Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Exploitation of Reactive Oxygen Species by Fungi: Roles in Host-Fungus Interaction and Fungal Development

  • Kim, Hyo Jin (Fermentation Research Center, Korea Food Research Institute)
  • Received : 2014.07.25
  • Accepted : 2014.08.11
  • Published : 2014.11.28
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Abstract

In the past, reactive oxygen species (ROS) have been considered a harmful byproduct of aerobic metabolism. However, accumulating evidence implicates redox homeostasis, which maintains appropriate ROS levels, in cell proliferation and differentiation in plants and animals. Similarly, ROS generation and signaling are instrumental in fungal development and host-fungus interaction. In fungi, NADPH oxidase, a homolog of human $gp91^{phox}$, generates superoxide and is the main source of ROS. The mechanism of activation and signaling by NADPH oxidases in fungi appears to be largely comparable to those in plants and animals. Recent studies have shown that the fungal NADPH oxidase homologs NoxA (Nox1), NoxB (Nox2), and NoxC (Nox3) have distinct functions. In particular, these studies have consistently demonstrated the impact of NoxA on the development of fungal multicellular structures. Both NoxA and NoxB (but not NoxC) are involved in host-fungus interactions, with the function of NoxA being more critical than that of NoxB.

Keywords

References

  1. Aguirre J, Rios-Momberg M, Hewitt D, Hansberg W. 2005. Reactive oxygen species and development in microbial eukaryotes. Trends Microbiol. 13: 111-118. https://doi.org/10.1016/j.tim.2005.01.007
  2. Ahmed KA, Sawa T, Ihara H, Kasamatsu S, Yoshitake J, Rahaman MM, et al. 2012. Regulation by mitochondrial superoxide and NADPH oxidase of cellular formation of nitrated cyclic GMP: potential implications for ROS signalling. Biochem. J. 441: 719-730. https://doi.org/10.1042/BJ20111130
  3. Akaike T, Nishida M, Fujii S. 2013. Regulation of redox signalling by an electrophilic cyclic nucleotide. J. Biochem. 153: 131-138. https://doi.org/10.1093/jb/mvs145
  4. Apel K, Hirt H. 2004. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55: 373-399. https://doi.org/10.1146/annurev.arplant.55.031903.141701
  5. Bindschedler LV, Dewdney J, Blee KA, Stone JM, Asai T, Plotnikov J, et al. 2006. Peroxidase-dependent apoplastic oxidative burst in Arabidopsis required for pathogen resistance. Plant J. 47: 851-863. https://doi.org/10.1111/j.1365-313X.2006.02837.x
  6. Bolwell GP, Bindschedler LV, Blee KA, Butt VS, Davies DR, Gardner SL, et al. 2002. The apoplastic oxidative burst in response to biotic stress in plants: a three-component system. J. Exp. Bot. 53: 1367-1376. https://doi.org/10.1093/jexbot/53.372.1367
  7. Bradley DJ, Kjellbom P, Lamb CJ. 1992. Elicitor- and woundinduced oxidative cross-linking of a proline-rich plant cell wall protein: a novel, rapid defense response. Cell 70: 21-30. https://doi.org/10.1016/0092-8674(92)90530-P
