DOI QR코드

DOI QR Code

Control of oomycete pathogens during Pyropia farming and processing using calcium propionate

  • Yong Tae Kim (Department of Biology, Kongju National University) ;
  • Ro-won Kim (Biotechnology Research Institute, Kongju National University) ;
  • Eunyoung Shim (Biotechnology Research Institute, Kongju National University) ;
  • Hana Park (Department of Biology, Kongju National University) ;
  • Tatyana A. Klochkova (Department of Biology, Kamchatka State Technical University) ;
  • Gwang Hoon Kim (Department of Biology, Kongju National University)
  • Received : 2023.02.02
  • Accepted : 2023.03.08
  • Published : 2023.03.15

Abstract

The oomycete pathogens Pythium porphyrae, causing red rot disease, and Olpidiopsis spp. causing Olpidiopsis-blight, cause serious economic losses to Pyropia sea farms in Korea. During the washing step for Pyropia processing, these pathogens proliferate rapidly, significantly reducing the quality of the final product. To develop non-acidic treatments for these pathogens, various calcium salts were tested against the infectivity of P. porphyrae and Olpidiopsis pyropiae on Pyropia gametophytes, and calcium propionate was the most effective. When Pyropia blades were immersed in 10 mM calcium propionate for 1 h after inoculation with the oomycete pathogen, infection rate of both oomycete pathogens on day 2 was significantly lower (7.1%) than control (>95%). Brief incubation of Pyropia blades in calcium propionate also reduced the spread of infection. The infected area of Pyropia thallus was reduced to 14.3% of the control in 2 days after treatment with 100 mM calcium propionate for 30 s. In field experiments conducted in actual aquaculture farms, it has been shown that a brief 30 s wash every two weeks with 100 mM calcium propionate can effectively reduce the spread of oomycetes throughout the entire culture period. The above results suggest that calcium propionate can be a useful means for controlling the spread of oomycetes not only during laver processing but also during aquaculture.

Keywords

Acknowledgement

This work was supported by the management of Marine Fishery Bio-resources Center (2023) funded by the National Marine Biodiversity Institute of Korea (MABIK) and by Development of technology for biomaterialization of marine fisheries by-products of Korea institute of Marine Scinece & Technology Promotion (KIMST) funded by the Ministry of Oceans and Fisheries (KIMST-20220128) and the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (NRF-2022R1A2C1091633).

