Skip to main content
SpringerLink
Log in

In vitro photodynamic inactivation of conidia of the phytopathogenic fungus Colletotrichum graminicola with cationic porphyrins

  • Paper
  • Published:
Photochemical & Photobiological Sciences Aims and scope Submit manuscript

Abstract

Photodynamic inactivation (PDI) is an efficient approach for the elimination of a series of microorganisms; however, PDI involving phytopathogenic filamentous fungi is scarce in the literature. In the present study, we have demonstrated the photoinactivating properties of five cationic meso-(1-methyl-4-pyridinio)porphyrins on conidia of the phytopathogen Colletotrichum graminicola. For this purpose, photophysical properties (photostability and 1O2 singlet production) of the porphyrins under study were first evaluated. PDI assays were then performed with a fluence of 30, 60, 90 and 120 J cm−2 and varying the porphyrin concentration from 1 to 25 μmol L−1. Considering the lowest concentration that enabled the best photoinactivation, with the respective lowest effective irradiation time, the meso-(1-methyl-4-pyridinio)porphyrins herein studied could be ranked as follows: triple-charged 4 (1 μmol L−1 with a fluence of 30 J cm−2) > double-charged-trans2 (1 μmol L−1 with 60 J cm−2) > tetra-charged 5 (15 μmol L−1 with 90 J cm−2) > mono-charged 1 (25 μmol L−1 with 120 J cm−2). Double-charged-cis-porphyrin 3 inactivated C. graminicola conidia in the absence of light. Evaluation of the porphyrin binding to the conidia and fluorescence microscopic analysis were also performed, which were in agreement with the PDI results. In conclusion, the cationic porphyrins herein studied were considered efficient photosensitizers to inactivate C. graminicola conidia. The amount and position of positive charges are related to the compounds’ amphiphilicity and therefore to their photodynamic activity.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. M. Wainwright, J. Antimicrob. Chemother., 1998, 42, 13–28.

    Article  CAS  PubMed  Google Scholar 

  2. F. Gad, T. Zahra, T. Hasan and M. R. Hamblin, Antimicrob. Agents Chemother., 2004, 48, 2173–2178.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. J. R. Perussi, Quim. Nova, 2007, 30, 988–994.

    Article  CAS  Google Scholar 

  4. E. Reddi, M. Ceccon, G. Valduga, G. Jori, J. C. Bommer, F. Elisei, L. Latterini and U. Mazzucato, Photochem. Photobiol., 2002, 75, 462–470.

    Article  CAS  PubMed  Google Scholar 

  5. E. Alves, L. Costa, C. M. B. Carvalho, J. P. C. Tomé, M. A. Faustino, M. G. P. M. S. Neves, A. C. Tomé, J. A. S. Cavaleiro, A. Cunha and A. Almeida, BMC Microbiol., 2009, 9, 70.

    Article  PubMed  PubMed Central  Google Scholar 

  6. L. Costa, M. A. F. Faustino, M. G. P. M. S. Neves, A. Cunha and A. Almeida, Viruses, 2012, 4, 1034–1074.

    Article  PubMed  PubMed Central  Google Scholar 

  7. V. Carré, O. Gaud, I. Sylvain, O. Bourdon, M. Spiro, J. Blais, R. Granet, P. Krausz and M. Guilloton, J. Photochem. Photobiol., B, 1999, 48, 57–62.

    Article  Google Scholar 

  8. J. S. Friedberg, C. Skema, E. D. Baum, J. Burdick, S. A. Vinogradov, D. F. Wilson, A. D. Horan and I. Nachamkin, J. Antimicrob. Chemother., 2001, 48, 105–107.

    Article  CAS  PubMed  Google Scholar 

  9. Z. Luksiene, D. Peciulyte and A. Lugauskas, Ann. Agric. Environ. Med., 2004, 11, 215–220.

    PubMed  Google Scholar 

  10. L. S. Peloi, C. E. G. Biondo, E. Kimura, M. J. Politi, M. V. C. Lonardoni, S. M. A. Aristides, R. C. C. Dorea, N. Hioka and T. G. V. Silveira, Exp. Parasitol., 2011, 128, 353–356.

