Plant Protect. Sci., 2020, 56(2):74-82 | DOI: 10.17221/102/2019-PPS

Effect of photosensitisers on growth and morphology of Phytophthora citrophthora coupled with leaf bioassays in pear seedlingsOriginal Paper

Antonios Zambounis*,1, Oksana Sytar2, Dimitris Valasiadis3, Zoe Hilioti*,3
1 Institute of Plant Breeding and Genetic Resources, Department of Deciduous Fruit Trees, Hellenic Agricultural Organization, Naoussa, Greece
2 Institute of Biology, Department of Plant Physiology and Ecology, Taras Shevchenko National University of Kyiv, Kyiv, Ukraine
3 Institute of Applied Biosciences, Center for Research & Technology (CERTH), Thessaloniki, Greece

The phytopathogenic oomycetes of the genus Phytophthora cause devastating economic losses worldwide. Naphthodianthrone compounds, present in plant extracts of buckwheat and Saint John's wort act as photosensitiser agents and exhibit antimicrobial activity against a number of pathogens. In this study, we investigated the potential inhibitory effects of fagopyrin and hypericin on Phytophthora citrophthora (R.E. Sm. & E.H. Sm.) Leonian 1906, the main causal agent of rot diseases in deciduous trees. Fagopyrin had the highest inhibitory effect in the colony growth at a concentration of 2% of a stock solution (3 mg/mL), inducing clubbed hyphae with round tips. Notably, hypericin also inhibited the radial colony growth and increased the hyphal branching at the subapical region, while also promo­ting the formation of enlarged cells with irregular shapes growing collectively as biofilm-like structures. In terms of the mycelial dry weight, although both photosensitisers had considerable inhibitory effects, the fagopyrin treatment was most effective. Leaf bioassays showed that under dark conditions the photosensitiser pre-treated zoospores formed a dense, but aberrant, mycelial growth with penetration defects. In contrast, when the zoospore production was perfor­med under light conditions, the zoospores failed to cause necrotic lesions and penetration events implying that their virulence was impaired. These findings shed light on the biological effects of fagopyrin and hypericin in the regulation of the mycelial growth, morphology and pathogenicity of P. citrophthora.

Keywords: crop protection; hypericin; hyphal morphology; oomycetes; phytochemicals; plant-microbe interactions

Published: June 30, 2020  Show citation

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Zambounis A, Sytar O, Valasiadis D, Hilioti Z. Effect of photosensitisers on growth and morphology of Phytophthora citrophthora coupled with leaf bioassays in pear seedlings. Plant Protect. Sci. 2020;56(2):74-82. doi: 10.17221/102/2019-PPS.
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References

