm of conidiation in Neurospora. Plant Physiol 42:1504–1510

    Article  PubMed  Google Scholar 

  • Schmit JC, Brody S (1976) Biochemical genetics of Neurospora crassa conidial germination. Bacteriol Rev 40:1–41

    PubMed  CAS  Google Scholar 

  • Schriner SE, Linford NJ, Martin GM, Treuting P, Ogburn CE, Emond M, Coskun PE, Ladiges W, Wolf N, Remmen HV, Wallace DC, Rabinovitch PS (2005) Extension of murine life span by overexpression of catalase targeted to mitochondria. Science 308:1909–1911

    Article  PubMed  CAS  Google Scholar 

  • Selker EU, Garrett PW (1988) DNA sequence duplications trigger gene inactivation in Neurospora crassa. Proc Natl Acad Sci USA 85:6870–6874

    Article  PubMed  CAS  Google Scholar 

  • Sokolovsky V, Kaldenhoff R, Ricci M, Russo VEA (1990) Fast and reliable mini-prep RNA extraction from Neurospora crassa. Fungal Genet Newslett 67:41–43

    Google Scholar 

  • Staben C, Jensen B, Singer M, Pollock J, Schechtman M, Kinsey J, Selker E (1989) Use of a bacterial hygromycin B resistance gene as a dominant selectable marker in Neurospora crassa transformation. Fungal Genet Newslett 36:79–81

    Google Scholar 

  • Vollmer SJ, Yanofsky C (1986) Efficient cloning of genes of Neurospora crassa. Proc Natl Acad Sci USA 83:4869–4873

    Article  PubMed  CAS  Google Scholar 

  • Yoshida Y, Hasunuma K (2004) Reactive oxygen species affect photo-morphogenesis in Neurospora crassa. J Biol Chem 279:6986–6993

    Article  PubMed  CAS  Google Scholar 

  • Yoshida Y, Ogura Y, Hasunuma K (2006) Interaction of nucleoside diphosphate kinase and catalases for stress and light responses in Neurospora crassa. FEBS Lett 580(13):3282–3286

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to Winslow R. Briggs for critical discussions. This work is supported by a grant-in-aid from the Japan Society for the Promotion of Science, the Kihara Memorial Yokohama Foundation for the Advancement of Life Science, the Mishima Kaiun Memorial Foundation, and the Yamada Science Foundation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kohji Hasunuma.

Additional information

Communicated by J. Perez-Martin.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, N., Yoshida, Y. & Hasunuma, K. Loss of Catalase-1 (Cat-1) results in decreased conidial viability enhanced by exposure to light in Neurospora crassa . Mol Genet Genomics 277, 13–22 (2007). https://doi.org/10.1007/s00438-006-0170-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-006-0170-4

Keywords

Navigation