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The inhibitor of apoptosis protein MoBir1 is involved in the suppression of hydrogen peroxide-induced fungal cell death, reactive oxygen species generation, and pathogenicity of rice blast fungus

  • Lisha Zhang
  • Kaili Zhong
  • Ruili Lv
  • Xiaobo Zheng
  • Zhengguang Zhang
  • Haifeng ZhangEmail author
Applied genetics and molecular biotechnology

Abstract

The inhibitor of apoptosis protein (IAP) family has been identified in a variety of organisms. All IAPs contain one to three baculoviral IAP repeat (BIR) domains, which are required for anti-apoptotic activity. Here, we identified a type II BIR domain-containing protein, MoBir1, in the rice blast fungus Magnaporthe oryzae. Expression of the MoBIR1 gene in Saccharomyces cerevisiae suppressed hydrogen peroxide-induced cell death and delayed yeast cell chronological aging. Delayed aging was found to require the carboxyl terminus of MoBir1. M. oryzae transformants overexpressing the MoBIR1 gene demonstrated increased growth rate and biomass, delayed mycelial aging, and enhanced resistance to hydrogen peroxide but reduced reactive oxygen species generation and virulence. Moreover, MoBIR1-overexpressing transformants exhibited anti-apoptotic activity. However, MoBIR1 silencing resulted in no obvious phenotypic changes, compared with the wild-type M. oryzae strain Guy11. Our findings broaden the knowledge on fungal type II BIR domain-containing proteins.

Keywords

Magnaporthe oryzae Inhibitor of apoptosis Cell death ROS Pathogenicity 

Notes

Funding

This study was funded by the National Key Research and Development Program of China (grant number 2016YFD0300700/2016YFD0300706), the Fundamental Research Funds for the Central Universities (grant number KYZ201816), and the Outstanding Youth Foundation of Jiangsu Province (grant number BK20160074).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

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

Supplementary material

253_2019_9931_MOESM1_ESM.pdf (568 kb)
ESM 1 (PDF 567 kb)

