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The Korean Society of Phycology (한국조류학회(藻類))
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Oomycete pathogens, red algal defense mechanisms and control measures

  • Xianying Wen (Department of Biological Sciences, Kongju National University) ;
  • Giuseppe C. Zuccarello (School of Biological Sciences, Victoria University of Wellington) ;
  • Tatyana A. Klochkova (Department of Biology, Kamchatka State Technical University) ;
  • Gwang Hoon Kim (Department of Biological Sciences, Kongju National University)
  • Received : 2023.11.12
  • Accepted : 2023.12.13
  • Published : 2023.12.21
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Abstract

Oomycete pathogens are one of the most serious threats to the rapidly growing global algae aquaculture industry but research into how they spread and how algae respond to infection is unresolved, let alone a proper classification of the pathogens. Even the taxonomy of the genera Pythium and Olpidiopsis, which contain the most economically damaging pathogens in red algal aquaculture, and are among the best studied, needs urgent clarification, as existing morphological classifications and molecular evidence are often inconsistent. Recent studies have reported a number of genes involved in defense responses against oomycete pathogens in red algae, including pattern-triggered immunity and effector-triggered immunity. Accumulating evidence also suggests that calcium-mediated reactive oxygen species signaling plays an important role in the response of red algae to oomycete pathogens. Current management strategies to control oomycete pathogens in aquaculture are based on the high resistance of red algae to abiotic stress, these have environmental consequences and are not fully effective. Here, we compile a revised list of oomycete pathogens known to infect marine red algae and outline the current taxonomic situation. We also review recent research on the molecular and cellular responses of red algae to oomycete infection that has only recently begun, and outline the methods currently used to control disease in the field.

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 the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (NRF-2022R1A2C1091633) and the development of technology for biomaterialization of marine fisheries by-products of Korea institute of Marine Science & Technology Promotion (KIMST) funded by the Ministry of Oceans and Fisheries (KIMST-20220128). The sample of Dasysiphonia japonica used in this study was obtained from the culture collection of the National Marine Biodiversity Institute of Korea (MABIK) (No. KNU000166).

References

  1. Adl, S. M., Bass, D., Lane, C. E., Lukes, J., Schoch, C. L., Smirnov, A., Agatha, S., Berney, C., Brown, M. W., Burki, F., Cardenas, P., Cepicka, I., Chistyakova, L., Del Campo, J., Dunthorn, M., Edvardsen, B., Eglit, Y., Guillou, L., Hampl, V., Heiss, A. A., Hoppenrath, M., James, T. Y., Karnkowska, A., Karpov, S., Kim, E., Kolisko, M., Kudryavtsev, A., Lahr, D. J. G., Lara, E., Le Gall, L., Lynn, D. H., Mann, D. G., Massana, R., Mitchell, E. A. D., Morrow, D., Park, J. S., Pawlowski, J. W., Powell, M. J., Richter, D. J., Rueckert, S., Shadwick, L., Shimano, S., Spiegel, F. W., Torruella, G., Youssef, N., Zlatogursky, V. & Zhang, Q. 2019. Revisions to the classification, nomenclature, and diversity of eukaryotes. J. Eukaryot. Microbiol. 66:4-119. https://doi.org/10.1111/jeu.12691
  2. Aleem, A. A. 1952. Olpidiopsis feldmannii sp. nov., Champignon marin parasite d'Algues de la famille des Bonnemaisoniacees. C. R. Acad. Sci. Paris 235:1250-1252.
  3. Arasaki, S. 1947. Studies on the rot of Porphyra tenera by a Pythium. Nippon Suisan Gakkaishi 13:74-90. (in Japanese) https://doi.org/10.2331/suisan.13.74
  4. Badis, Y., Klochkova, T. A., Brakel, J., Arce, P., Ostrowski, M., Tringe, S. G., Kim, G. H. & Gachon, C. M. M. 2020. 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
  5. Badis, Y., Klochkova, T. A., Strittmatter, M., Garvetto, A., Murua, P., Sanderson, J. C., Kim, G. H. & Gachon, C. M. M. 2019. 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
  6. Bari, R. & Jones, J. D. G. 2009. Role of plant hormones in plant defence responses. Plant Mol. Biol. 69:473-488. https://doi.org/10.1007/s11103-008-9435-0
  7. Beakes, G. W., Glockling, S. L. & Sekimoto, S. 2012. The evolutionary phylogeny of the oomycete "fungi". Protoplasma 249:3-19.
