Skip to main content
SpringerLink
Log in

Reactive Oxygen Species in the Botrytis – Host Interaction

  • Chapter
  • First Online:
Botrytis – the Fungus, the Pathogen and its Management in Agricultural Systems

Abstract

Reactive oxygen species (ROS) are unavoidable byproducts of several metabolic processes. Due to their high reactivity they can cause molecular damages such as protein oxidations or DNA mutations, but they also serve as important signalling molecules within cells. Intracellular ROS primarily originate in the mitochondria; however enzymatic ROS generating systems such as the membrane associated NADPH oxidase complex (Nox) contribute to their production. In particular, during host-pathogen interactions ROS are of key importance for plant defence but also for fungal attack. As an early response to pathogen infestation the plant releases high amounts of reactive oxygen species to counteract the pathogen, known as the oxidative burst. It was shown that Botrytis exploits this plant defence reaction and even contributes to this oxidative burst by forming its’ own ROS. Thus, the fungus needs a robust oxidative stress responsive (OSR) system to cope with ROS. In order to balance the intracellular redox state, effective antioxidant systems, including the thioredoxin and the glutathione system, are indispensable. Furthermore, catalases, superoxide dismutases and several peroxidases support ROS scavenging by enzymatic inactivation. Transcription factors such as the Botrytis activator protein (Bap1) and the response regulator Skn7 were shown to be involved in OSR. In this chapter we discuss the role of ROS in Botrytis – host interaction and both ROS generating and detoxifying systems and their importance for Botrytis pathogenicity.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Adrian M, Rajaei H, Jeandet P et al (1998) Resveratrol oxidation in Botrytis cinerea conidia. Phytopathology 88:472–476

    Article  CAS  PubMed  Google Scholar 

  • Afanas’ev IB (2007) Signaling functions of free radicals superoxide & nitric oxide under physiological & pathological conditions. Mol Biotechnol 37:2–4

    Article  PubMed  CAS  Google Scholar 

  • Aguirre J, Lambeth JD (2010) Nox enzymes from fungus to fly to fish and what they tell us about Nox function in mammals. Free Radic Biol Med 49:1342–1353

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Alepuz PM, Jovanovic A, Reiser V et al (2001) Stress-induced map kinase Hog1 is part of transcription activation complexes. Mol Cell 7:767–777

    Article  CAS  PubMed  Google Scholar 

  • Appenzeller-Herzog C, Riemer J, Zito E et al (2010) Disulphide production by Ero1 alpha-PDI relay is rapid and effectively regulated. EMBO J 29:3318–3329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arner ES, Holmgren A (2000) Physiological functions of thioredoxin and thioredoxin reductase. Eur J Biochem 267:6102–6109

    Article  CAS  PubMed  Google Scholar 

  • Babior BM, Lambeth JD, Nauseef W (2002) The neutrophil NADPH oxidase. Arch Biochem Biophys 397:342–344

    Article  CAS  PubMed  Google Scholar 

  • Balaban RS, Nemoto S, Finkel T (2005) Mitochondria, oxidants, and aging. Cell 120:483–495

    Article  CAS  PubMed  Google Scholar 

  • Bedard K, Krause KH (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87:245–313

    Article  CAS  PubMed  Google Scholar 

  • Brisson LF, Tenhaken R, Lamb C (1994) Function of oxidative cross-linking of cell wall structural proteins in plant disease resistance. Plant Cell 6:1703–1712

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Calvo IA, Garcia P, Ayte J et al (2012) The transcription factors Pap1 and Prr1 collaborate to activate antioxidant, but not drug tolerance, genes in response to H2O2. Nucleic Acids Res 40:4816–4824

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cano-Dominguez N, Alvarez-Delfin K, Hansberg W et al (2008) NADPH oxidases NOX-1 and NOX-2 require the regulatory subunit NOR-1 to control cell differentiation and growth in Neurospora crassa. Eukaryot Cell 7:1352–1361

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carmel-Harel O, Storz G (2000) Roles of the glutathione- and thioredoxin-dependent reduction systems in the Escherichia coli and Saccharomyces cerevisiae responses to oxidative stress. Annu Rev Microbiol 54:439–461