  8. Cano-Dominguez N, Alvarez-Delfin K, Hansberg W, Aguirre J. 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.
  9. Cheng YJ, Kim MD, Deng XP, Kwak SS, Chen W. 2013. Enhanced salt stress tolerance in transgenic potato plants expressing IbMYB1, a sweet potato transcription factor. J. Microbiol. Biotechnol. 23: 1737-1746. https://doi.org/10.4014/jmb.1307.07024
  10. Choi H, Lee DG. 2013. The influence of the N-terminal region of antimicrobial peptide pleurocidin on fungal apoptosis. J. Microbiol. Biotechnol. 23: 1386-1394. https://doi.org/10.4014/jmb.1306.06012
  11. Decoursey TE, Ligeti E. 2005. Regulation and termination of NADPH oxidase activity. Cell Mol. Life Sci. 62: 2173-2193. https://doi.org/10.1007/s00018-005-5177-1
  12. Delaunay A, Isnard AD, Toledano MB. 2000. $H_{2}O_{2}$ sensing through oxidation of the Yap1 transcription factor. EMBO J. 19: 5157-5166. https://doi.org/10.1093/emboj/19.19.5157
  13. Dunand C, Crevecoeur M, Penel C. 2007. Distribution of superoxide and hydrogen peroxide in Arabidopsis root and their influence on root development: possible interaction with peroxidases. New Phytol. 174: 332-341. https://doi.org/10.1111/j.1469-8137.2007.01995.x
  14. Eaton CJ, Jourdain I, Foster SJ, Hyams JS, Scott B. 2008. Functional analysis of a fungal endophyte stress-activated MAP kinase. Curr. Genet. 53: 163-174. https://doi.org/10.1007/s00294-007-0174-6
  15. Egan MJ, Wang ZY, Jones MA, Smirnoff N, Talbot NJ. 2007. Generation of reactive oxygen species by fungal NADPH oxidases is required for rice blast disease. Proc. Natl. Acad. Sci. USA 104: 11772-11777. https://doi.org/10.1073/pnas.0700574104
  16. Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, Torres MA, et al. 2003. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422: 442-446. https://doi.org/10.1038/nature01485
  17. Funato Y, Terabayashi T, Sakamoto R, Okuzaki D, Ichise H, Nojima H, et al. 2010. Nucleoredoxin sustains Wnt/betacatenin signaling by retaining a pool of inactive dishevelled protein. Curr. Biol. 20: 1945-1952. https://doi.org/10.1016/j.cub.2010.09.065
  18. Giesbert S, Schurg T, Scheele S, Tudzynski P. 2008. The NADPH oxidase Cpnox1 is required for full pathogenicity of the ergot fungus Claviceps purpurea. Mol. Plant Pathol. 9: 317-327. https://doi.org/10.1111/j.1364-3703.2008.00466.x
  19. Grant JJ, Yun BW, Loake GJ. 2000. Oxidative burst and cognate redox signalling reported by luciferase imaging: identification of a signal network that functions independently of ethylene, SA and Me-JA but is dependent on MAPKK activity. Plant J. 24: 569-582. https://doi.org/10.1046/j.1365-313x.2000.00902.x
  20. Gupta R, Luan S. 2003. Redox control of protein tyrosine phosphatases and mitogen-activated protein kinases in plants. Plant Physiol. 132: 1149-1152. https://doi.org/10.1104/pp.103.020792
  21. Gutteridge JM. 1994. Antioxidants, nutritional supplements and life-threatening diseases. Br. J. Biomed. Sci. 51: 288-295.
  22. Holmgren A, Lu J. 2010. Thioredoxin and thioredoxin reductase: current research with special reference to human disease. Biochem. Biophys. Res. Commun. 396: 120-124. https://doi.org/10.1016/j.bbrc.2010.03.083
  23. Kim EJ, Oh EK, Lee JK. 2014. Peroxidase and photoprotective activities of magnesium protoporphyrin IX. J. Microbiol. Biotechnol. 24: 36-43. https://doi.org/10.4014/jmb.1311.11088
  24. Kim HJ, Chen C, Kabbage M, Dickman MB. 2011. Identification and characterization of Sclerotinia sclerotiorum NADPH oxidases. Appl. Environ. Microbiol. 77: 7721-7729. https://doi.org/10.1128/AEM.05472-11
  25. Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, et al. 2003. NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J. 22: 2623-2633. https://doi.org/10.1093/emboj/cdg277
  26. Lambeth JD. 2004. NOX enzymes and the biology of reactive oxygen. Nat. Rev. Immunol. 4: 181-189. https://doi.org/10.1038/nri1312
  27. 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.