  8. Beakes, G. W. & Thines, M. 2017. Hyphochytriomycota and Oomycota. In Archibald, J., Simpson, A. & Slamovits, C. (Eds.) Handbook of the Protists. Springer, Cham, pp. 435-505.
  9. Boller, T. & Felix, G. 2009. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 60:379-406. https://doi.org/10.1146/annurev.arplant.57.032905.105346
  10. Borowitzka, M. A. 2013. High-value products from microalgae: their development and commercialisation. J. Appl. Phycol. 25:743-756. https://doi.org/10.1007/s10811-013-9983-9
  11. Bouwmeester, M. M., Goedknegt, M. A., Poulin, R. & Thieltges, D. W. 2021. Collateral diseases: aquaculture impacts on wildlife infections. J. Appl. Ecol. 58:453-464. https://doi.org/10.1111/1365-2664.13775
  12. Brawley, S. H., Blouin, N. A., Ficko-Blean, E., Wheeler, G. L., Lohr, M., Goodson, H. V., Jenkins, J. W., Blaby-Haas, C. E., Helliwell, K. E., Chan, C. X., Marriage, T. N., Bhattacharya, D., Klein, A. S., Badis, Y., Brodie, J., Cao, Y., Collen, J., Dittami, S. M., Gachon, C. M. M., Green, B. R., Karpowicz, S. J., Kim, J. W., Kudahl, U. J., Lin, S., Miche, G., Mittag, M., Olson, B. J. S. C., Pangilinan, J. L., Peng, Y., Qiu, H., Shu, S., Singer, J. T., Smith, A. G., Sprecher, B. N., Wagner, V., Wang, W., Wang, Z.-Y., Yan, J., Yarish, C., Zauner-Riek, S., Zhuang, Y., Zou, Y., Lindquist, E. A., Grimwood, J., Barry, K. W., Rokhsar, D. S., Schmutz, J., Stiller, J. W., Grossman, A. R. & Prochnik, S. E. 2017. Insights into the red algae and eukaryotic evolution from the genome of Porphyra umbilicalis (Bangiophyceae, Rhodophyta). Proc. Natl. Acad. Sci. U. S. A. 114:E6361-E6370.
  13. Buaya, A. T., Ploch, S., Inaba, S. & Thines, M. 2019. Holocarpic oomycete parasitoids of red algae are not Olpidiopsis. Fung. Syst. Evol. 4:21-31.
  14. Buaya, A. T., Scholz, B. & Thines, M. 2021. Sirolpidium bryopsidis, a parasite of green algae, is probably conspecific with Pontisma lagenidioides, a parasite of red algae. J. Syst. Evol. 7:223-231.
  15. Buaya, A. T. & Thines, M. 2020. Diatomophthoraceae: a new family of Olpidiopsis-like diatom parasitoids largely unrelated to Ectrogella. Fungal Syst. Evol. 5:113-118. https://doi.org/10.3114/fuse.2020.05.06
  16. Cai, J., Lovatelli, A., Aguilar-Manjarrez, J., Cornish, L., Dabbadie, L., Desrochers, A., Diffey, S., Garrido Gamarro, E., Geehan, J., Hurtado, A., Lucente, D., Mair, G., Miao, W., Potin, P., Przybyla, C., Reantaso, M., Roubach, R., Tauati, M. & Yuan, X. 2021. Seaweeds and microalgae: an overview for unlocking their potential in global aquaculture development. FAO Fisheries and Aquaculture Circular. No. 1229. Food and Agriculture Organization, Rome, 48 pp.
  17. Chakraborty, S., Moeder, W. & Yoshioka, K. 2017. Plant immunity. In Roitberg, B. D. (Ed.) Reference Module in Life Sciences. Elsevier, Amsterdam, pp. 1-8.