    Article  CAS  PubMed  Google Scholar 

  • Casso D, Beach D (1996) A mutation in a thioredoxin reductase homolog suppresses p53-induced growth inhibition in the fission yeast Schizosaccharomyces pombe. Mol Gen Genet 252:518–529

    CAS  PubMed  Google Scholar 

  • Chaves GM, da Silva WP (2012) Superoxide dismutases and glutaredoxins have a distinct role in the response of Candida albicans to oxidative stress generated by the chemical compounds menadione and diamide. Mem Inst Oswaldo Cruz 107:998–1005

    Article  CAS  PubMed  Google Scholar 

  • Chung WH, Kim KD, Cho YJ et al (2004) Differential expression and role of two dithiol glutaredoxins Grx1 and Grx2 in Schizosaccharomyces pombe. Biochem Biophys Res Commun 321:922–929

    Article  CAS  PubMed  Google Scholar 

  • Collinson EJ, Wheeler GL, Garrido EO et al (2002) The yeast glutaredoxins are active as glutathione peroxidases. J Biol Chem 277:16712–16717

    Article  CAS  PubMed  Google Scholar 

  • da Silva Dantas A, Patterson MJ, Smith DA et al (2010) Thioredoxin regulates multiple hydrogen peroxide-induced signaling pathways in Candida albicans. Mol Cell Biol 30:4550–4563

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Delaunay A, Isnard AD, Toledano MB (2000) H2O2 sensing through oxidation of the Yap1 transcription factor. EMBO J 19:5157–5166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dickman MB, Park YK, Oltersdorf T et al (2001) Abrogation of disease development in plants expressing animal antiapoptotic genes. Proc Natl Acad Sci U S A 98:6957–6962

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dixon KP, Xu JR, Smirnoff N et al (1999) Independent signaling pathways regulate cellular turgor during hyperosmotic stress and appressorium-mediated plant infection by Magnaporthe grisea. Plant Cell 11:2045–2058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Du C, Sarfati J, Latge JP et al (2006) The role of the sakA (Hog1) and tcsB (s1n1) genes in the oxidant adaptation of Aspergillus fumigatus. Med Mycol 44:211–218

    Article  CAS  PubMed  Google Scholar 

  • Egan MJ, Wang ZY, Jones MA et al (2007) Generation of reactive oxygen species by fungal NADPH oxidases is required for rice blast disease. Proc Natl Acad Sci U S A 104:11772–11777

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Elad Y (1992) The use of antioxidants (free-radical scavengers) to control grey mould (Botrytis cinerea) and white mould (Sclerotinia sclerotiorum) in various crops. Plant Pathol 41:417–426

    Article  CAS  Google Scholar 

  • Elad Y, Lapsker Z (2001) Involvement of reactive oxygen species and antioxidative processes in the disease caused by B. cinerea on bean leaves and in its biological control by means of Trichoderma harzianum T39. IOBC Bull 24(3):21–25

    Google Scholar 

  • Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gan ZR (1991) Yeast thioredoxin genes. J Biol Chem 266:1692–1696

    CAS  PubMed  Google Scholar 

  • Garrido EO, Grant CM (2002) Role of thioredoxins in the response of Saccharomyces cerevisiae to oxidative stress induced by hydroperoxides. Mol Microbiol 43:993–1003

    Article  CAS  PubMed  Google Scholar 

  • Giesbert S, Schürg T, Scheele S et al (2008) The NADPH oxidase Cpnox1 is required for full pathogenicity of the ergot fungus Claviceps purpurea. Mol Plant Pathol 9:317–327

    Article  CAS  PubMed  Google Scholar 

  • Giesbert S, Siegmund U, Schumacher J et al (2014) Functional analysis of BcBem1 and its interaction partners in Botrytis cinerea: impact on differentiation and virulence. PLoS One 9(5):e95172. doi:10.1371/journal.pone.0095172

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gil-ad NL, Bar-Nun N, Noy T et al (2000) Enzymes of Botrytis cinerea capable of breaking down hydrogen peroxide. FEMS Microbiol Lett 190:121–126

    Article  CAS  PubMed  Google Scholar 

  • Giorgio M, Trinei M, Migliaccio E et al (2007) Hydrogen peroxide: a metabolic by-product or a common mediator of ageing signals? Nat Rev Mol Cell Biol 8:722–728