  28. Lessing F, Kniemeyer O, Wozniok I, Loeffler J, Kurzai O, Haertl A, Brakhage AA. 2007. The Aspergillus fumigatus transcriptional regulator AfYap1 represents the major regulator for defense against reactive oxygen intermediates but is dispensable for pathogenicity in an intranasal mouse infection model. Eukaryot. Cell 6: 2290-2302. https://doi.org/10.1128/EC.00267-07
  29. Lev S, Hadar R, Amedeo P, Baker SE, Yoder OC, Horwitz BA. 2005. Activation of an AP1-like transcription factor of the maize pathogen Cochliobolus heterostrophus in response to oxidative stress and plant signals. Eukaryot. Cell 4: 443-454. https://doi.org/10.1128/EC.4.2.443-454.2005
  30. Lin CH, Yang SL, Chung KR. 2009. The YAP1 homologmediated oxidative stress tolerance is crucial for pathogenicity of the necrotrophic fungus Alternaria alternata in citrus. Mol. Plant Microbe Interact. 22: 942-952. https://doi.org/10.1094/MPMI-22-8-0942
  31. Livanos P, Apostolakos P, Galatis B. 2012. Plant cell division: ROS homeostasis is required. Plant Signal. Behav. 7: 771-778. https://doi.org/10.4161/psb.20530
  32. Malagnac F, Lalucque H, Lepere G, Silar P. 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. https://doi.org/10.1016/j.fgb.2004.07.008
  33. Meng TC, Fukada T, Tonks NK. 2002. Reversible oxidation and inactivation of protein tyrosine phosphatases in vivo. Mol. Cell 9: 387-399. https://doi.org/10.1016/S1097-2765(02)00445-8
  34. Miller G, Schlauch K, Tam R, Cortes D, Torres MA, Shulaev V, et al. 2009. The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci. Signal. 2: ra45.
  35. Montero-Barrientos M, Hermosa R, Cardoza RE, Gutierrez S, Monte E. 2011. Functional analysis of the Trichoderma harzianum nox1 gene, encoding an NADPH oxidase, relates production of reactive oxygen species to specific biocontrol activity against Pythium ultimum. Appl. Environ. Microbiol. 77: 3009-3016. https://doi.org/10.1128/AEM.02486-10
  36. Morinaka A, Yamada M, Itofusa R, Funato Y, Yoshimura Y, Nakamura F, et al. 2011. Thioredoxin mediates oxidationdependent phosphorylation of CRMP2 and growth cone collapse. Sci. Signal. 4: ra26.
  37. Nauseef WM. 2004. Assembly of the phagocyte NADPH oxidase. Histochem. Cell Biol. 122: 277-291. https://doi.org/10.1007/s00418-004-0679-8
  38. Nauseef WM. 2008. Biological roles for the NOX family NADPH oxidases. J. Biol. Chem. 283: 16961-16965. https://doi.org/10.1074/jbc.R700045200
  39. Nishida M, Sawa T, Kitajima N, Ono K, Inoue H, Ihara H, et al. 2012. Hydrogen sulfide anion regulates redox signaling via electrophile sulfhydration. Nat. Chem. Biol. 8: 714-724. https://doi.org/10.1038/nchembio.1018
  40. Novo E, Parola M. 2008. Redox mechanisms in hepatic chronic wound healing and fibrogenesis. Fibrogenesis Tissue Repair 1: 5. https://doi.org/10.1186/1755-1536-1-5
  41. Ostman A, Frijhoff J, Sandin A, Bohmer FD. 2011. Regulation of protein tyrosine phosphatases by reversible oxidation. J. Biochem. 150: 345-356. https://doi.org/10.1093/jb/mvr104
  42. Owusu-Ansah E, Banerjee U. 2009. Reactive oxygen species prime Drosophila haematopoietic progenitors for differentiation. Nature 461: 537-541. https://doi.org/10.1038/nature08313
  43. Podder B, Song HY, Kim YS. 2014. Naringenin exerts cytoprotective effect against paraquat-induced toxicity in human bronchial epithelial BEAS-2B cells through NRF2 activation. J. Microbiol. Biotechnol. 24: 605-613. https://doi.org/10.4014/jmb.1402.02001