References

  1. Addepalli, M. K. & Fujita, Y. 2002. Regulatory role of external calcium on Pythium porphyrae (Oomycota) zoospore release, development and infection in causing red rot disease of Porphyra yezoensis (Rhodophyta). FEMS Microbiol. Lett. 211:253-257. https://doi.org/10.1111/j.1574-6968.2002.tb11233.x
  2. Aldon, D., Mbengue, M., Mazars, C. & Galaud, J. -P. 2018. Calcium signaling in plant biotic interactions. Int. J. Mol. Sci. 19:665.
  3. Arasaki, S. 1947. Studies on the rot of Porphyra tenera by Pythium. Nippon Suisan Gakkaishi 13:74-90. https://doi.org/10.2331/suisan.13.74
  4. Arasaki, S., Akino, K. & Tomiyama, T. 1968. A comparison of some physiological aspects in a marine Pythium on the host and on the artificial medium. Bull. Misaki Mar. Biol. Inst. Kyoto Univ. 12:203-206.
  5. Badis, Y., Han, J. W., Klochkova, T. A., Gachon, C. M. M. & Kim, G. H. 2020a. The gene repertoire of Pythium porphyrae (Oomycota) suggests an adapted plant pathogen tackling red algae. Algae 35:133-144. https://doi.org/10.4490/algae.2020.35.6.4
  6. Badis, Y., Klochkova, T. A., Brakel, J., Arce, P., Ostrowski, M., Tringe, S. G., Kim, G. H. & Gachon, C. M. M. 2020b. Hidden diversity in the oomycete genus Olpidiopsis is a potential hazard to red algal cultivation and conservation worldwide. Eur. J. Phycol. 55:162-171. https://doi.org/10.1080/09670262.2019.1664769
  7. Badis, Y., Klochkova, T. A., Strittmatter, M., Garvetto, A., Murua, P., Sanderson, J. C., Kim, G. H. & Gachon, C. M. M. 2018. Novel species of the oomycete Olpidiopsis potentially threaten European red algal cultivation. J. Appl. Phycol. 31:1239-1250. https://doi.org/10.1007/s10811-018-1641-9
  8. Biggs, A. R., El-Kholi, M. M., El-Neshawy, S. & Nickerson, R. 1997. Effects of calcium salts on growth, polygalacturonase activity, and infection of peach fruit by Monilinia fructicola. Plant Dis. 81:399-403. https://doi.org/10.1094/PDIS.1997.81.4.399
  9. Brunelli, A. 1995. I prodotti naturali nella lotta alle malattie fungine. La Difesa delle Piante 18:57-69.
  10. Campanella, V., Ippolito, A. & Nigro, F. 2002. Activity of calcium salts in controlling Phytophthora root rot of citrus. Crop Prot. 21:751-756. https://doi.org/10.1016/S0261-2194(02)00032-7
  11. Cho, Y. C. & Chang, J. W. 1986. On the disease occurrence of cultured laver (Porphyra tenera Kjellman form. tamatsuensis Miura), and production at the Nokdong laver farming area. Bull. Nat. Fish. Res. Dev. Agency 39:111-125.
  12. Cottier-Cook, E. J., Nagabhatla, N., Asri, A., Beveridge, M., Bianchi, P., Bolton, J., Bondad-Reantaso, M. G., Brodie, J., Buschmann, A. H., Cabarubias, J., Campbell, I., Chopin, T., Critchley, A. T., De Lombaerde, P., Doumeizel, V., Gachon, C. M. M., Hayashi, L., Hewitt, C. L., Huang, J., Hurtado, A., Kambey, C., Kim, G. H., Masson, V., Lim, P. E., Liu, T., Malin, G., Matoju, I., Montalescot, V., Msuya, F. E., Potin, P., Puspita, M., Qi, Z., Shaxson, L., Pinto, I. S., Stentiford, G. D., Suyo, J. & Yarish, C. 2021. Ensuring the sustainable future of the rapidly expanding global seaweed aquaculture industry: a vision. United Nations University (Institute on Comparative Regional Integration Studies) and Scottish Association for Marine Science, Hamilton, ON, 14 pp.