    Article  CAS  PubMed  Google Scholar 

  • Gourgues M, Brunet-Simon A, Lebrun MH et al (2004) The tetraspanin BcPls1 is required for appressorium-mediated penetration of Botrytis cinerea into host plant leaves. Mol Microbiol 51:619–629

    Article  CAS  PubMed  Google Scholar 

  • Govrin EM, Levine A (2000) The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr Biol 10:751–757

    Article  CAS  PubMed  Google Scholar 

  • Grant CM, Collinson LP, Roe JH et al (1996) Yeast glutathione reductase is required for protection against oxidative stress and is a target gene for yAP-1 transcriptional regulation. Mol Microbiol 21:171–179

    Article  CAS  PubMed  Google Scholar 

  • Grissa I, Bidard F, Grognet P et al (2010) The Nox/Ferric reductase/Ferric reductase-like families of Eumycetes. Fungal Biol 114:766–777

    Article  CAS  PubMed  Google Scholar 

  • Gutierrez-Escobedo G, Orta-Zavalza E, Castano I et al (2013) Role of glutathione in the oxidative stress response in the fungal pathogen Candida glabrata. Curr Genet 59:91–106

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hasan R, Leroy C, Isnard AD et al (2002) The control of the yeast H2O2 response by the Msn2/4 transcription factors. Mol Microbiol 45:233–241

    Article  CAS  PubMed  Google Scholar 

  • Heller J, Tudzynski P (2011) Reactive oxygen species in phytopathogenic fungi: signaling, development, and disease. Annu Rev Phytopathol 49:369–390

    Article  CAS  PubMed  Google Scholar 

  • Heller J, Meyer AJ, Tudzynski P (2012a) Redox-sensitive GFP2: use of the genetically encoded biosensor of the redox status in the filamentous fungus Botrytis cinerea. Mol Plant Pathol 13:935–947

    Article  CAS  PubMed  Google Scholar 

  • Heller J, Ruhnke N, Espino JJ et al (2012b) The mitogen-activated protein kinase BcSak1 of Botrytis cinerea is required for pathogenic development and has broad regulatory functions beyond stress response. Mol Plant-Microbe Interact 25:802–816

    Article  CAS  PubMed  Google Scholar 

  • Herrmann A, Tillmann B, Schürmann J et al (2014) Small GTPase-associated signaling by the guanine nucleotide exchange factors CpDock180 and CpCdc24, the GTPase effector CpSte20 and the scaffold CpBem1 in Claviceps purpurea. Eukaryot Cell 13(4):470–482

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Holmgren A (1989) Thioredoxin and glutaredoxin systems. J Biol Chem 264:13963–13966

    CAS  PubMed  Google Scholar 

  • Izawa S, Maeda K, Sugiyama K et al (1999) Thioredoxin deficiency causes the constitutive activation of Yap1, an AP-1-like transcription factor in Saccharomyces cerevisiae. J Biol Chem 274:28459–28465

    Article  CAS  PubMed  Google Scholar 

  • Jamieson DJ (1998) Oxidative stress responses of the yeast Saccharomyces cerevisiae. Yeast 14:1511–1527

    Article  CAS  PubMed  Google Scholar 

  • Kim JH, Kim DH (2006) Cloning and characterization of a thioredoxin gene, CpTrx1, from the chestnut blight fungus Cryphonectria parasitica. J Microbiol 44:556–561

    CAS  PubMed  Google Scholar 

  • Kim H, Chen C, Kabbage M et al (2011) Identification and characterization of Sclerotinia sclerotiorum NADPH oxidases. Appl Environ Microbiol 77:7721–7729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klotz LO (2002) Oxidant-induced signaling: effects of peroxynitrite and singlet oxygen. Biol Chem 383:443–456

    Article  CAS  PubMed  Google Scholar 

  • Kuzniak E, Sklodowska M (1999) The effect of Botrytis cinerea infection on ascorbate-glutathione cycle in tomato leaves. Plant Sci 148:69–76

    Article  CAS  Google Scholar 

  • Lacaze I, Lalucque H, Silar P et al (2014) Identification of NoxD/Pro41 as the homologue of the p22phox NADPH oxidase subunit in fungi. Mol Microbiol. doi:10.1111/mmi.12876