  44. Rinnerthaler M, Buttner S, Laun P, Heeren G, Felder TK, Klinger H, 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. USA 109: 8658-8663. https://doi.org/10.1073/pnas.1201629109
  45. Roca MG, Weichert M, Siegmund U, Tudzynski P, Fleissner A. 2012. Germling fusion via conidial anastomosis tubes in the grey mould Botrytis cinerea requires NADPH oxidase activity. Fungal Biol. 116: 379-387. https://doi.org/10.1016/j.funbio.2011.12.007
  46. Rodriguez R, Redman R. 2005. Balancing the generation and elimination of reactive oxygen species. Proc. Natl. Acad. Sci. USA 102: 3175-3176. https://doi.org/10.1073/pnas.0500367102
  47. Rolke Y, Tudzynski P. 2008. The small GTPase Rac and the p21-activated kinase Cla4 in Claviceps purpurea: interaction and impact on polarity, development and pathogenicity. Mol. Microbiol. 68: 405-423. https://doi.org/10.1111/j.1365-2958.2008.06159.x
  48. Ryder LS, Dagdas YF, Mentlak TA, Kershaw MJ, Thornton CR, Schuster M, et al. 2013. NADPH oxidases regulate septin-mediated cytoskeletal remodeling during plant infection by the rice blast fungus. Proc. Natl. Acad. Sci. USA 110: 3179- 3184. https://doi.org/10.1073/pnas.1217470110
  49. Saitoh M, Nishitoh H, Fujii M, Takeda K, Tobiume K, Sawada Y, et al. 1998. Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J. 17: 2596-2606. https://doi.org/10.1093/emboj/17.9.2596
  50. Sawa T, Zaki MH, Okamoto T, Akuta T, Tokutomi Y, Kim- Mitsuyama S, et al. 2007. Protein S -guany lation by the biological signal 8-nitroguanosine 3',5'-cyclic monophosphate. Nat. Chem. Biol. 3: 727-735. https://doi.org/10.1038/nchembio.2007.33
  51. Schopfer FJ, Cipollina C, Freeman BA. 2011. Formation and signaling actions of electrophilic lipids. Chem. Rev. 111: 5997- 6021. https://doi.org/10.1021/cr200131e
  52. Scott B, Eaton CJ. 2008. Role of reactive oxygen species in fungal cellular differentiations. Curr. Opin. Microbiol. 11: 488-493. https://doi.org/10.1016/j.mib.2008.10.008
  53. Segal AW. 2005. How neutrophils kill microbes. Annu. Rev. Immunol. 23: 197-223. https://doi.org/10.1146/annurev.immunol.23.021704.115653
  54. Segmuller N, Kokkelink L, Giesbert S, Odinius D, van Kan J, Tudzynski P. 2008. NADPH oxidases are involved in differentiation and pathogenicity in Botrytis cinerea. Mol. Plant Microbe Interact. 21: 808-819. https://doi.org/10.1094/MPMI-21-6-0808
  55. Singh KK. 2000. The Saccharomyces cerevisiae Sln1p-Ssk1p two-component system mediates response to oxidative stress and in an oxidant-specific fashion. Free Radic. Biol. Med. 29: 1043-1050. https://doi.org/10.1016/S0891-5849(00)00432-9
  56. Suh YA, Arnold RS, Lassegue B, Shi J, Xu X, Sorescu D, et al. 1999. Cell transformation by the superoxide-generating oxidase Mox1. Nature 401: 79-82. https://doi.org/10.1038/43459
  57. Takemoto D, Kamakura S, Saikia S, Becker Y, Wrenn R, Tanaka A, et al. 2011. Polarity proteins Bem1 and Cdc24 a re components of the filamentous fungal NADPH oxidase complex. Proc. Natl. Acad. Sci. USA 108: 2861-2866. https://doi.org/10.1073/pnas.1017309108
  58. Takemoto D, Tanaka A, Scott B. 2006. A $p67^{Phox}$-like regulator is recruited to control hyphal branching in a fungal-grass mutualistic symbiosis. Plant Cell 18: 2807-2821. https://doi.org/10.1105/tpc.106.046169
  59. 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. https://doi.org/10.1016/j.fgb.2007.04.011