  18. Choudhury, F. K., Rivero, R. M., Blumwald, E. & Mittler, R. 2017. Reactive oxygen species, abiotic stress and stress combination. Plant J. 90:856-867. https://doi.org/10.1111/tpj.13299
  19. Coll, N. S., Epple, P. & Dangl, J. L. 2011. Programmed cell death in the plant immune system. Cell Death Differ. 18:1247-1256. https://doi.org/10.1038/cdd.2011.37
  20. Cottier-Cook, E. J., Nagabhatla, N., Asri, A., Beveridge, M., Bianchi, P., Bolton, J., Bondad-Reantaso, M. G., Brodie, J., Buschmann, A., Cabarubias, J., Campbell, I., Chopin, T., Critchley, A., De Lombaerde, P., Doumeizel, V., Gachon, C. M. M., Hayashi, L., Hewitt, C. L., Huang, J., Hurtado, A., Kambey, C., Kim, G. H., Le Masson, V., Lim, P. E., Liu, T., Malin, G., Matoju, II., 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 Press, Hamilton, ON, 14 pp.
  21. Craigie, J. S. & Shacklock, P. F. 1995. Culture of Irish moss. In Boghen, A. D. (Ed.) Cold-water Aquaculture in Atlantic Canada. University of Moncton Press, Moncton, pp. 243-270.
  22. De Cock, A. W. A. M. 1986. Marine Pythiaceae from decaying seaweeds in the Netherlands. Mycotaxon 25:101-110.
  23. de Oliveira, L. S., Tschoeke, D. A., Magalhaes Lopes, A. C. R., Sudatti, D. B., Meirelles, P. M., Thompson, C. C., Pereira, R. C. & Thompson, F. L. 2017. Molecular mechanisms for microbe recognition and defense by the red seaweed Laurencia dendroidea. mSphere 2:e00094-17.
  24. 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
  25. 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
  26. Ding, L.-N., Li, Y.-T., Wu, Y.-Z., Li, T., Geng, R., Cao, J., Zhang, W. & Tan, X.-L. 2022. Plant disease resistance-related signaling pathways: recent progress and future prospects. Int. J. Mol. Sci. 23:16200.
  27. Fawke, S., Doumane, M. & Schornack, S. 2015. Oomycete interactions with plants: infection strategies and resistance principles. Microbiol. Mol. Biol. Rev. 79:263-280. https://doi.org/10.1128/MMBR.00010-15
  28. 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. Org. 117:45-57. https://doi.org/10.3354/dao02930
  29. 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.
  30. Gachon, C. M. M., Sime-Ngando, T., Strittmatter, M., Chambouvet, A. & Kim, G. H. 2010. Algal diseases: spotlight on a black box. Trends Plant Sci. 15:633-640. https://doi.org/10.1016/j.tplants.2010.08.005
  31. Hallmann, A. 2007. Algal transgenics and biotechnology. Transgenic Plant J. 1:81-98.
  32. Hardham, A. R. 2007. Cell biology of plant-oomycete interactions. Cell. Microbiol. 9:31-39. https://doi.org/10.1111/j.1462-5822.2006.00833.x
  33. Herrero, M.-L., Brurberg, M. B., Ojeda, D. I. & Roleda, M. Y. 2020. Occurrence and pathogenicity of Pythium (Oomycota) on Ulva species (Chlorophyta) at different salinities. Algae 35:79-89. https://doi.org/10.4490/algae.2020.35.2.25
  34. Hyde, K. D., Nilsson, R. H., Alias, S. A., Ariyawansa, H. A., Blair, J. E., Cai, L., de Cock, A. W. A. M., Dissanayake, A. J., Glockling, S. L., Goonasekara, I. D., Gorczak, M., Hahn, M., Jayawardena, R. S., van Kan, J. A. L., Laurence, M. H., Levesque, C. A., Li, X., Liu, J.-K., Maharachchikumbura, S. S. N., Manamgoda, D. S., Martin, F. N., McKenzie, E. H. C., McTaggart, A. R., Mortimer, P. E., Nair, P. V. R., Pawlowska, J., Rintoul, T. L., Shivas, R. G., Spies, C. F. J., Summerell, B. A., Taylor, P. W. J., Terhem, R. B., Udayanga, D., Vaghefi, N., Walther, G., Wilk, M., Wrzosek, M., Xu, J.-C., Yan, J. & Zhou, N. 2014. One stop shop: backbones trees for important phytopathogenic genera: I (2014). Fungal Divers. 67:21-125. https://doi.org/10.1007/s13225-014-0298-1
  35. 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