    PubMed  Google Scholar 

  • Lambeth JD (2004) NOX enzymes and the biology of reactive oxygen. Nat Rev Immunol 4:181–189

    Article  CAS  PubMed  Google Scholar 

  • Lambou K, Malagnac F, Barbisan C et al (2008) The crucial role of the Pls1 tetraspanin during ascospore germination in Podospora anserina provides an example of the convergent evolution of morphogenetic processes in fungal plant pathogens and saprobes. Eukaryot Cell 7:1809–1818

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lara-Ortiz T, Riveros-Rosas H, Aguirre J (2003) Reactive oxygen species generated by microbial NADPH oxidase NoxA regulate sexual development in Aspergillus nidulans. Mol Microbiol 50:1241–1255

    Article  CAS  PubMed  Google Scholar 

  • Laurindo FR, Pescatore LA, Fernandes Dde C (2012) Protein disulfide isomerase in redox cell signaling and homeostasis. Free Radic Biol Med 52:1954–1969

    Article  CAS  PubMed  Google Scholar 

  • Laurindo FR, Araujo TL, Abrahao TB (2014) Nox NADPH oxidases and the endoplasmic reticulum. Antioxid Redox Signal. doi:10.1089/ars.2013.5605

    PubMed  PubMed Central  Google Scholar 

  • Lee J, Dawes IW, Roe JH (1997) Isolation, expression, and regulation of the pgr1(+) gene encoding glutathione reductase absolutely required for the growth of Schizosaccharomyces pombe. J Biol Chem 272:23042–23049

    Article  CAS  PubMed  Google Scholar 

  • Levine A, Tenhaken R, Dixon R et al (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583–593

    Article  CAS  PubMed  Google Scholar 

  • Liu S, Oeljeklaus S, Gerhardt B et al (1998) Purification and characterization of glucose oxidase of Botrytis cinerea. Physiol Mol Plant Pathol 53:123–132

    Article  CAS  Google Scholar 

  • Liu W, Leroux P, Fillinger S (2008) The HOG1-like MAP kinase Sak1 of Botrytis cinerea is negatively regulated by the upstream histidine kinase Bos1 and is not involved in dicarboximide- and phenylpyrrole-resistance. Fungal Genet Biol 45:1062–1074

    Article  CAS  PubMed  Google Scholar 

  • Loewus FA (1999) Biosynthesis and metabolism of ascorbic acid in plants and of analogs of ascorbic acid in fungi. Phytochemistry 52:193–210

    Article  CAS  Google Scholar 

  • Malagnac F, Lalucque H, Lepere G et al (2004) Two NADPH oxidase isoforms are required for sexual reproduction and ascospore germination in the filamentous fungus Podospora anserina. Fungal Genet Biol 41:982–997

    Article  CAS  PubMed  Google Scholar 

  • Malagnac F, Klapholz B, Silar P (2007) PaTrx1 and PaTrx3, two cytosolic thioredoxins of the filamentous ascomycete Podospora anserina involved in sexual development and cell degeneration. Eukaryot Cell 6:2323–2331

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martinez AT, Speranza M, Ruiz-Duenas FJ et al (2005) Biodegradation of lignocellulosics: microbial, chemical, and enzymatic aspects of the fungal attack of lignin. Int Microbiol 8:195–204

    CAS  PubMed  Google Scholar 

  • Martinez-Pastor MT, Marchler G, Schuller C et al (1996) The Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress-response element (STRE). EMBO J 15:2227–2235

    CAS  PubMed  PubMed Central  Google Scholar 

  • Matoba T, Shimokawa H, Nakashima M et al (2000) Hydrogen peroxide is an endothelium-derived hyperpolarizing factor in mice. J Clin Invest 106:1521–1530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Meyer AJ, Brach T, Marty L et al (2007) Redox-sensitive GFP in Arabidopsis thaliana is a quantitative biosensor for the redox potential of the cellular glutathione redox buffer. Plant J 52:973–986

    Article  CAS  PubMed  Google Scholar 

  • Minz Dub A, Kokkelink L, Tudzynski B et al (2013) Involvement of Botrytis cinerea small GTPases BcRAS1 and BcRAC in differentiation, virulence, and the cell cycle. Eukaryot Cell 12:1609–1618