References

  1. Ambrosini G, Adida C, Altieri DC (1997) A novel anti-apoptosis gene, survivin, expressed in cancer and lymphoma. Nat Med 3:917–921CrossRefGoogle Scholar
  2. Baehrecke EH (2002) How death shapes life during development. Nat Rev Mol Cell Biol 3:779–787Google Scholar
  3. Barry M, Heibein J, Pinkoski M, Bleackley RC (2000) Quantitative measurement of apoptosis induced by cytotoxic T lymphocytes. Methods Enzymol 322:40–46CrossRefGoogle Scholar
  4. Cai X, Zhang X, Li X, Liu M, Liu X, Wang X, Zhang HF, Zheng XB, Zhang ZG (2017) The atypical guanylate kinase MoGuk2 plays important roles in asexual/sexual development, conidial septation, and pathogenicity in the rice blast fungus. Front Microbiol 8:2467Google Scholar
  5. Carroll AM, Sweigard JA, Valent B (1994) Improved vectors for selecting resistance to hygromycin. Fungal Genet Newsl 41:22Google Scholar
  6. Crook NE, Clem RJ, Miller LK (1993) An apoptosis-inhibiting baculovirus gene with a zinc finger-like motif. J Virol 67:2168–2174Google Scholar
  7. Cummings BS, Wills LP, Schnellmann RG (2004) Measurement of cell death in mammalian cells. Curr Protoc Pharmacol Chapter 12:Unit 12.8Google Scholar
  8. Deveraux QL, Reed JC (1999) IAP family proteins suppressors of apoptosis. Genes Dev 13:239–252CrossRefGoogle Scholar
  9. Deveraux QL, Takahashi R, Salvesen GS, Reed JC (1997a) X-linked IAP is a direct inhibitor of cell-death proteases. Nature 388:300–304CrossRefGoogle Scholar
  10. Deveraux QL, Roy N, Takahashi R, Salvesen GS, Reed JC (1997b) The c-IAP-1 and c-IAP-2 proteins are direct inhibitors of specific caspases. EMBO J 16:6914–6925CrossRefGoogle Scholar
  11. 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 U S A 104:11772–11777CrossRefGoogle Scholar
  12. Gao K, Xiong Q, Xu J, Wang K, Wang K (2013) CpBir1 is required for conidiation, virulence and anti-apoptotic effects and influences hypovirus transmission in Cryphonectria parasitica. Fungal Genet Biol 51:60–71CrossRefGoogle Scholar
  13. Green DR (2005) Apoptotic pathways: ten minutes to dead. Cell 121:671–674CrossRefGoogle Scholar
  14. Guo M, Guo W, Chen Y, Dong S, Zhang X, Zhang H, Song W, Wang W, Wang Q, Lv R, Zhang Z, Wang Y, Zheng X (2010) The basic leucine zipper transcription factor Moatf1 mediates oxidative stress response and is necessary for full virulence of the rice blast fungus Magnaporthe oryzae. Mol Plant-Microbe Interact 23:1053–1068CrossRefGoogle Scholar
  15. Guo M, Chen Y, Du Y, Dong Y, Guo W, Zhai S, Zhang H, Dong S, Zhang Z, Wang Y, Wang P, Zheng X (2011) The bZIP transcription factor MoAP1 mediates the oxidative stress response and is critical for pathogenicity of the rice blast fungus Magnaporthe oryzae. PLoS Pathog 7:e1001302CrossRefGoogle Scholar
  16. Hengartner MO, Bryant JA (2000) Apoptotic cell death: from worms to wombats ... but what about the weeds? Symp Soc Exp Biol 52:1–12Google Scholar
  17. Herker E, Jungwirth H, Lehmann KA, Maldener C, Fröhlich KU, Wissing S, Buttner S, Fehr M, Sigrist S, Madeo F (2004) Chronological aging leads to apoptosis in yeast. J Cell Biol 164:501–507CrossRefGoogle Scholar
  18. Kershaw MJ, Talbot NJ (2009) Genome-wide functional analysis reveals that infection-associated fungal autophagy is necessary for rice blast disease. Proc Natl Acad Sci U S A 106:15967–15972CrossRefGoogle Scholar
  19. Kocab AJ, Duckett CS (2016) Inhibitor of apoptosis proteins as intracellular signaling intermediates. FEBS J 283:221–231CrossRefGoogle Scholar
  20. Laun P, Pichova A, Madeo F, Fuchs J, Ellinger A, Kohlwein S, Dawes I, Fröhlich KU, Breitenbach M (2001) Aged mother cells of Saccharomyces cerevisiae show markers of oxidative stress and apoptosis. Mol Microbiol 39:1166–1173CrossRefGoogle Scholar
  21. Li F, Flanary PL, Altieri DC, Dohlman HG (2000) Cell division regulation by BIR1, a member of the inhibitor of apoptosis family in yeast. J Biol Chem 275:6707–6711CrossRefGoogle Scholar
  22. Lieberthal W, Triaca V, Levine J (1996) Mechanisms of death induced by cisplatin in proximal tubular epithelial cells: apoptosis vs. necrosis. Am J Phys 270:F700–F708Google Scholar
  23. Liu XY, Qian B, Gao CY, Huang SH, Cai YC, Zhang HF, Zheng XB, Wang P, Zhang ZG (2016) The putative protein phosphatase MoYvh1 functions upstream of MoPdeH to regulate the development and pathogenicity in Magnaporthe oryzae. Mol Plant-Microbe Interact 29:496–507CrossRefGoogle Scholar
  24. Liu XH, Zhao YH, Zhu XM, Zeng XQ, Huang LY, Dong B, Su ZZ, Wang Y, Lu JP, Lin FC (2017) Autophagy-related protein MoAtg14 is involved in differentiation, development and pathogenicity in the rice blast fungus Magnaporthe oryzae. Sci Rep 7:40018CrossRefGoogle Scholar
  25. Madeo F, Herker E, Maldener C, Wissing S, Lachelt S, Herlan M, Fehr M, Lauber K, Sigrist SJ, Wesselborg S, Fröhlich KU (2002) A caspase-related protease regulates apoptosis in yeast. Mol Cell 9:911–917CrossRefGoogle Scholar
