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The Korean Society of Phycology (한국조류학회(藻類))
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Kelps in Korea: from population structure to aquaculture to potential carbon sequestration

  • Hwang, Eun Kyoung (Fisheries Seed and Breeding Research Institute, National Institute of Fisheries Science) ;
  • Boo, Ga Hun (Department of Biological Sciences, Sungkyunkwan University) ;
  • Graf, Louis (Department of Biological Sciences, Sungkyunkwan University) ;
  • Yarish, Charles (Department of Ecology and Evolutionary Biology, University of Connecticut) ;
  • Yoon, Hwan Su (Department of Biological Sciences, Sungkyunkwan University) ;
  • Kim, Jang Kyun (Department of Marine Science, Incheon National University)
  • Received : 2022.01.10
  • Accepted : 2022.03.03
  • Published : 2022.06.15
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Abstract

Korea is one of the most advanced countries in kelp aquaculture. The brown algae, Undaria pinnatifida and Saccharina japonica are major aquaculture species and have been principally utilized for human food and abalone feed in Korea. This review discusses the diversity, population structure and genomics of kelps. In addition, we have introduced new cultivar development efforts considering climate change, and potential carbon sequestration of kelp aquaculture in Korea. U. pinnatifida showed high diversity within the natural populations but reduced genetic diversity in cultivars. However, very few studies of S. japonica have been conducted in terms of population structure. Since studies on cultivar development began in early 2000s, five U. pinnatifida and one S. japonica varieties have been registered to the International Union for the Protection of New Varieties of Plants (UPOV). To meet the demands for seaweed biomass in various industries, more cultivars should be developed with specific traits to meet application demands. Additionally, cultivation technologies should be diversified, such as integrated multi-trophic aquaculture (IMTA) and offshore aquaculture, to achieve environmental and economic sustainability. These kelps are anticipated to be important sources of blue carbon in Korea.

Keywords

Acknowledgement

This research was supported by grants from the National Institute of Fisheries Science, Republic of Korea (R2022012) to EK Hwang, the Korea Institute of Marine Science and Technology Promotion (KIMST) funded by the Ministry of Oceans and Fisheries (MOF) (20180430, 20210469) to HS Yoon and the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (NRF-2017R1A6A1A06015181) to JK Kim.