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Moriwaki A, Kubo E, Arase S et al (2006) Disruption of SRM1, a mitogen-activated protein kinase gene, affects sensitivity to osmotic and ultraviolet stressors in the phytopathogenic fungus Bipolaris oryzae. FEMS Microbiol Lett 257:253–261

    Article  CAS  PubMed  Google Scholar 

  • Muckenschnabel I, Goodman BA, Williamson B et al (2002) Infection of leaves of Arabidopsis thaliana by Botrytis cinerea: changes in ascorbic acid, free radicals and lipid peroxidation products. J Exp Bot 53:207–214

    Article  CAS  PubMed  Google Scholar 

  • Mulford KE, Fassler JS (2011) Association of the Skn7 and Yap1 transcription factors in the Saccharomyces cerevisiae oxidative stress response. Eukaryot Cell 10:761–769

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muller EG (1996) A glutathione reductase mutant of yeast accumulates high levels of oxidized glutathione and requires thioredoxin for growth. Mol Biol Cell 7:1805–1813

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mustacich D, Powis G (2000) Thioredoxin reductase. Biochem J 346(Pt 1):1–8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279

    Article  CAS  PubMed  Google Scholar 

  • Oliveira MA, Discola KF, Alves SV et al (2010) Insights into the specificity of thioredoxin reductase-thioredoxin interactions. A structural and functional investigation of the yeast thioredoxin system. Biochemistry 49:3317–3326

    Article  CAS  PubMed  Google Scholar 

  • Onai K, Nakashima H (1997) Mutation of the cys-9 gene, which encodes thioredoxin reductase, affects the circadian conidiation rhythm in Neurospora crassa. Genetics 146:101–110

    CAS  PubMed  PubMed Central  Google Scholar 

  • Orozco-Cardenas ML, Narvaez-Vasquez J, Ryan CA (2001) Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate. Plant Cell 13:179–191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pujol-Carrion N, Belli G, Herrero E et al (2006) Glutaredoxins Grx3 and Grx4 regulate nuclear localisation of Aft1 and the oxidative stress response in Saccharomyces cerevisiae. J Cell Sci 119:4554–4564

    Article  CAS  PubMed  Google Scholar 

  • Rinnerthaler M, Buttner S, Laun P et al (2012) Yno1p/Aim14p, a NADPH-oxidase ortholog, controls extramitochondrial reactive oxygen species generation, apoptosis, and actin cable formation in yeast. Proc Natl Acad Sci U S A 109:8658–8663

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roca MG, Weichert M, Siegmund U et al (2012) Germling fusion via conidial anastomosis tubes in the grey mould Botrytis cinerea requires NADPH oxidase activity. Fungal Biol 116:379–387

    Article  CAS  PubMed  Google Scholar 

  • Rolke Y, Liu SJ, Quidde T et al (2004) Functional analysis of H2O2-generating systems in Botrytis cinerea: the major Cu-Zn-superoxide dismutase (BCSOD1) contributes to virulence on French bean, whereas a glucose oxidase (BCGOD1) is dispensable. Mol Plant Pathol 5:17–27

    Article  CAS  PubMed  Google Scholar 

  • Sato I, Shimizu M, Hoshino T et al (2009) The glutathione system of Aspergillus nidulans involves a fungus-specific glutathione S-transferase. J Biol Chem 284:8042–8053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sato I, Shimatani K, Fujita K et al (2011) Glutathione reductase/glutathione is responsible for cytotoxic elemental sulfur tolerance via polysulfide shuttle in fungi. J Biol Chem 286:20283–20291

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schouten A, Tenberge KB, Vermeer J et al (2002) Functional analysis of an extracellular catalase of Botrytis cinerea. Mol Plant Pathol 3:227–238

    Article  CAS  PubMed  Google Scholar 

  • Schumacher J, Simon A, Cohrs KC et al (2014) The transcription factor BcLTF1 regulates virulence and light responses in the necrotrophic plant pathogen Botrytis cinerea. PLoS Genet 10:e1004040

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schürmann J, Buttermann D, Herrmann A et al (2013) Molecular characterization of the NADPH oxidase complex in the ergot fungus Claviceps purpurea: CpNox2 and CpPls1 are important for a balanced host-pathogen interaction. Mol Plant-Microbe Interact 26:1151–1164