  13. Cottier-Cook, E. J., Nagabhatla, N., Badis, Y., Campbell, M., Chopin, T., Dai, W., Fang, J., He, P., Hewitt, C., Kim, G. H., Huo, Y., Jiang, Z., Kema, G., Li, X., Liu, F., Liu, H., Liu, Y., Lu, Q., Luo, Q., Mao, Y., Msuya, F. E., Rebours, C., Shen, H., Stentiford, G. D., Yarish, C., Wu, H., Yang, X., Zhang, J., Zhou, Y. & Gachon, C. M. M. 2016. Safeguarding the future of the global seaweed aquaculture industry. United Nations University (Institute for Water, Environment and Health) and Scottish Association for Marine Science, Hamilton, ON, 12 pp.
  14. Diehl, N., Kim, G. H. & Zuccarello, G. C. 2017. A pathogen of New Zealand Pyropia plicata (Bangiales, Rhodophyta), Pythium porphyrae (Oomycota). Algae 32:29-39. https://doi.org/10.4490/algae.2017.32.2.25
  15. Ding, H. & Ma, J. 2005. Simultaneous infection by red rot and chytrid diseases in Porphyra yezoensis Ueda. J. Appl. Phycol. 17:51-56. https://doi.org/10.1007/s10811-005-5523-6
  16. EFSA Panel on Food Additives and Nutrient Sources Added to Food (ANS). 2014. Scientific opinion on the re-evaluation of propionic acid (E280), sodium propionate (E281), calcium propionate (E282) and potassium propionate (E283) as food additives. EFSA J. 12:3779.
  17. Fletcher, K., Uljevic, A., Tsirigoti, A., Antolic, B., Katsaros, C., Nikolic, V., van West, P. & Kupper, F. C. 2015. New record and phylogenetic affinities of the oomycete Olpidiopsis feldmanni infecting Asparagopsis sp. (Rhodophyta). Dis. Aquat. Organ. 117:45-57. https://doi.org/10.3354/dao02930
  18. Fujita, Y. & Migita, S. 1980. Death of parasitic Pythium porphyrae by drying and freeze-preservation of red rot infected thalli of Porphyra yezoensis. Bull. Fac. Fish. Nagasaki Univ. 49:11-16.
  19. Fujita, Y. & Zenitani, B. 1977. Studies on pathogenic Pythium of laver red rot in Ariake Sea farm. 2. Experimental conditions and nutritional requirements for growth. Bull. Jpn. Soc. Sci. Fish. 43:89-95. https://doi.org/10.2331/suisan.43.89
  20. Furia, T. E. 1973. CRC handbook of food additives. CRC Press, Cleveland, OH, 1240 pp.
  21. Im, S. H., Klochkova, T. A., Lee, D. J., Gachon, C. M. M. & Kim, G. H. 2019. Genetic toolkits of the red alga Pyropia tenera against the three most common diseases in Pyropia farms. J. Phycol. 55:801-815. https://doi.org/10.1111/jpy.12857
  22. Kaiser, C., Hamm, P. B., Gieck, S., David, N., Long, L., Meland, M. & Christensen, J. M. 2011. In vitro fungicidal activity of calcium and potassium salts on several commercially significant plant pathogens. HortScience 46:913-916. https://doi.org/10.21273/HORTSCI.46.6.913
  23. Kim, G. H., Klochkova, T. A., Lee, D. J. & Im, S. H. 2016. Chloroplast virus causes green-spot disease in cultivated Pyropia of Korea. Algal Res. 17:293-299. https://doi.org/10.1016/j.algal.2016.05.023
  24. Kim, G. H., Moon, K. -H., Kim, J. -Y., Shim, J. & Klochkova, T. A. 2014. A revaluation of algal diseases in Korean Pyropia (Porphyra) sea farms and their economic impact. Algae 29:249-265. https://doi.org/10.4490/algae.2014.29.4.249
  25. Klochkova, T. A., Jung, S. & Kim, G. H. 2017. Host range and salinity tolerance of Pythium porphyrae may indicate its terrestrial origin. J. Appl. Phycol. 29:371-379. https://doi.org/10.1007/s10811-016-0947-8
  26. Klochkova, T. A., Shim, J. B., Hwang, M. S. & Kim, G. H. 2012. Host-parasite interactions and host sepecies susceptibility of the marine oomycete parasite, Olpidiopsis sp., from Korea that infects red algae. J. Appl. Phycol. 24:135-144. https://doi.org/10.1007/s10811-011-9661-8