  26. Nakayashiki H, Hanada S, Nguyen BQ, Kadotani N, Tosa Y, Mayama S (2005) RNA silencing as a tool for exploring gene function in ascomycete fungi. Fungal Genet Biol 42:275–283CrossRefGoogle Scholar
  27. Otsuki Y, Li Z, Shibata MA (2003) Apoptotic detection methods-from morphology to gene. Prog Histochem Cytochem 38:275–339CrossRefGoogle Scholar
  28. Roy N, Deveraux QL, Takahashi R, Salvesen GS, Reed JC (1997) The c-IAP-1 and c-IAP-2 proteins are direct inhibitors of specific caspases. EMBO J 16:6914–6925CrossRefGoogle Scholar
  29. Sharon A, Finkelstein F, Shlezinger N, Hatam I (2009) Fungal apoptosis: function, genes and gene function. FEMS Microbiol Rev 33:833–854CrossRefGoogle Scholar
  30. Shlezinger N, Doron A, Sharon A (2011a) Apoptosis-like programmed cell death in the grey mould fungus Botrytis cinerea: genes and their role in pathogenicity. Biochem Soc Trans 39:1493–1498CrossRefGoogle Scholar
  31. Shlezinger N, Minz A, Gur Y, Hatam I, Dagdas YF, Talbot NJ, Sharon A (2011b) Anti-apoptotic machinery protects the necrotrophic fungus Botrytis cinerea from host-induced apoptotic-like cell death during plant infection. PLoS Pathog 7:e1002185CrossRefGoogle Scholar
  32. Shlezinger N, Goldfinger N, Sharon A (2012) Apoptotic-like programed cell death in fungi: the benefits in filamentous species. Front Oncol 2:97CrossRefGoogle Scholar
  33. Shlezinger N, Israeli M, Mochly E, Oren-Young L, Zhu WJ Sharon A (2016) Translocation from nuclei to cytoplasm is necessary for anti A-PCD activity and turnover of the type II IAP BcBir1. Mol Micoriol 99:393–406CrossRefGoogle Scholar
  34. Shlezinger N, Irmer H, Dhingra S, Beattie SR, Cramer RA, Braus GH, Sharon A, Hohl TM (2017) Sterilizing immunity in the lung relies on targeting fungal apoptosis-like programmed cell death. Science 357:1037–1041CrossRefGoogle Scholar
  35. Talbot NJ, Ebbole DJ, Hamer JE (1993) Identification and characterization of MPG1, a gene involved in pathogenicity from the rice blast fungus Magnaporthe grisea. Plant Cell 5:1575–1590CrossRefGoogle Scholar
  36. Tang W, Ru YY, Hong L, Zhu Q, Zuo RF, Guo XX, Wang JZ, Zhang HF, Zheng XB, Wang P, Zhang ZG (2015) System-wide characterization of bZIP transcription factor proteins involved in infection-related morphogenesis of Magnaporthe oryzae. Environ Microbiol 17:1377–1396CrossRefGoogle Scholar
  37. Valent B, Farrall L, Chumley FG (1991) Magnaporthe grisea genes for pathogenicity and virulence identified through a series of backcrosses. Genetics 127:87–101Google Scholar
  38. Veneault-Fourrey C, Barooah M, Egan M, Wakley G, Talbot NJ (2006) Autophagic fungal cell death is necessary for infection by the rice blast fungus. Science 312:580–583CrossRefGoogle Scholar
  39. Verhagen AM, Coulson EJ, Vaux DL (2001) Inhibitor of apoptosis proteins and their relatives: IAPs and other BIRPs. Genome Biol 2:3009CrossRefGoogle Scholar
  40. Walter D, Wissing S, Madeo F, Fahrenkrog B (2006) The inhibitor-of-apoptosis protein Bir1p protects against apoptosis in S. cerevisiae and is a substrate for the yeast homologue of Omi/HtrA2. J Cell Sci 119:1843–1851CrossRefGoogle Scholar
  41. Widlund PO, Lyssand JS, Anderson S, Niessen S, Yates JR, Davis TN (2006) Phosphorylation of the chromosomal passenger protein Bir1 is required for localization of Ndc10 to the spindle during anaphase and full spindle elongation. Mol Biol Cell 17:1065–1074CrossRefGoogle Scholar
  42. Zhang HF, Tang W, Liu KY, Huang Q, Zhang X, Yan X, Chen Y, Wang JS, Qi ZQ, Wang ZY, Zheng XB, Wang P, Zhang ZG (2011) Eight RGS and RGS-like proteins orchestrate growth, differentiation, and pathogenicity of Magnaporthe oryzae. PLoS Pathog 7:e1002450CrossRefGoogle Scholar
  43. Zhang HF, Ma HY, Xie X, Ji J, Dong YH, Du Y, Tang W, Zheng XB, Wang P, Zhang ZG (2014) Comparative proteomic analyses reveal that the regulators of G-protein signaling proteins regulate amino acid metabolism of the rice blast fungus Magnaporthe oryzae. Proteomics 14:2508–2522CrossRefGoogle Scholar
  44. Zhao X, Xue C, Kim Y, Xu J (2004) A ligation-PCR approach for generating gene replacement constructs in Magnaporthe grisea. Fungal Genet Newsl 51:17–18Google Scholar
  45. Zou SS, Liu Y, Min GY, Liang YH (2018) Trs20, Trs23, Trs31 and Bet5 participate in autophagy through GTPase Ypt1 in Saccharomyces cerevisiae. Arch Biol Sci 70:109–118CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University and Key Laboratory of Integrated Management of Crop Diseases and PestsMinistry of EducationNanjingChina
  2. 2.Department of Plant Biochemistry, Center of Plant Molecular Biology (ZMBP)Eberhard Karls University TübingenTübingenGermany

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