    Article  PubMed  CAS  Google Scholar 

  • Scott B, Eaton CJ (2008) Role of reactive oxygen species in fungal cellular differentiations. Curr Opin Microbiol 11:488–493

    Article  CAS  PubMed  Google Scholar 

  • Segmüller N, Ellendorf U, Tudzynski B et al (2007) BcSAK1, a stress-activated mitogen-activated protein kinase, is involved in vegetative differentiation and pathogenicity in Botrytis cinerea. Eukaryot Cell 6:211–221

    Article  PubMed  CAS  Google Scholar 

  • Segmüller N, Kokkelink L, Giesbert S et al (2008) NADPH oxidases are involved in differentiation and pathogenicity in Botrytis cinerea. Mol Plant-Microbe Interact 21:808–819

    Article  PubMed  CAS  Google Scholar 

  • Severin FF, Hyman AA (2002) Pheromone induces programmed cell death in S. cerevisiae. Curr Biol 12:R233–R235

    Article  CAS  PubMed  Google Scholar 

  • Sevier CS, Kaiser CA (2008) Ero1 and redox homeostasis in the endoplasmic reticulum. Biochim Biophys Acta 1783:549–556

    Article  CAS  PubMed  Google Scholar 

  • Siegmund U, Heller J, Van Kan JAL et al (2013) The NADPH Oxidase Complexes in Botrytis cinerea: evidence for a close association with the ER and the tetraspanin Pls1. PLoS One 8:e55879

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Siegmund U, Marschall R, Tudzynski P (2014) BcNoxD, a putative ER protein, is a new component of the NADPH oxidase complex in Botrytis cinerea. Mol Microbiol. doi:10.1111/mmi.12869

    Google Scholar 

  • Simon UK, Polanschutz LM, Koffler BE et al (2013) High resolution imaging of temporal and spatial changes of subcellular ascorbate, glutathione and H2O2 distribution during Botrytis cinerea infection in Arabidopsis. PLoS One 8:e65811

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Starkov AA (2008) The role of mitochondria in reactive oxygen species metabolism and signaling. Ann N Y Acad Sci 1147:37–52

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sugiura Y, Araki K, Iemura S et al (2010) Novel thioredoxin-related transmembrane protein TMX4 has reductase activity. J Biol Chem 285:7135–7142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takemoto D, Tanaka A, Scott B (2006) A p67Phox-like regulator is recruited to control hyphal branching in a fungal-grass mutualistic symbiosis. Plant Cell 18:2807–2821

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takemoto D, Tanaka A, Scott B (2007) NADPH oxidases in fungi: diverse roles of reactive oxygen species in fungal cellular differentiation. Fungal Genet Biol 44:1065–1076

    Article  CAS  PubMed  Google Scholar 

  • Takemoto D, Kamakura S, Saikia S et al (2011) Polarity proteins Bem1 and Cdc24 are components of the filamentous fungal NADPH oxidase complex. Proc Natl Acad Sci U S A 108:2861–2866

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tan SX, Greetham D, Raeth S et al (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 

  • Temme N, Tudzynski P (2009) Does Botrytis cinerea ignore H2O2-induced oxidative stress during infection? Characterization of Botrytis activator protein 1. Mol Plant Microbe Interact 22:987–998

    Article  CAS  PubMed  Google Scholar 

  • Tenberge KB (2004) Morphology and cellular organization in Botrytis interaction with plants. In: Elad Y, Williamson P, Tudzinski P, Delen N (eds) Botrytis: biology, pathology and control. Kluwer Academic, Dordrecht, pp 67–84

    Google Scholar 

  • Thon M, Al-Abdallah Q, Hortschansky P et al (2007) The thioredoxin system of the filamentous fungus Aspergillus nidulans: impact on development and oxidative stress response. J Biol Chem 282:27259–27269

    Article  PubMed  Google Scholar 

  • Toledano MB, Delaunay-Moisan A, Outten CE et al (2013) Functions and cellular compartmentation of the thioredoxin and glutathione pathways in yeast. Antioxid Redox Signal 18:1699–1711

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Torres MA, Dangl JL, Jones JD (2002) Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc Natl Acad Sci U S A 99:517–522