  60. Tanaka A, Christensen MJ, Takemoto D, Park P, Scott B. 2006. Reactive oxygen species play a role in regulating a fungus-perennial ryegrass mutualistic interaction. Plant Cell 18: 1052-1066. https://doi.org/10.1105/tpc.105.039263
  61. Tanaka A, Takemoto D, Hyon GS, Park P, Scott B. 2008. NoxA activation by the small GTPase RacA is required to maintain a mutualistic symbiotic association between Epichloe festucae and perennial ryegrass. Mol. Microbiol. 68: 1165-1178. https://doi.org/10.1111/j.1365-2958.2008.06217.x
  62. Temme N, Tudzynski P. 2009. Does Botrytis cinerea ignore $H_2O_2$-induced oxidative stress during infection? Characterization of Botrytis activator protein 1. Mol. Plant Microbe Interact. 22: 987-998. https://doi.org/10.1094/MPMI-22-8-0987
  63. Theopold U. 2009. Developmental biology: a bad boy comes good. Nature 461: 486-487. https://doi.org/10.1038/461486a
  64. Torres MA, Dangl JL, Jones JD. 2002. Arabidopsis $gp91^{phox}$ homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc. Natl. Acad. Sci. USA 99: 517-522. https://doi.org/10.1073/pnas.012452499
  65. Torres MA, Jones JD, Dangl JL. 2005. Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nat. Genet. 37: 1130-1134. https://doi.org/10.1038/ng1639
  66. Torres MA, Jones JD, Dangl JL. 2006. Reactive oxygen species signaling in response to pathogens. Plant Physiol. 141: 373-378. https://doi.org/10.1104/pp.106.079467
  67. Tripathy BC, Oelmuller R. 2012. Reactive oxygen species generation and signaling in plants. Plant Signal. Behav. 7: 1621-1633. https://doi.org/10.4161/psb.22455
  68. Tsukagoshi H, Busch W, Benfey PN. 2010. Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 143: 606-616. https://doi.org/10.1016/j.cell.2010.10.020
  69. van Montfort RL, Congreve M, Tisi D, Carr R, Jhoti H. 2003. Oxidation state of the active-site cysteine in protein tyrosine phosphatase 1B. Nature 423: 773-777. https://doi.org/10.1038/nature01681
  70. Veal EA, Findlay VJ, D ay AM, B ozonet SM, Evans J M, Quinn J, Morgan BA. 2004. A 2-Cys peroxiredoxin regulates peroxide-induced oxidation and activation of a stressactivated MAP kinase. Mol. Cell 15: 129-139. https://doi.org/10.1016/j.molcel.2004.06.021
  71. Venugopalan V, Tripathi SK, Nahar P, Saradhi PP, Das RH, Gautam HK. 2013. Characterization of canthaxanthin isomers isolated from a new soil Dietzia sp. and their antioxidant activities. J. Microbiol. Biotechnol. 23: 237-245. https://doi.org/10.4014/jmb.1203.03032
  72. Wang K, Zhang T, Dong Q, Nice EC, Huang C, Wei Y. 2013. Redox homeostasis: the linchpin in stem cell self-renewal and differentiation. Cell Death Dis. 4: e537. https://doi.org/10.1038/cddis.2013.50
  73. Wang L, Mogg C, Walkowiak S, Joshi M, Subramaniam R. 2014. Characterization of NADPH oxidase genes NoxA and NoxB in Fusarium graminearum. Can. J. Plant Pathol. 36: 12-21. https://doi.org/10.1080/07060661.2013.868370
  74. Yang SL, Chung KR. 2012. The NADPH oxidase-mediated production of hydrogen peroxide ($H_2O_2$) and resistance to oxidative stress in the necrotrophic pathogen Alternaria alternata of citrus. Mol. Plant Pathol. 13: 900-914. https://doi.org/10.1111/j.1364-3703.2012.00799.x
  75. Zhang X, De Micheli M, Coleman ST, Sanglard D, Moye- Rowley WS. 2000. Analysis of the oxidative stress regulation of the Candida albicans transcription factor, Cap1p. Mol. Microbiol. 36: 618-629.

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