    Article  CAS  PubMed  Google Scholar 

  11. K. Kassab, D. Dei, G. Roncucci, G. Jori and O. Coppellotti, Photochem. Photobiol. Sci., 2003, 2, 668–672.

    Article  CAS  PubMed  Google Scholar 

  12. A. Ceklovsky, Doctoral Dissertation, Slovak Academy of Sciences, 2009.

    Google Scholar 

  13. G. Jori, J. Environ. Pathol., Toxicol. Oncol., 2006, 25, 505–519.

    Article  Google Scholar 

  14. M. P. Cormick, M. G. Alvarez, M. Rovera and E. N. Durantini, Eur. J. Med. Chem., 2009, 44, 1592–1599.

    Article  CAS  PubMed  Google Scholar 

  15. D. A. Caminos and E. N. Durantini, J. Photochem. Photobiol., A, 2008, 198, 274–281.

    Article  CAS  Google Scholar 

  16. B. Chen, S. Wu, A. Li, F. Liang, X. Zhou, X. Cao and Z. He, Tetrahedron, 2006, 62, 5487–5497.

    Article  CAS  Google Scholar 

  17. S. A. G. Lambrechts, M. C. G. Aalders and J. Van Marle, Antimicrob. Agents Chemother., 2005, 49, 2026–2034.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. M. C. Gomes, S. M. W. Barreira, M. A. F. Faustino, R. Fernandes, M. G. P. M. S. Neves, A. C. Tom, N. C. M. Gomes, A. Almeida and P. C. Tom, Photochem. Photobiol. Sci., 2011, 10, 1735–1743.

    Article  CAS  PubMed  Google Scholar 

  19. E. Alves, M. A. F. Faustino, J. P. C. Tomé, M. G. P. M. S. Neves, A. C. Tomé, J. A. S. Cavaleiro, Â. Cunha, N. C. M. Gomes and A. Almeida, Bioorg. Med. Chem., 2013, 21, 4311–4318.

    Article  CAS  PubMed  Google Scholar 

  20. S. Beirão, S. Fernandes, J. Coelho, M. A. F. Faustino, J. P. C. Tomé, M. G. P. M. S. Neves, A. C. Tomé, A. Almeida and A. Cunha, Photochem. Photobiol., 2014, 90, 1387–1396.

    Article  PubMed  CAS  Google Scholar 

  21. K. Komagoe, H. Kato, T. Inoue and T. Katsu, Photochem. Photobiol. Sci., 2011, 10, 1181–1188.

    Article  CAS  PubMed  Google Scholar 

  22. M. C. Gonçalves-Vidigal, L. P. Bonett, P. S. V. Filho, A. Gonela and A. S. Ribeiro, Braz. Arch. Biol. Technol., 2007, 50, 579–586.

    Article  Google Scholar 

  23. E. D. Quiroga, M. P. Cormick, P. Pons, M. G. Alvarez and E. N. Durantini, Eur. J. Med. Chem., 2012, 58, 332–339.

    Article  CAS  PubMed  Google Scholar 

  24. W. A. Vargas, J. M. S. Martín, G. E. Rech, L. P. Rivera, E. P. Benito, J. M. Díaz-Mínguez, M. R. Thon and S. A. Sukno, Plant Physiol., 2012, 158, 1342–1358.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. C. Venard and L. Vaillancourt, Biochem. Cell Biol., 2007, 97, 438–447.

    CAS  Google Scholar 

  26. L. V. Cota, R. V. Costa, D. D. Silva, C. R. Casela and D. F. Parreira, J. Phytopathol., 2012, 160, 680–684.

    Article  Google Scholar 

  27. H. L. Warren, R. L. Nicholson, A. J. Ullstrup and E. G. Sharvelle, Plant Dis. Rep., 1973, 57, 143–144.

    Google Scholar 

  28. K. J. Leonard, Plant Dis. Rep., 1974, 58, 532–534.

    Google Scholar 

  29. N. P. Keller, G. C. Bergstrom and R. I. Carruthers, Phytopathology, 1986, 76, 586–589.

    Article  CAS  Google Scholar 

  30. R. M. S. Coêlho, H. P. Silva, K. R. Brunelli and L. E. A. Camargo, Fitopatol. Bras., 2001, 26, 640–643.

    Article  Google Scholar 

  31. M. A. Vizvary and H. L. Warren, Phytopathology, 1982, 72, 522–525.

    Article  Google Scholar 

  32. P. E. Lipps, Phytopathology, 1985, 75, 1212–1216.

    Article  Google Scholar 

  33. C. R. Casela, A. S. Ferreira and F. G. Santos, Fitopatol. Bras., 2001, 26, 217–219.

    Article  Google Scholar 

  34. M. L. F. Lima and M. Menezes, Fitopatol. Bras., 2002, 27, 12–16.

    Article  CAS  Google Scholar 

  35. R. V. Costa, L. V. Cota, D. D. Silva, D. F. Parreira, C. R. Casela, E. C. Landau and J. E. F. Figueiredo, Crop Prot., 2014, 56, 44–49.

