1887

Abstract

Antibiosis is one of the widespread strategies used by spp. against plant fungal pathogens, the mechanism of which, however, remains poorly understood. Peptaibols are a large family of antimicrobial peptides produced by spp. Our previous study showed that trichokonins, a type of peptaibol from SMF2, exhibited antibiotic activities against plant fungal pathogens. In this study, we first demonstrated that trichokonin VI (TK VI) induced extensive apoptotic programmed cell death in plant fungal pathogens. For a deeper insight into the apoptotic mechanism involved in the action of TK VI, was used as a model. Cells of treated with TK VI showed apoptotic hallmarks, such as exposure of phosphatidylserine, the appearance of reactive oxygen species and fragmentation of nuclear DNA. Moreover, TK VI-treated cells exhibited an accumulation of cytoplasmic vacuoles with loss of the mitochondrial transmembrane potential, and this process was independent of metacaspases. Therefore, TK VI induces metacaspase-independent apoptotic cell death in . This represents what is believed to be the first report to reveal the antibiotic mechanism of peptaibols against plant fungal pathogens.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.052670-0
2012-01-01
2019-12-11
Loading full text...

Full text loading...

/deliver/fulltext/micro/158/1/166.html?itemId=/content/journal/micro/10.1099/mic.0.052670-0&mimeType=html&fmt=ahah