References

  1. APVC (Aquatic Plant Variety Center at the National Institute of Fisheries Science). 2021. List of registration seaweed cultivars. Available from: http://nifs.go.kr/apvc/index.ap. Accessed Aug 10, 2021.
  2. Bolton, J. J. 2010. The biogeography of kelps (Laminariales, Phaeophyceae): a global analysis with new insights from recent advances in molecular phylogenetics. Helgol. Mar. Res. 64:263-279. https://doi.org/10.1007/s10152-010-0211-6
  3. Boo, G. H., Lindstrom, S. C., Klochkova, N. G., Yotsukura, N., Yang, E. C., Kim, H. G., Waaland, J. R., Cho, G. Y., Miller, K. A. & Boo, S. M. 2011. Taxonomy and biogeography of Agarum and Thalassiophyllum (Laminariales, Phaeophyceae) based on sequences of nuclear, mitochondrial, and plastid markers. Taxon 60:831-840. https://doi.org/10.1002/tax.603015
  4. Boo, S. M., Lee, W. J., Yoon, H. S., Kato, A. & Kawai, H. 1999. Molecular phylogeny of Laminariales (Phaeophyceae) inferred from small subunit ribosomal DNA sequences. Phycol. Res. 47:109-114. https://doi.org/10.1111/j.1440-1835.1999.tb00291.x
  5. Bringloe, T. T., Starko, S., Wade, R. M., Vieira, C., Kawai, H., De Clerck, O., Cock, J. M., Coelho, S. M., Destombe, C., Valero, M., Neiva, J., Pearson, G. A., Faugeron, S., Serrao, E. A. & Verbruggen, H. 2020. Phylogeny and evolution of the brown algae. Crit. Rev. Plant Sci. 39:281-321. https://doi.org/10.1080/07352689.2020.1787679
  6. Buck, B. H., Krause, G. & Rosenthal, H. 2004. Extensive open ocean aquaculture development within wind farms in Germany: the prospect of offshore co-management and legal constraints. Ocean Coast. Manag. 47:95-122. https://doi.org/10.1016/j.ocecoaman.2004.04.002
  7. Buschmann, A. H. & Camus, C. 2019. An introduction to farming and biomass utilisation of marine macroalgae. Phycologia 58:443-445. https://doi.org/10.1080/00318884.2019.1638149
  8. Buschmann, A. H., Camus, C., Infante, I., Neori, A., Hernandez-Gonzalez, M. C., Pereda, S. V., Gomez-Pinchetti, J. L., Golberg, A., Tadmor-Shalev, N. & Critchley, A. T. 2017. Seaweed production: overview of the global state of exploitation, farming and emerging research activity. Eur. J. Phycol. 52:391-406. https://doi.org/10.1080/09670262.2017.1365175
  9. Chang, J. W. & Geon, S. H. 1970. Studies on the culture of Laminaria. (1) On the transplantation of tangle Laminaria religiosa Miyabe in temperate zone (the coast of Ilsan-Dong, Ulsan city). Bull. Fish. Res. Dev. Agency 5:63-75.
  10. Choi, J. W., Graf, L., Peters, A. F., Cock, J. M., Nishitsuji, K., Arimoto, A., Shoguchi, E., Nagasato, C., Choi, C. G. & Yoon, H. S. 2020. Organelle inheritance and genome architecture variation in isogamous brown algae. Sci. Rep. 10:2048. https://doi.org/10.1038/s41598-020-58817-7
  11. Choi, K. -J. 2020. Development of the automation system for seaweed biomass mass production. J. Korean Soc. Ind. Converg. 23:351-359.
  12. Chung, I. K. 2007. Seaweed coastal CO2 removal belt in Korea and algal paper and biofuel. In United Nations Framework Conv. Clim. Change 13th Conf. Parties, United Nations Framework Convention on Climate Change, Rio de Janeiro.
  13. Chung, I. K., Beardall, J., Mehta, S., Sahoo, D. & Stojkovic, S. 2011. Using marine macroalgae for carbon sequestration: a critical appraisal. J. Appl. Phycol. 23:877-886. https://doi.org/10.1007/s10811-010-9604-9
  14. Daguin, C., Voisin, M., Engel, C. & Viard, F. 2005. Microsatellites isolation and polymorphism in introduced populations of the cultivated seaweed Undaria pinnatifida (Phaeophyceae, Laminariales). Conserv. Genet. 6:647-650.
  15. Duarte, C. M., Wu, J., Xiao, X., Bruhn, A. & Krause-Jensen, D. 2017. Can seaweed farming play a role in climate change mitigation and adaptation? Front. Mar. Sci. 4:100.
  16. Epstein, G. & Smale, D. A. 2017. Undaria pinnatifida: a case study to highlight challenges in marine invasion ecology and management. Ecol. Evol. 7:8624-8642. https://doi.org/10.1002/ece3.3430
  17. FAO (Food and Agriculture Organization of the United Nations). 2021. Fishery and aquaculture statistics. Global aquaculture production 1950-2019 (FishtatJ). Available from: http://www.fao.org/fishery/statistics/software/fishstatj/en. Accessed Jun 21, 2021.
  18. FIRA (Korea Fisheries Resources Agency). 2021. Information and data. Available from: https://fira.or.kr. Accessed Jun 21, 2021.
  19. Fu, Y. X. 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915-925. https://doi.org/10.1093/genetics/147.2.915