    Article  Google Scholar 

  36. C. Avila-Adame, G. Olaya and W. Köller, Plant Dis., 2003, 87, 1426–1432.

    Article  CAS  PubMed  Google Scholar 

  37. J. A. Crouch, B. B. Clarke and B. I. Hillman, Int. Turfgrass Soc. Res. J., 2005, 10, 186–195.

    Google Scholar 

  38. W. L. Soares, Doctoral Dissertation, Escola Nacional de Saúde Pública Sergio Arouca, 2010.

    Google Scholar 

  39. P. G. Calzavara-Pinton, M. Venturini and R. Sala, J. Photochem. Photobiol., B, 2005, 78, 1–6.

    Article  CAS  Google Scholar 

  40. H. D. Menezes, G. B. Rodrigues, S. D. P. Teixeira, N. S. Massola, L. Bachmann, M. Wainwright and G. U. L. Braga, Appl. Environ. Microbiol., 2014, 80, 1623–1632.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  41. H. D. Menezes, A. C. Pereira, G. T. P. Brancini, H. C. de Leão, N. S. Massola Júnior, L. Bachmann, M. Wainwright, J. K. Bastos and G. U. L. Braga, J. Photochem. Photobiol., B, 2014, 131, 74–83.

    Article  CAS  Google Scholar 

  42. R. F. Donnelly, C. M. Cassidy, R. G. Loughlin, A. Brown, M. M. Tunney, M. G. Jenkins and P. A. McCarron, J. Photochem. Photobiol., B, 2009, 96, 223–231.

    Article  CAS  Google Scholar 

  43. A. Jurczak, B. Szramka, M. Grinholc, J. Legendziewicz and K. P. Bielawski, Acta Biochim. Pol., 2008, 55, 581–585.

    Article  CAS  PubMed  Google Scholar 

  44. M. Salmon-Divon, Y. Nitzan and Z. Malik, Photochem. Photobiol. Sci., 2004, 3, 423–429.

    Article  CAS  PubMed  Google Scholar 

  45. G. Valduga, B. Breda, G. M. Giacometti, G. Jori and E. Reddi, Biochem. Biophys. Res. Commun., 1999, 256, 84–88.

    Article  CAS  PubMed  Google Scholar 

  46. M. Merchat, J. D. Spikes, G. Bertoloni and G. Jori, J. Photochem. Photobiol., B, 1996, 35, 149–157.

    Article  CAS  Google Scholar 

  47. Y. Chabrier-Roselló, B. R. Giesselman, F. J. Jesús-Andino, T. H. Foster, S. Mitra and C. G. Haidaris, J. Photochem. Photobiol., B, 2010, 99, 117–125.

    Article  CAS  Google Scholar 

  48. S. Mitra, C. G. Haidaris, S. B. Snell, B. R. Giesselman, S. M. Hupcher and T. H. Foster, Lasers Surg. Med., 2011, 43, 324–332.

    Article  PubMed  PubMed Central  Google Scholar 

  49. E. D. Quiroga, M. G. Alvarez and E. N. Durantini, FEMS Immunol. Med. Microbiol., 2010, 60, 123–131.

    Article  CAS  PubMed  Google Scholar 

  50. S. C. Zimmerman, I. Zharov, M. S. Wendland, N. A. Rakow and K. S. Suslick, J. Am. Chem. Soc., 2003, 125, 13504–13518.