  1. Agostinis P., Donella-Deana A., Cuveele J., Vandenbogaerde A., Sarno S., Merlevede W., Witte P. (1996): A Comparative analysis of the photosensitized inhibition of growth-factor regulated protein kinases by hypericin-derivatives. Biochemical and Biophysical Research Communications, 220: 613-617. Go to original source... Go to PubMed...
  2. Bilia R., Bergonzi C., Morgenni F., Mazzi G.,Vincieri F. (2001): Evaluation of chemical stability of St. John's wort commercial extract and some preparations. International Journal of Pharmaceutics, 213: 199-208. Go to original source... Go to PubMed...
  3. Bilkis I., Silman I., Weiner L. (2018): Generation of reactive oxygen species by photosensitizers and their modes of action on proteins. Current Medicinal Chemistry, 25: 5528-5539. Go to original source... Go to PubMed...
  4. Blair E., Coffey D., Park Y., Geiser M., Kang S. (2008): A multi-locus phylogeny for Phytophthora utilizing markers derived from complete genome sequences. Fungal Genetics and Biology, 45: 266-277. Go to original source... Go to PubMed...
  5. Borges A., Abreu C., Dias C., Saavedra J., Borges F., Simões M. (2016): New perspectives on the use of phytochemicals as an emergent strategy to control bacterial infections including biofilms. Molecules, 21: 877-918. Go to original source... Go to PubMed...
  6. Bush A., Stromberg L., Hong C., Richardson A., Kong P. (2006): Illustration of key morphological characteristics of Phytophthora species identified in Virginia nursery irrigation water. Plant Health Progress, 7: 1-12. Go to original source...
  7. Cacciola O., Lio M. di S. (2008): Management of Citrus diseases caused by Phytophthora spp. In: Ciancio A., Mukerji K.G. (eds): Integrated Management of Diseases Caused by Fungi, Phytoplasma and Bacteria. Dordrecht, Springer: 61-84. Go to original source...
  8. Díaz K., Espinoza J., Espinoza L., González C., Madrid A. (2018): Labdanes: antifungal compounds isolates from the resinous exudate of Madia sativa against Phytophthora cinnamomi Rands. Natural Product Research, 25: 1-5. Go to original source... Go to PubMed...
  9. Elena K., Paplomatas E. (1999): Collar rot caused by Phytophthora citrophthora on pear trees in Greece. Phytoparasitica, 27: 291-298. Go to original source...
  10. Harding W., Marques R., Howard J., Olson E. (2010): Biofilm morphologies of plant pathogenic fungi. The Americas Journal of Plant Science and Biotechnology, 4: 43-47. Go to original source...
  11. Huang C., Shen M., Huang Y.J., Lin H.C., Chen C.T. (2018): Photodynamic inactivation potentiates the susceptibility of antifungal agents against the planktonic and biofilm cells of Candida albicans. International Journal of Molecular Sciences, 19: 434-446. Go to original source... Go to PubMed...
  12. Jendželovská Z., Jendželovský R., Kuchárová B., Fedoročko P. (2016): Hypericin in the light and in the dark: two sides of the same coin. Frontiers in Plant Science, 7: 1-20. Go to original source... Go to PubMed...
  13. Krebs H., Dorn B., Forrer H.R. (2006): Control of late blight of potato with medicinal plant suspensions. Agrarforschung, 13: 16-21.
  14. Larousse M., Govetto B., Séassau A., Etienne C., Industri B., Theodorakopoulos N., Deleury E., Ponchet M., Panabières F., Galiana E. (2014): Characterization of PPMUCL1/2/3, Three members of a new oomycete-specific mucin-like protein family residing in Phytophthora parasitica biofilm. Protist, 165: 275-292. Go to original source... Go to PubMed...
  15. Martin F.N., Blair J.E., Coffey M.D. (2014): A combined mitochondrial and nuclear multilocus phylogeny of the genus Phytophthora. Fungal Genetics and Biology, 66: 19-32. Go to original source... Go to PubMed...
  16. Nakajima N., Kawashima N. (2012): A basic study on hypericin-PDT in vitro. Photodiagnosis and Photodynamic Therapy, 9: 196-203. Go to original source... Go to PubMed...
  17. Nielsen C.J., Ferrin D.M., Stanghellini M.E. (2006): Cyclic production of sporangia and zoospores by Phytophthora capsici on pepper roots in hydroponic culture. Canadian Journal of Plant Pathology, 28: 461-466. Go to original source...
  18. Pane A., Cacciola S., Scibetta S., Bentivenga G., Magnano di San Lio G. (2009): Four Phytophthora species causing foot and root rot of apricot in Italy. Plant Disease, 93: 844-845. Go to original source... Go to PubMed...
  19. Peiqian L., Xiaoming P., Huifang S., Jingxin Z., Ning H., Birun L. (2014): Biofilm formation by Fusarium oxysporum f. sp. cucumerinum and susceptibility to environmental stress. FEMS Microbiology Letters, 350: 138-145. Go to original source... Go to PubMed...
  20. Rieger P.H., Liermann J.C., Opatz T., Anke H., Thines E. (2010): Caripyrin, a new inhibitor of infection-related morphogenesis in the rice blast fungus Magnaporthe oryzae. Journal of Antibiotics, 63: 285-289. Go to original source... Go to PubMed...
  21. Semighini P., Harris D. (2008): Regulation of apical dominance in Aspergillus nidulans hyphae by reactive oxygen species. Genetics, 179: 1919-1932. Go to original source... Go to PubMed...
  22. Simonetti G., Tocci N., Valletta A., Brasili E., D'Auria F. D., Idoux A., Pasqua G. (2016): In vitro antifungal activity of extracts obtained from Hypericum perforatum adventitious roots cultured in a mist bioreactor against planktonic cells and biofilm of Malassezia furfur. Natural Product Research, 30: 544-550. Go to original source... Go to PubMed...
  23. Stephan D., Koch E. (2002): Screening of plant extracts, microrganisms and commercial prepartions for biocontrol of Phytophthora infestans on detached potato leaves. Bulletin OILB/SROP, 25: 341-394.
  24. Süntar I., Oyardi O., Akkol E.K., Ozçelik B. (2016): Antimicrobial effect of the extracts from Hypericum perforatum against oral bacteria and biofilm formation. Pharmaceutical Biology, 54: 1065-1070. Go to original source... Go to PubMed...
  25. Sytar O., Švedienė J., Ložienė K., Paškevičius A., Kosyan A., Taran N. (2016): Antifungal properties of hypericin, hypericin tetrasulphonic acid and fagopyrin on pathogenic fungi and spoilage yeasts. Pharmaceutical Biology, 54: 3121-3125. Go to original source... Go to PubMed...
  26. Villacorta R.B., Roque K.F.J., Tapang G.A., Jacinto S.D. (2017): Plant extracts as natural photosensitizers in photodynamic therapy: in vitro activity against human mammary adenocarcinoma MCF-7 cells. Asian Pacific Journal of Tropical Biomedicine, 7: 358-366. Go to original source...
  27. Yanar Y., Kadioğlu I., Gökçe A., Demirtaş B., Gören N., Cam H., Whalon M. (2011): In vitro antifungal activities of 26 plant extracts on mycelial growth of Phytophthora infestans (Mont.) de Bary. African Journal of Biotechnology, 10: 2625-2629. Go to original source...
  28. Yang X., Tyler B.M., Hong C. (2017): An expanded phylogeny for the genus Phytophthora. IMA Fungus, 8: 355-384. Go to original source... Go to PubMed...
  29. Yow C.M.N., Tang H.M., Chu E.S.M., Huang, Z. (2012): Hypericin-mediated photodynamic antimicrobial effect on clinically isolated pathogens. Photochemistry and Photobiology, 88: 626-632. Go to original source... Go to PubMed...

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