  20. Graf, L., Shin, Y., Yang, J. H., Choi, J. W., Hwang, I. K., Nelson, W., Bhattacharya, D., Viard, F. & Yoon, H. S. 2021. A genome-wide investigation of the effect of farming and human-mediated introduction on the ubiquitous seaweed Undaria pinnatifida. Nat. Ecol. Evol. 5:360-368. https://doi.org/10.1038/s41559-020-01378-9
  21. Grant, W. A. S. & Bowen, B. W. 1998. Shallow population histories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation. J. Hered. 89:415-426. https://doi.org/10.1093/jhered/89.5.415
  22. Guzinski, J., Ballenghien, M., Daguin-Thiebaut, C., Leveque, L. & Viard, F. 2018. Population genomics of the introduced and cultivated Pacific kelp Undaria pinnatifida: marinas-not farms-drive regional connectivity and establishment in natural rocky reefs. Evol. Appl. 11:1582-1597. https://doi.org/10.1111/eva.12647
  23. Ha, D. S., Hwang, E. K., Yoo, H. I., Lee, S. J. & Baek, J. I. 2018. Cultivation manual of Undaria pinnatifida. Maple Desgine Co., Busan, 105 pp.
  24. Harper, J. T. & Saunders, G. W. 2001. Molecular systematics of the Florideophyceae (Rhodophyta) using nuclear large and small subunit rDNA sequence data. J. Phycol. 37:1073-1082. https://doi.org/10.1046/j.1529-8817.2001.00160.x
  25. Hebert, P. D. N., Cywinska, A., Ball, S. L. & deWaard, J. R. 2003. Biological identifications through DNA barcodes. Proc. R. Soc. B 270:313-321. https://doi.org/10.1098/rspb.2002.2218
  26. Hoegh-Guldberg, O. 2019. The ocean as a solution to climate change: five opportunities for action. Available from: http://www.oceanpanel.org/climate. Accessed Jun 21, 2021.
  27. Hu, Z. -M., Shan, T. -F., Zhang, J., Zhang, Q. -S., Critchley, A. T., Choi, H. -G., Yotsukura, N., Liu, F. -L. & Duan, D. -L. 2021. Kelp aquaculture in China: a retrospective and future prospects. Rev. Aquac. 13:1324-1351. https://doi.org/10.1111/raq.12524
  28. Huh, M. K. & Huh, H. W. 2002. Genetic diversity and population structure of wild and cultivated brown sea mustard, Undaria pinnatifida. Protistology 2:159-168.
  29. Hwang, E. K., Choi, J. W., Yoon, H. S. & Park, C. S. 2020. Morphological and genetic differences between Korean Sugwawon No. 301 and Chinese Huangguan No. 1 strains of Saccharina japonica (Phaeophyceae) in a Korean aquaculture farm. J. Appl. Phycol. 32:2245-2252. https://doi.org/10.1007/s10811-019-02029-8
  30. Hwang, E. K., Gong, Y. G. & Park, C. S. 2012. Cultivation of a hybrid of free-living gametophytes between Undariopsis peterseniana and Undaria pinnatifida: morphological aspects and cultivation period. J. Appl. Phycol. 24:401-408. https://doi.org/10.1007/s10811-011-9727-7
  31. Hwang, E. K., Ha, D. S. & Park, C. S. 2017. Strain selection and initiation timing influence the cultivation period of Saccharina japonica and their impact on the abalone feed industry in Korea. J. Appl. Phycol. 29:2297-2305. https://doi.org/10.1007/s10811-017-1179-2
  32. Hwang, E. K., Hwang, I. K., Park, E. J., Gong, Y. G. & Park, C. S. 2014. Development and cultivation of F2 hybrid between Undariopsis peterseniana and Undaria pinnatifida for abalone feed and commercial mariculture in Korea. J. Appl. Phycol. 26:747-752. https://doi.org/10.1007/s10811-013-0164-7
  33. Hwang, E. K., Liu, F., Lee, K. H., Ha, D. S. & Park, C. S. 2018. Comparison of the cultivation performance between Korean (Sugwawon No. 301) and Chinese strains (Huangguan No. 1) of kelp Saccharina japonica in an aquaculture farm in Korea. Algae 33:101-108. https://doi.org/10.4490/algae.2018.33.2.4
  34. Hwang, E. K. & Park, C. S. 2020. Seaweed cultivation and utilization of Korea. Algae 35:107-121. https://doi.org/10.4490/algae.2020.35.5.15
  35. Hwang, E. K., Yotsukura, N., Pang, S. J., Su, L. & Shan, T. F. 2019. Seaweed breeding programs and progress in eastern Asian countries. Phycologia 58:484-495. https://doi.org/10.1080/00318884.2019.1639436
  36. Intergovernmental Panel on Climate Change. 2021. Climate change 2021: the physical science basis. Working group I contribution to the sixth assessment report of the Intergovernmental Panel on Climate Change. Intergovernmental Panel on Climate Change, Geneva, 3949 pp.
  37. Jackson, C., Salomaki, E. D., Lane, C. E. & Saunders, G. W. 2017. Kelp transcriptomes provide robust support for interfamilial relationships and revision of the little known Arthrothamnaceae (Laminariales). J. Phycol. 53:1-6. https://doi.org/10.1111/jpy.12465
  38. Jesumani, V., Du, H., Aslam, M., Pei, P. & Huang, N. 2019. Potential use of seaweed bioactive compounds in skincare: a review. Mar. Drugs 17:688. https://doi.org/10.3390/md17120688