  27. Klochkova, T. A., Shin, Y. J., Moon, K. -H., Motomura, T. & Kim, G. H. 2016. New species of unicellular obligate parasite, Olpidiopsis pyropiae sp. nov., that plagues Pyropia sea farms in Korea. J. Appl. Phycol. 28:73-83. https://doi.org/10.1007/s10811-015-0595-4
  28. Kwak, M. S., Klochkova, T. A., Jeong, S. & Kim, G. H. 2017. Olpidiopsis porphyrae var. koreanae, an endemic endo-parasite infecting cultivated Pyropia yezoensis in Korea. J. Appl. Phycol. 29:2003-2012. https://doi.org/10.1007/s10811-017-1109-3
  29. Mo, Z., Li, S., Kong, F., Tang, X. & Mao, Y. 2016. Characterization of a novel fungal disease that infects the gametophyte of Pyropia yezoensis (Bangiales, Rhodophyta). J. Appl. Phycol. 28:395-404. https://doi.org/10.1007/s10811-015-0539-z
  30. Nigro, F., Ippolito, A., Ligorio, A. & Romanazzi, G., 1997. In vitro and in vivo effectiveness of different salts toward Botrytis storage rot of table grapes. In Preliminary results. Proceedings of the COST914-COST 915 on Non Conventional Methods for the Control of Post-harvest Disease and Microbiological Spoilage. COST Association, Brussels, pp. 175-180.
  31. Park, C. S., Kakinuma, M. & Amano, H. 2001. Detection and quantitative analysis of zoospores of Pythium porphyrae, causative organism of red rot disease in Porphyra, by competitive PCR. J. Appl. Phycol. 13:433-441. https://doi.org/10.1023/A:1011982105124
  32. Park, C. S., Sakaguchi, K., Kakinuma, M. & Amano, H. 2000. Comparison of electrophoretic patterns of soluble proteins and isozymes of the red rot disease fungus Pythium sp. isolated from Porphyra yezoensis from Korea and Japan. Fish. Sci. 66:1158-1162. https://doi.org/10.1046/j.1444-2906.2000.00183.x
  33. Sekimoto, S., Klochkova, T. A., West, J. A., Beakes, G. W. & Honda, D. 2009. Olpidiopsis bostrychiae sp. nov.: an endoparasitic oomycete that infects Bostrychia and other red algae (Rhodophyta). Phycologia 48:460-472. https://doi.org/10.2216/08-11.1
  34. Sekimoto, S., Yokoo, K., Kawamura, Y. & Honda, D. 2008. Taxonomy, molecular phylogeny, and ultrastructural morphology of Olpidiopsis porphyrae sp. nov. (Oomycetes, straminipiles), a unicellular obligate endoparasite of Bangia and Porphyra spp. (Bangiales, Rhodophyta). Mycol. Res. 112:361-374. https://doi.org/10.1016/j.mycres.2007.11.002
  35. Takahashi, M., Ichitani, T. & Sasaki, M. 1977. Pythium porphyrae Takahashi et Sasaki, sp. nov. causing red rot of marine algae Porphyra spp. Trans. Mycol. Soc. Jpn. 18:279-285.
  36. Turkkan, M. 2013. Antifungal effect of various salts against Fusarium oxysporum f.sp. cepae, the causal agent of Fusarium basal rot of Onion. J. Agric. Sci. 19:178-187.
  37. Uppalapati, S. R. & Fujita, Y. 2000. Carbohydrate regulation of attachment, encystment and appressorium formation by Pythium porphyrae (Oomycota) zoospores on Porphyra yezoensis (Rhodophyta). J. Phycol. 36:359-366. https://doi.org/10.1046/j.1529-8817.2000.99099.x
  38. West, J. A., Klochkova, T. A., Kim, G. H. & Goer, S. L. 2006. Olpidiopsis sp., an oomycete from Madagascar that infects Bostrychia and other red algae: host species susceptibility. Phycol. Res. 54:72-85. https://doi.org/10.1111/j.1440-1835.2006.00410.x
  39. Zhang, L., Du, L. & Poovaiah, B. W. 2014. Calcium signaling and biotic defense responses in plants. Plant Signal Behav. 9:e973818.
  40. Zuccarello, G. C., Wen, X. & Kim, G. H. 2022. Splitting blades: why genera need to be more carefully defined; the case for Pyropia (Bangiales, Rhodophyta). Algae 37:205-211. https://doi.org/10.4490/algae.2022.37.9.11