    Article  CAS  PubMed  Google Scholar 

  51. C. Casas, B. Saint-Jalmes, C. Loup, C. J. Lacey and B. Meunier, J. Org. Chem., 1993, 58, 2913–2917.

    Article  CAS  Google Scholar 

  52. G. G. Meng, B. R. James, K. A. Skov and M. Korbelik, Can. J. Chem., 1994, 72, 2447.

    Article  CAS  Google Scholar 

  53. G. Z. G. Meng, B. R. James and K. A. Skov, Can. J. Chem., 1994, 72, 1894–1909.

    Article  CAS  Google Scholar 

  54. N. G. Angeli, M. G. Lagorio, E. A. San Román and L. E. Dicelio, Photochem. Photobiol., 2000, 72, 49–56.

    Article  CAS  PubMed  Google Scholar 

  55. C. Simões, M. C. Gomes, M. G. P. M. S. Neves, Â. Cunha, J. P. C. Tomé, A. C. Tomé, J. A. S. Cavaleiro, A. Almeida and M. A. F. Faustino, Catal. Today, 2016, 266, 197–204.

    Article  CAS  Google Scholar 

  56. D. Kessel, R. Luguya and M. G. H. Vicente, Photochem. Photobiol., 2003, 78, 431–435.

    Article  CAS  PubMed  Google Scholar 

  57. J. C. C. Dallagnol, D. R. B. Ducatti, S. M. W. Barreira, M. D. Noseda, M. E. R. Duarte and A. G. Gonçalves, Dyes Pigm., 2014, 107, 69–80.

    Article  CAS  Google Scholar 

  58. F. Engelmann, S. V. O. Rocha, H. E. Toma, K. Araki and M. S. Baptista, Int. J. Pharm., 2007, 329, 12–18.

    Article  CAS  PubMed  Google Scholar 

  59. A. Lazzaro, M. Corominas, C. Martí, C. Flors, L. R. Izquierdo, T. A. Grillo, J. G. Luis and S. Nonell, Photochem. Photobiol. Sci., 2004, 3, 706–710.

    Article  CAS  PubMed  Google Scholar 

  60. D. Mares, B. Tosi, F. Poli, E. Andreotti and C. Romagnoli, Microbiol. Res., 2004, 159, 295–304.

    Article  CAS  PubMed  Google Scholar 

  61. S. E. Binns, B. Purgina, C. Bergeron, M. L. Smith, L. Ball, B. R. Baum and J. T. Arnason, Planta Med., 2000, 66, 241–244.

    Article  CAS  PubMed  Google Scholar 

  62. K. K. Niyogi, Annu. Rev. Plant Physiol. Plant Mol. Biol., 1999, 50, 333–359.

    Article  CAS  PubMed  Google Scholar 

  63. D. A. Dalton, S. A. Russell, F. J. Hanus, G. A. Pascoe and H. J. Evans, Proc. Natl. Acad. Sci. U. S. A., 1986, 83, 3811–3815.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. K. K. Niyogi, O. Björkman and A. R. Grossman, Proc. Natl. Acad. Sci. U. S. A., 1997, 94, 14162–14167.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. F. M. Engelmann, I. Mayer, D. S. Gabrielli, H. E. Toma, A. J. Kowaltowski, K. Araki and M. S. Baptista, J. Bioenerg. Biomembr., 2007, 39, 175–185.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Departamento de Farmácia, Universidade Federal do Paraná, Av. Lothário Meissner, 3400, Jardim Botânico, Curitiba, Paraná, Brazil

    Camila Chevonica Vandresen, Alan Guilherme Gonçalves, Fabio Seigi Murakami & Sandra Mara Woranovicz Barreira

  2. Departamento de Bioquímica e Biologia Molecular, Universidade Federal do Paraná, PO Box, 19046, Curitiba, Paraná, Brazil

    Diogo Ricardo Bazan Ducatti, Miguel Daniel Noseda & Maria Eugenia Rabello Duarte

Authors
  1. Camila Chevonica Vandresen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alan Guilherme Gonçalves
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Diogo Ricardo Bazan Ducatti
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fabio Seigi Murakami
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Miguel Daniel Noseda
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Maria Eugenia Rabello Duarte
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Sandra Mara Woranovicz Barreira
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sandra Mara Woranovicz Barreira.

Additional information

Electronic supplementary information (ESI) available. See DOI: 10.1039/c5pp00372e

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vandresen, C.C., Gonçalves, A.G., Ducatti, D.R.B. et al. In vitro photodynamic inactivation of conidia of the phytopathogenic fungus Colletotrichum graminicola with cationic porphyrins. Photochem Photobiol Sci 15, 673–681 (2016). https://doi.org/10.1039/c5pp00372e

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1039/c5pp00372e

Search

Navigation