    Article  CAS  PubMed  Google Scholar 

  • Tudzynski P, Heller J, Siegmund U (2012) Reactive oxygen species generation in fungal development and pathogenesis. Curr Opin Microbiol 15:653–659

    Article  CAS  PubMed  Google Scholar 

  • Van Baarlen P, Woltering EJ, Staats M et al (2007) Histochemical and genetic analysis of host and non-host interactions of Arabidopsis with three Botrytis species: an important role for cell death control. Mol Plant Pathol 8:41–54

    Article  Google Scholar 

  • Van der Vlugt-Bergmans CJB, Wagemakers CAM, Dees DCT et al (1997) Catalase A from Botrytis cinerea is not expressed during infection on tomato leaves. Physiol Mol Plant Pathol 50:1–15

    Article  Google Scholar 

  • Viefhues A, Heller J, Temme N (2014) Redox systems in Botrytis cinerea: impact on development and virulence. Mol Plant Microbe Interact 27:858–874

    Article  CAS  PubMed  Google Scholar 

  • Viefhues A, Schlathoelter I, Simon A, et al (2015) Unravelling the function of the response regulator BcSkn7 in the stress signaling network of Botrytis cinerea. Eukaryot Cell pii: EC.00043-15. [Epub ahead of print]

    Google Scholar 

  • von Tiedemann A (1997) Evidence for a primary role of active oxygen species in induction of host cell death during infection of bean leaves with Botrytis cinerea. Physiol Mol Plant Pathol 50:151–166

    Article  CAS  Google Scholar 

  • Werner E, Werb Z (2002) Integrins engage mitochondrial function for signal transduction by a mechanism dependent on Rho GTPases. J Cell Biol 158:357–368

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wojtaszek P (1997) Oxidative burst: an early plant response to pathogen infection. Biochem J 322(Pt 3):681–692

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang SL, Chung KR (2012) The NADPH oxidase-mediated production of hydrogen peroxide (H2O2) and resistance to oxidative stress in the necrotrophic pathogen Alternaria alternata of citrus. Mol Plant Pathol 13:900–914

    Article  CAS  PubMed  Google Scholar 

  • Yang Q, Yin D, Yin Y et al (2014) The response regulator BcSkn7 is required for vegetative differentiation and adaptation to oxidative and osmotic stresses in Botrytis cinerea. Mol Plant Pathol. doi:10.1111/mpp.12181

    Google Scholar 

  • Yoshida T, Oka S, Masutani H et al (2003) The role of thioredoxin in the aging process: involvement of oxidative stress. Antioxid Redox Signal 5:563–570

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Lamm R, Pillonel C et al (2002) Osmoregulation and fungicide resistance: the Neurospora crassa os-2 gene encodes a HOG1 mitogen-activated protein kinase homologue. Appl Environ Microbiol 68:532–538

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang DX, Borbouse L, Gebremedhin D et al (2012) H2O2-induced dilation in human coronary arterioles: role of protein kinase G dimerization and large-conductance Ca2+-activated K+ channel activation. Circ Res 110:471–480

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Paul Tudzynski, Marty Dickman and Julia Schumacher for critical reading and/or discussion, Bettina Richter for excellent technical assistance and the DFG (Tu 50/19) and the GRK (Graduate Research School) 1409 for funding.

Author information

Authors and Affiliations

  1. Institut fuer Biologie und Biotechnologie der Pflanzen, Westfaelische Wilhelms, Universitaet Muenster, Schlossplatz 8, 48143, Muenster, Germany

    Ulrike Siegmund & Anne Viefhues

Authors
  1. Ulrike Siegmund
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anne Viefhues
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ulrike Siegmund .

Editor information

Editors and Affiliations

  1. Centre de Versailles-Grignon, INRA, Thiverval-Grignon, France

    Sabine Fillinger

  2. Dept. Plant Path. and Weed Res., ARO, Bet Dagan, Israel

    Yigal Elad

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Siegmund, U., Viefhues, A. (2016). Reactive Oxygen Species in the Botrytis – Host Interaction. In: Fillinger, S., Elad, Y. (eds) Botrytis – the Fungus, the Pathogen and its Management in Agricultural Systems. Springer, Cham. https://doi.org/10.1007/978-3-319-23371-0_14

Download citation

Publish with us

Policies and ethics

Search

Navigation