  36. Iwasaki, A. & Medzhitov, R. 2010. Regulation of adaptive immunity by the innate immune system. Science 327:291-295. https://doi.org/10.1126/science.1183021
  37. Jiang, Y. N., Haudenshield, J. S. & Hartman, G. L. 2012. Characterization of Pythium spp. from soil samples in Illinois. Can. J. Plant Pathol. 34:448-454. https://doi.org/10.1080/07060661.2012.705326
  38. Jones, J. D. G. & Dangl, J. L. 2006. The plant immune system. Nature 444:323-329. https://doi.org/10.1038/nature05286
  39. Kamoun, S., Furzer, O., Jones, J. D. G., Judelson, H. S., Ali, G. S., Dalio, R. J. D., Roy, S. G., Schena, L., Zambounis, A., Panabieres, F., Cahill, D., Ruocco, M., Figueiredo, A., Chen, X.-R., Hulvey, J., Stam, R., Lamour, K., Gijzen, M., Tyler, B. M., Grunwald, N. J., Mukhtar, M. S., Tome, D. F. A., Tor, M., Van Den Ackerveken, G., McDowell, J., Daayf, F., Fry, W. E., Lindqvist-Kreuze, H., Meijer, H. J. G., Petre, B., Ristaino, J., Yoshida, K., Birch, P. R. J. & Govers, F. 2015. The Top 10 oomycete pathogens in molecular plant pathology. Mol. Plant Pathol. 16:413-434. https://doi.org/10.1111/mpp.12190
  40. 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
  41. Kim, Y. T., Kim, R.-W., Shim, E., Park, H., Klochkova, T. A. & Kim, G. H. 2023. Control of oomycete pathogens during Pyropia farming and processing using calcium propionate. Algae 38:71-80. https://doi.org/10.4490/algae.2023.38.3.8
  42. Klochkova, T. A., Jung, S. & Kim, G. H. 2017a. 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
  43. Klochkova, T. A., Kwak, M. S. & Kim, G. H. 2017b. A new endoparasite Olpidiopsis heterosiphoniae sp. nov. that infects red algae in Korea. Algal Res. 28:264-269. https://doi.org/10.1016/j.algal.2017.09.019
  44. Klochkova, T. A., Shim, J. B., Hwang, M. S. & Kim, G. H. 2012. Host-parasite interactions and host species 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
  45. 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
  46. Kwak, M. S., Klochkova, T. A., Jeong, S. & Kim, G. H. 2017. Olpidiopsis porphyrae var. koreanae, an endemic endoparasite infecting cultivated Pyropia yezoensis in Korea. J. Appl. Phycol. 29:2003-2012. https://doi.org/10.1007/s10811-017-1109-3
  47. Lagerheim, G. 1899. Om vaxt- och djurlamningarna i Andrees polarboj. Swedish Soc. Anthropol. Geogr. 19:425-443.
  48. Latijnhouwers, M., de Wit, P. J. G. M. & Govers, F. 2003. Oomycetes and fungi: similar weaponry to attack plants. Trends Microbiol. 11:462-469. https://doi.org/10.1016/j.tim.2003.08.002
  49. Lee, S. J., Hwang, M. S., Park, M. A., Baek, J. M., Ha, D.-S., Lee, J. E. & Lee, S.-R. 2015. Molecular identification of the algal pathogen Pythium chondricola (Oomycetes) from Pyropia yezoensis (Rhodophyta) using ITS and cox1 markers. Algae 30:217-222. https://doi.org/10.4490/algae.2015.30.3.217
  50. Lee, S. J., Jee, B. Y., Son, M.-H. & Lee, S.-R. 2017. Infection and cox2 sequence of Pythium chondricola (Oomycetes) causing red rot disease in Pyropia yezoensis (Rhodophyta) in Korea. Algae 32:155-160. https://doi.org/10.4490/algae.2017.32.5.16
  51. Lee, S. J. & Lee, S.-R. 2022. Rapid detection of red rot disease pathogens (Pythium chondricola and P. porphyrae) in Pyropia yezoensis (Rhodophyta) with PCR-RFLP. Plant Dis. 106:30-33. https://doi.org/10.1094/PDIS-07-21-1494-SC
  52. LeVesque, C. A. & De Cock, A. W. A. M. 2004. Molecular phylogeny and taxonomy of the genus Pythium. Mycol. Res. 108:1363-1383. https://doi.org/10.1017/S0953756204001431
  53. Magnus, P. 1872. Ueber Chytridium tumefaciens n. sp. in den Wurzelhaaren von Ceramium flabelligerum und acanthonotum und andere in Meeresalgen lebende. Sber. Ges. Naturf. Freunde Berl. 1872:87-90.
  54. Mayor, A., Martinon, F., De Smedt, T., Petrilli, V. & Tschopp, J. 2007. A crucial function of SGT1 and HSP90 in inflammasome activity links mammalian and plant innate immune responses. Nat. Immunol. 8:497-503. https://doi.org/10.1038/ni1459
  55. Moon, J.-S., Hong, C.-Y., Lee, J.-W. & Kim, G.-H. 2022. ROS signaling mediates directional cell elongation and somatic cell fusion in the red alga Griffithsia monilis. Cells 11:2124.
  56. Nguyen, H. D. T., Dodge, A., Dadej, K., Rintoul, T. L., Ponomareva, E., Martin, F. N., de Cock, A. W. A. M., Levesque, C. A., Redhead, S. A. & Spies, C. F. J. 2022. Whole genome sequencing and phylogenomic analysis show support for the splitting of genus Pythium. Mycologia 114:501-515. https://doi.org/10.1080/00275514.2022.2045116
  57. Ortiz, D. & Dodds, P. N. 2018. Plant NLR origins traced back to green algae. Trends Plant Sci. 23:651-654. https://doi.org/10.1016/j.tplants.2018.05.009
  58. Park, C., Sakaguchi, K., Kakinuma, M. & Amano, H. 2000. Comparison of the morphological and physiological features of the red rot disease fungus Pythium sp. isolated from Porphyra yezoensis from Korea and Japan. Fish Sci. 66:261-269. https://doi.org/10.1046/j.1444-2906.2000.00043.x
  59. 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
  60. Pelaez-Vico, M. A., Fichman, Y., Zandalinas, S. I., Van Breusegem, F., Karpinski, S. M. & Mittler, R. 2022. ROS and redox regulation of cell-to-cell and systemic signaling in plants during stress. Free Radic. Biol. Med. 193:354-362. https://doi.org/10.1016/j.freeradbiomed.2022.10.305
  61. Perez, I. B. & Brown, P. J. 2014. The role of ROS signaling in cross-tolerance: from model to crop. Front. Plant Sci. 5:754.
  62. Petersen, H. E. 1905. Contributions a la connaissance des Phycomycetes marins (Chytridineae Fischer). Oversigt Kgl. Danske Vidensk. Selskabs Forhandl. 5:439-488.
  63. Phillips, A. J., Anderson, V. L., Robertson, E. J., Secombes, C. J. & van West, P. 2008. New insights into animal pathogenic oomycetes. Trends Microbiol. 16:13-19. https://doi.org/10.1016/j.tim.2007.10.013
  64. Potin, P., Bouarab, K., Salaun, J.-P., Pohnert, G. & Kloareg, B. 2002. Biotic interactions of marine algae. Curr. Opin. Plant Biol. 5:308-317. https://doi.org/10.1016/S1369-5266(02)00273-X
  65. Qiu, L., Mao, Y., Tang, L., Tang, X. & Mo, Z. 2019. Characterization of Pythium chondricola associated with red rot disease of Pyropia yezoensis (Ueda) (Bangiales, Rhodophyta) from Lianyungang, China. J. Oceanol. Limnol. 37:1102-1112. https://doi.org/10.1007/s00343-019-8075-3
  66. Roh, H. & Kannimuthu, D. 2023. Assessments of epidemic spread in aquaculture: comparing different scenarios of infectious bacteria incursion through spatiotemporal hybrid modeling. Front. Vet. Sci. 10:1205506.
  67. Saraiva, M., Scislak, M. E., Ascurra, Y. T., Ferrando, T. M., Zic, N., Henard, C., van West, P., Trusch, F. & Vleeshouwers, V. G. A. A. 2023. The molecular dialog between oomycete effectors and their plant and animal hosts. Fungal Biol. Rev. 43:100289.