  39. Jiang, G. -L. 2015. Molecular marker-assisted breeding: a plant breeder's review. In Al-Khayri, J. M., Jain, S. M. & Johnson, D. V. (Eds.) Advances in Plant Breeding Strategies: Breeding, Biotechnology and Molecular Tools. Springer International Publishing, Cham, pp. 431-472.
  40. Kawai, H., Hanyuda, T., Gao, X., Terauchi, M., Miyata, M., Lindstrom, S. C., Klochkova, N. G. & Miller, K. A. 2017. Taxonomic revision of the Agaraceae with a description of Neoagarum gen. nov. and reinstatement of Thalassiophyllum. J. Phycol. 53:261-270. https://doi.org/10.1111/jpy.12511
  41. Kawai, H., Hanyuda, T., Lindeberg, M. & Lindstrom, S. C. 2008. Morphology and molecular phylogeny of Aureophycus aleuticus gen. et sp. nov. (Laminariales, Phaeophyceae) from the Aleutian Islands. J. Phycol. 44:1013- 1021. https://doi.org/10.1111/j.1529-8817.2008.00548.x
  42. Kawai, H., Hanyuda, T., Ridgway, L. M. & Holser, K. 2013. Ancestral reproductive structure in basal kelp Aureophycus aleuticus. Sci. Rep. 3:2491. https://doi.org/10.1038/srep02491
  43. Kawai, H., Hanyuda, T. & Uwai, S. 2016. Evolution and biogeography of Laminarialean kelps. In Hu, Z. -M. & Fraser, C. (Eds.) Seaweed Phylogeography. Springer Netherlands, Dordrecht, pp. 227-249.
  44. Kim, J. K., Stekoll, M. & Yarish, C. 2019. Opportunities, challenges and future directions of open-water seaweed aquaculture in the United States. Phycologia 58:446-461. https://doi.org/10.1080/00318884.2019.1625611
  45. Kim, J. K., Yarish, C., Hwang, E. K., Park, M. & Kim, Y. 2017. Seaweed aquaculture: cultivation technologies, challenges and its ecosystem services. Algae 32:1-13. https://doi.org/10.4490/algae.2017.32.3.3
  46. Kim, Y. D., Shim, J. M., Park, M. S., Hong, J. -P., Yoo, H. I., Min, B. H., Jin, H. -J., Yarish, C.& Kim, J. K. 2013. Size determination of Ecklonia cava for successful transplantation onto artificial seaweed reef. Algae 28:365-369. https://doi.org/10.4490/algae.2013.28.4.365
  47. Kimura, K., Nagasato, C., Uwai, S. & Motomura, T. 2010. Sperm mitochondrial DNA elimination in the zygote of the oogamous brown alga Undaria pinnatifida (Laminariales, Phaeophyceae). Cytologia 75:353-361. https://doi.org/10.1508/cytologia.75.353
  48. Klimova, A. V. & Klochkova, T. A. 2021. Cytological and chromosomal features of Alaria species (Laminariales, Phaeophyceae) from Kamchatka. Bull. Kamchatka State Tech. Univ. 58:71-86. https://doi.org/10.17217/2079-0333-2021-58-71-86
  49. Klochkova, T. A., Kim, G. H., Klimova, A. V. & Klochkova, N. G. 2018. Taxonomic significance of phenotypic and genotypic characters to describe new genera and species. Kamchatka Res. Inst. Fish. Oceanogr. 51:60-72.
  50. Kogame, K., Uwai, S., Shimada, S. & Masuda, M. 2005. A study of sexual and asexual populations of Scytosiphon lomentaria (Scytosiphonaceae, Phaeophyceae) in Hokkaido, northern Japan, using molecular markers. Eur. J. Phycol. 40:313-322. https://doi.org/10.1080/09670260500193008
  51. Krause-Jensen, D. & Duarte, C. M. 2016. Substantial role of macroalgae in marine carbon sequestration. Nat. Geosci. 9:737-742. https://doi.org/10.1038/ngeo2790
  52. Lane, C. E., Lindstrom, S. C. & Saunders, G. W. 2007. A molecular assessment of northeast Pacific Alaria species (Laminariales, Phaeophyceae) with reference to the utility of DNA barcoding. Mol. Phylogenet. Evol. 44:634-648. https://doi.org/10.1016/j.ympev.2007.03.016
  53. Lane, C. E., Mayes, C., Druehl, L. D. & Saunders, G. W. 2006. A multi-gene molecular investigation of the kelp (Laminariales, Phaeophyceae) supports substantial taxonomic re-organization. J. Phycol. 42:493-512. https://doi.org/10.1111/j.1529-8817.2006.00204.x
  54. Li, Q., Zhang, J., Yao, J., Wang, X. & Duan, D. 2016. Development of Saccharina japonica genomic SSR markers using next-generation sequencing. J. Appl. Phycol. 28:1387-1390. https://doi.org/10.1007/s10811-015-0643-0
  55. Liu, T., Wang, X., Wang, G., Jia, S., Liu, G., Shan, G., Chi, S., Zhang, J., Yu, Y., Xue, T. & Yu, J. 2019. Evolution of complex thallus alga: genome sequencing of Saccharina japonica. Front. Genet. 10:378. https://doi.org/10.3389/fgene.2019.00378
  56. Luning, K. 1990. Seaweeds: their environment, biogeography, and ecophysiology. In Yarish, C. & Kirkman, H. (Eds.) Edited Translation of the German Language Edition Meeresbotanik: Verbreitung, Okophysiologie und Nutzung der marinen Makroalgen by Klaus Luning. John Wiley and Sons, Inc., New York, pp. 1-527.
  57. McDevit, D. C. & Saunders, G. W. 2010. A DNA barcode examination of the Laminariaceae (Phaeophyceae) in Canada reveals novel biogeographical and evolutionary insights. