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

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

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.

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. https://doi.org/10.1006/bbrc.1996.0451
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. https://doi.org/10.1016/S0378-5173(00)00660-8
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. https://doi.org/10.2174/0929867325666180104153848
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.  https://doi.org/10.1016/j.fgb.2007.10.010
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.  https://doi.org/10.3390/molecules21070877
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.  https://doi.org/10.1094/PHP-2006-0621-01-RS
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.
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. https://doi.org/10.1080/14786419.2018.1531402
Elena K., Paplomatas E. (1999): Collar rot caused by Phytophthora citrophthora on pear trees in Greece. Phytoparasitica, 27: 291–298.  https://doi.org/10.1007/BF02981485
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.
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.  https://doi.org/10.3390/ijms19020434
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.  https://doi.org/10.3389/fpls.2016.00560
Krebs H., Dorn B., Forrer H.R. (2006): Control of late blight of potato with medicinal plant suspensions. Agrarforschung, 13: 16–21.
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. https://doi.org/10.1016/j.protis.2014.03.003
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.  https://doi.org/10.1016/j.fgb.2014.02.006
Nakajima N., Kawashima N. (2012): A basic study on hypericin-PDT in vitro. Photodiagnosis and Photodynamic Therapy, 9: 196–203.  https://doi.org/10.1016/j.pdpdt.2012.01.008
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. https://doi.org/10.1080/07060660609507320
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. https://doi.org/10.1094/PDIS-93-8-0844C
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.  https://doi.org/10.1111/1574-6968.12310
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. https://doi.org/10.1038/ja.2010.31
Semighini P., Harris D. (2008): Regulation of apical dominance in Aspergillus nidulans hyphae by reactive oxygen species. Genetics, 179: 1919–1932. https://doi.org/10.1534/genetics.108.089318
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.  https://doi.org/10.1080/14786419.2015.1028059
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.
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.  https://doi.org/10.3109/13880209.2015.1102948
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.  https://doi.org/10.1080/13880209.2016.1211716
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.  https://doi.org/10.1016/j.apjtb.2017.01.025
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. https://doi.org/10.5897/AJB10.1219
Yang X., Tyler B.M., Hong C. (2017): An expanded phylogeny for the genus Phytophthora. IMA Fungus, 8: 355–384.  https://doi.org/10.5598/imafungus.2017.08.02.09
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. https://doi.org/10.1111/j.1751-1097.2012.01085.x
download PDF

© 2022 Czech Academy of Agricultural Sciences | Prohlášení o přístupnosti