References

  1. Almeida B. , Silva A. , Mesquita A. , Sampaio-Marques B. , Rodrigues F. , Ludovico P. . ( 2008; ). Drug-induced apoptosis in yeast. . Biochim Biophys Acta 1783:, 1436–1448. [CrossRef] [PubMed]
    [Google Scholar]
  2. Andrés M. T. , Viejo-Díaz M. , Fierro J. F. . ( 2008; ). Human lactoferrin induces apoptosis-like cell death in Candida albicans: critical role of K+-channel-mediated K+ efflux. . Antimicrob Agents Chemother 52:, 4081–4088. [CrossRef] [PubMed]
    [Google Scholar]
  3. Benedetti E. , Bavoso A. , Di Blasio B. , Pavone V. , Pedone C. , Toniolo C. , Bonora G. M. . ( 1982; ). Peptaibol antibiotics: a study on the helical structure of the 2-9 sequence of emerimicins III and IV. . Proc Natl Acad Sci U S A 79:, 7951–7954. [CrossRef] [PubMed]
    [Google Scholar]
  4. Benítez T. , Rincón A. M. , Limón M. C. , Codón A. C. . ( 2004; ). Biocontrol mechanisms of Trichoderma strains. . Int Microbiol 7:, 249–260.[PubMed]
    [Google Scholar]
  5. Berrocal-Lobo M. , Molina A. . ( 2008; ). Arabidopsis defense response against Fusarium oxysporum . . Trends Plant Sci 13:, 145–150. [CrossRef] [PubMed]
    [Google Scholar]
  6. Béven L. , Wróblewski H. . ( 1997; ). Effect of natural amphipathic peptides on viability, membrane potential, cell shape and motility of mollicutes. . Res Microbiol 148:, 163–175. [CrossRef] [PubMed]
    [Google Scholar]
  7. Bonnafous J. C. , Dornand J. , Mani J. C. . ( 1982; ). Alamethicin or detergent permeabilization of the cell membrane as a tool for adenylate cyclase determination. . Biochim Biophys Acta 720:, 235–241. [CrossRef] [PubMed]
    [Google Scholar]
  8. Chen L. L. , Liu L. J. , Shi M. , Song X. Y. , Zheng C. Y. , Chen X. L. , Zhang Y. Z. . ( 2009; ). Characterization and gene cloning of a novel serine protease with nematicidal activity from Trichoderma pseudokoningii SMF2. . FEMS Microbiol Lett 299:, 135–142. [CrossRef] [PubMed]
    [Google Scholar]
  9. Cheng J. , Park T. S. , Chio L. C. , Fischl A. S. , Ye X. S. . ( 2003; ). Induction of apoptosis by sphingoid long-chain bases in Aspergillus nidulans . . Mol Cell Biol 23:, 163–177. [CrossRef] [PubMed]
    [Google Scholar]
  10. Cheng W. C. , Leach K. M. , Hardwick J. M. . ( 2008; ). Mitochondrial death pathways in yeast and mammalian cells. . Biochim Biophys Acta 1783:, 1272–1279. [CrossRef] [PubMed]
    [Google Scholar]
  11. Chet I. , Inbar J. . ( 1994; ). Biological control of fungal pathogens. . Appl Biochem Biotechnol 48:, 37–43. [CrossRef] [PubMed]
    [Google Scholar]
  12. Chugh J. K. , Wallace B. A. . ( 2001; ). Peptaibols: models for ion channels. . Biochem Soc Trans 29:, 565–570. [CrossRef] [PubMed]
    [Google Scholar]
  13. Csermely P. , Radics L. , Rossi C. , Szamel M. , Ricci M. , Mihály K. , Somogyi J. . ( 1994; ). The nonapeptide leucinostatin A acts as a weak ionophore and as an immunosuppressant on T lymphocytes. . Biochim Biophys Acta 1221:, 125–132. [CrossRef] [PubMed]
    [Google Scholar]
  14. Daniel J. F. S. , Filho E. R. . ( 2007; ). Peptaibols of Trichoderma . . Nat Prod Rep 24:, 1128–1141. [CrossRef] [PubMed]
    [Google Scholar]
  15. Eisenberg T. , Büttner S. , Kroemer G. , Madeo F. . ( 2007; ). The mitochondrial pathway in yeast apoptosis. . Apoptosis 12:, 1011–1023. [CrossRef] [PubMed]
    [Google Scholar]
  16. Feissner R. F. , Skalska J. , Gaum W. E. , Sheu S. S. . ( 2009; ). Crosstalk signaling between mitochondrial Ca2+ and ROS. . Front Biosci 14:, 1197–1218. [CrossRef] [PubMed]
    [Google Scholar]
  17. Häcker G. . ( 2000; ). The morphology of apoptosis. . Cell Tissue Res 301:, 5–17. [CrossRef] [PubMed]
    [Google Scholar]
  18. Hamann A. , Brust D. , Osiewacz H. D. . ( 2008; ). Apoptosis pathways in fungal growth, development and ageing. . Trends Microbiol 16:, 276–283. [CrossRef] [PubMed]
    [Google Scholar]
  19. Harman G. E. , Howell C. R. , Viterbo A. , Chet I. , Lorito M. . ( 2004; ). Trichoderma species – opportunistic, avirulent plant symbionts. . Nat Rev Microbiol 2:, 43–56. [CrossRef] [PubMed]
    [Google Scholar]
  20. Howell C. R. . ( 2003; ). Mechanisms employed by Trichoderma species in the biological control of plant diseases: the history and evolution of current concepts. . Plant Dis 87:, 4–10. [CrossRef]