  68. 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
  69. 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
  70. Shim, E., Lee, J. W., Park, H., Zuccarello, G. C. & Kim, G. H. 2022. Hydrogen peroxide signalling mediates fertilization and post-fertilization development in the red alga Bostrychia moritziana. J. Exp. Bot. 73:727-741. https://doi.org/10.1093/jxb/erab453
  71. Shine, M. B., Xiao, X., Kachroo, P. & Kachroo, A. 2019. Signaling mechanisms underlying systemic acquired resistance to microbial pathogens. Plant Sci. 279:81-86. https://doi.org/10.1016/j.plantsci.2018.01.001
  72. Sparrow, F. K. 1934. Observations on marine phycomycetes collected in Denmark. Dansk. Bot. Arkiv. 8:1-24.
  73. Sparrow, F. K. 1960. Aquatic Phycomycetes. 2nd ed. University of Michigan Press, Ann Arbor, MI, 1187 pp.
  74. Swarupa, V., Ravishankar, K. V. & Rekha, A. 2014. Plant defense response against Fusarium oxysporum and strategies to develop tolerant genotypes in banana. Planta 239:735-751. https://doi.org/10.1007/s00425-013-2024-8
  75. Takahashi, M., Ichitani, T. & Sasaki, M. 1977. Pythium porphyrae Takahashi et Sasaki, sp. nov. causing red rot of marine red algae Porphyra spp. Trans. Mycol. Soc. Jpn. 18:279-285.
  76. Tang, L., Qiu, L., Liu, C., Du, G., Mo, Z., Tang, X. & Mao, Y. 2019. Transcriptomic insights into innate immunity responding to red rot disease in red alga Pyropia yezoensis. Int. J. Mol. Sci. 20:5970.
  77. Tedesco, P., Saraiva, M., Sandoval-Sierra, J. V., Fioravanti, M. L., Morandi, B., Dieguez-Uribeondo, J., van West, P. & Galuppi, R. 2021. Evaluation of potential transfer of the pathogen Saprolegnia parasitica between farmed salmonids and wild fish. Pathogens 10:926.
  78. Torres, M. A., Jones, J. D. G. & Dangl, J. L. 2006. Reactive oxygen species signaling in response to pathogens. Plant Physiol. 141:373-378. https://doi.org/10.1104/pp.106.079467
  79. Ullmann, J. & Grimm, D. 2021. Algae and their potential for a future bioeconomy, landless food production, and the socio-economic impact of an algae industry. Org. Agric. 11:261-267. https://doi.org/10.1007/s13165-020-00337-9
  80. van Bentem, S. F., Vossen, J. H., de Vries, K. J., van Wees, S., Tameling, W. I. L., Dekker, H. L., de Koster, C. G., Haring, M. A., Takken, F. L. W. & Cornelissen, B. J. C. 2005. Heat shock protein 90 and its co-chaperone protein phosphatase 5 interact with distinct regions of the tomato I-2 disease resistance protein. Plant J. 43:284-298. https://doi.org/10.1111/j.1365-313X.2005.02450.x
  81. Van der Meer, J. P. & Pueschel, C. M. 1985. Petersenia palmariae n. sp. (Oomycetes): a pathogenic parasite of the red alga Palmaria mollis (Rhodophyceae). Can. J. Bot. 63:404-408. https://doi.org/10.1139/b85-048
  82. Weinberger, F. 1999. Epiphyte-host interactions: Gracilaria conferta (Rhodophyta) and associated bacteria. Ph.D. dissertation, Christian Albrechts Universitat, Kiel, Germany, 150 pp.
  83. Weinberger, F., Leonardi, P., Miravalles, A., Correa, J. A., Lion, U., Kloareg, B. & Potin, P. 2005. Dissection of two distinct defense-related responses to agar oligosaccharides in Gracilaria chilensis (Rhodophyta) and Gracilaria conferta (Rhodophyta). J. Phycol. 41:863-873. https://doi.org/10.1111/j.0022-3646.2005.05009.x
  84. Whittick, A. & South, G. R. 1972. Olpidiopsis antithamnionis n. sp. (Oomycetes, Olpidiopsidaceae), a parasite of Antithamnion floccosum (O. F. Mull.) Kleen from Newfoundland. Arch. Mikrobiol. 82:353-360. https://doi.org/10.1007/BF00424938