    [Google Scholar]
  21. Huang Q. , Tezuka Y. , Kikuchi T. , Momose Y. . ( 1994; ). Trichokonin VI, a new Ca2+ channel agonist in bullfrog cardiac myocytes. . Eur J Pharmacol 271:, R5–R6. [CrossRef] [PubMed]
    [Google Scholar]
  22. Huang Q. , Tezuka Y. , Hatanaka Y. , Kikuchi T. , Nishi A. , Tubaki K. . ( 1995; ). Studies on metabolites of mycoparasitic fungi. IV. Minor peptaibols of Trichoderma koningii . . Chem Pharm Bull (Tokyo) 43:, 1663–1667.[PubMed] [CrossRef]
    [Google Scholar]
  23. Katayama T. , Miyagawa K. , Kodama T. , Oikawa S. . ( 2001; ). Trichorzin HA V, a member of the peptaibol family, stimulates intracellular cAMP formation in cells expressing the calcitonin receptor. . Biol Pharm Bull 24:, 1420–1422. [CrossRef] [PubMed]
    [Google Scholar]
  24. Lehtopolku M. , Nakari U. M. , Kotilainen P. , Huovinen P. , Siitonen A. , Hakanen A. J. . ( 2010; ). Antimicrobial susceptibilities of multidrug-resistant Campylobacter jejuni and C. coli strains: in vitro activities of 20 antimicrobial agents. . Antimicrob Agents Chemother 54:, 1232–1236. [CrossRef] [PubMed]
    [Google Scholar]
  25. Leiter E. , Szappanos H. , Oberparleiter C. , Kaiserer L. , Csernoch L. , Pusztahelyi T. , Emri T. , Pócsi I. , Salvenmoser W. , Marx F. . ( 2005; ). Antifungal protein PAF severely affects the integrity of the plasma membrane of Aspergillus nidulans and induces an apoptosis-like phenotype. . Antimicrob Agents Chemother 49:, 2445–2453. [CrossRef] [PubMed]
    [Google Scholar]
  26. Liang Q. L. , Li W. , Zhou B. . ( 2008; ). Caspase-independent apoptosis in yeast. . Biochim Biophys Acta 1783:, 1311–1319. [CrossRef] [PubMed]
    [Google Scholar]
  27. Madeo F. , Herker E. , Maldener C. , Wissing S. , Lächelt S. , Herlan M. , Fehr M. , Lauber K. , Sigrist S. J. . & other authors ( 2002; ). A caspase-related protease regulates apoptosis in yeast. . Mol Cell 9:, 911–917. [CrossRef] [PubMed]
    [Google Scholar]
  28. Madeo F. , Herker E. , Wissing S. , Jungwirth H. , Eisenberg T. , Fröhlich K. U. . ( 2004; ). Apoptosis in yeast. . Curr Opin Microbiol 7:, 655–660. [CrossRef] [PubMed]
    [Google Scholar]
  29. Matsuzaki K. , Shioyama T. , Okamura E. , Umemura J. , Takenaka T. , Takaishi Y. , Fujita T. , Miyajima K. . ( 1991; ). A comparative study on interactions of α-aminoisobutyric acid containing antibiotic peptides, trichopolyn I and hypelcin A with phosphatidylcholine bilayers. . Biochim Biophys Acta 1070:, 419–428. [CrossRef] [PubMed]
    [Google Scholar]
  30. Mazzoni C. , Falcone C. . ( 2008; ). Caspase-dependent apoptosis in yeast. . Biochim Biophys Acta 1783:, 1320–1327. [CrossRef] [PubMed]
    [Google Scholar]
  31. Mes J. J. , Wit R. , Testerink C. S. , de Groot F. , Haring M. A. , Cornelissen B. J. . ( 1999; ). Loss of avirulence and reduced pathogenicity of a gamma-irradiated mutant of Fusarium oxysporum f. sp. lycopersici . . Phytopathology 89:, 1131–1137. [CrossRef] [PubMed]
    [Google Scholar]
  32. Mousavi S. A. , Robson G. D. . ( 2004; ). Oxidative and amphotericin B-mediated cell death in the opportunistic pathogen Aspergillus fumigatus is associated with an apoptotic-like phenotype. . Microbiology 150:, 1937–1945. [CrossRef] [PubMed]
    [Google Scholar]
  33. Peltola J. , Ritieni A. , Mikkola R. , Grigoriev P. A. , Pócsfalvi G. , Andersson M. A. , Salkinoja-Salonen M. S. . ( 2004; ). Biological effects of Trichoderma harzianum peptaibols on mammalian cells. . Appl Environ Microbiol 70:, 4996–5004. [CrossRef] [PubMed]
    [Google Scholar]
  34. Pereira C. , Silva R. D. , Saraiva L. , Johansson B. , Sousa M. J. , Côrte-Real M. . ( 2008; ). Mitochondria-dependent apoptosis in yeast. . Biochim Biophys Acta 1783:, 1286–1302. [CrossRef] [PubMed]
    [Google Scholar]
  35. Perrone G. G. , Tan S. X. , Dawes I. W. . ( 2008; ). Reactive oxygen species and yeast apoptosis. . Biochim Biophys Acta 1783:, 1354–1368. [CrossRef] [PubMed]
    [Google Scholar]
  36. Phillips A. J. , Crowe J. D. , Ramsdale M. . ( 2006; ). Ras pathway signaling accelerates programmed cell death in the pathogenic fungus Candida albicans . . Proc Natl Acad Sci U S A 103:, 726–731. [CrossRef] [PubMed]
    [Google Scholar]
  37. Pyke T. R. , Dietz A. . ( 1966; ). U-21,963, a new antibiotic. I. Discovery and biological activity. . Appl Microbiol 14:, 506–510.[PubMed]
    [Google Scholar]
  38. Ramsdale M. . ( 2008; ). Programmed cell death in pathogenic fungi. . Biochim Biophys Acta 1783:, 1369–1380.[CrossRef]
    [Google Scholar]
  39. Reiter J. , Herker E. , Madeo F. , Schmitt M. J. . ( 2005; ). Viral killer toxins induce caspase-mediated apoptosis in yeast. . J Cell Biol 168:, 353–358. [CrossRef] [PubMed]
    [Google Scholar]
  40. Rippa S. , Eid M. , Formaggio F. , Toniolo C. , Béven L. . ( 2010; ). Hypersensitive-like response to the pore-former peptaibol alamethicin in Arabidopsis thaliana . . Chem BioChem 11:, 2042–2049. [CrossRef] [PubMed]
    [Google Scholar]
  41. Roze L. V. , Linz J. E. . ( 1998; ). Lovastatin triggers an apoptosis-like cell death process in the fungus Mucor racemosus. . Fungal Genet Biol 25:, 119–133. [CrossRef] [PubMed]
    [Google Scholar]
  42. Schrauwen P. , Schrauwen-Hinderling V. , Hoeks J. , Hesselink M. K. . ( 2010; ). Mitochondrial dysfunction and lipotoxicity. . Biochim Biophys Acta 1801:, 266–271.[PubMed] [CrossRef]
    [Google Scholar]
  43. Semighini C. P. , Hornby J. M. , Dumitru R. , Nickerson K. W. , Harris S. D. . ( 2006; ). Farnesol-induced apoptosis in Aspergillus nidulans reveals a possible mechanism for antagonistic interactions between fungi. . Mol Microbiol 59:, 753–764. [CrossRef] [PubMed]
    [Google Scholar]
  44. Shi M. , Wang H. N. , Xie S. T. , Luo Y. , Sun C. Y. , Chen X. L. , Zhang Y. Z. . ( 2010; ). Antimicrobial peptaibols, novel suppressors of tumor cells, targeted calcium-mediated apoptosis and autophagy in human hepatocellular carcinoma cells. . Mol Cancer 9:, 26. [CrossRef] [PubMed]
    [Google Scholar]
  45. Shima A. , Fukushima K. , Arai T. , Terada H. . ( 1990; ). Dual inhibitory effects of the peptide antibiotics leucinostatins on oxidative phosphorylation in mitochondria. . Cell Struct Funct 15:, 53–58. [CrossRef] [PubMed]
    [Google Scholar]
  46. Song X. Y. , Shen Q. T. , Xie S. T. , Chen X. L. , Sun C. Y. , Zhang Y. Z. . ( 2006; ). Broad-spectrum antimicrobial activity and high stability of trichokonins from Trichoderma koningii SMF2 against plant pathogens. . FEMS Microbiol Lett 260:, 119–125. [CrossRef] [PubMed]
    [Google Scholar]
  47. Song X. Y. , Xie S. T. , Chen X. L. , Sun C. Y. , Shi M. , Zhang Y. Z. . ( 2007; ). Solid-state fermentation for trichokonins production from Trichoderma koningii SMF2 and preparative purification of trichokonin VI by a simple protocol. . J Biotechnol 131:, 209–215. [CrossRef] [PubMed]
    [Google Scholar]
  48. Vercammen D. , Declercq W. , Vandenabeele P. , Van Breusegem F. . ( 2007; ). Are metacaspases caspases?. J Cell Biol 179:, 375–380. [CrossRef] [PubMed]
    [Google Scholar]
  49. Viterbo A. , Harel M. , Horwitz B. A. , Chet I. , Mukherjee P. K. . ( 2005; ). Trichoderma mitogen-activated protein kinase signaling is involved in induction of plant systemic resistance. . Appl Environ Microbiol 71:, 6241–6246. [CrossRef] [PubMed]
    [Google Scholar]
  50. Whitmore L. , Wallace B. A. . ( 2004; ). The Peptaibol Database: a database for sequences and structures of naturally occurring peptaibols. . Nucleic Acids Res 32: (Database issue), D593–D594. [CrossRef] [PubMed]
    [Google Scholar]
  51. Wiest A. , Grzegorski D. , Xu B. W. , Goulard C. , Rebuffat S. , Ebbole D. J. , Bodo B. , Kenerley C. . ( 2002; ). Identification of peptaibols from Trichoderma virens and cloning of a peptaibol synthetase. . J Biol Chem 277:, 20862–20868. [CrossRef] [PubMed]
    [Google Scholar]
  52. Yedidia I. , Benhamou N. , Chet I. . ( 1999; ). Induction of defense responses in cucumber plants (Cucumis sativus L.) by the biocontrol agent Trichoderma harzianum . . Appl Environ Microbiol 65:, 1061–1070.[PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.052670-0
Loading
/content/journal/micro/10.1099/mic.0.052670-0
Loading

Data & Media loading...

Supplements

Supplementary Figs S1 - S3 

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error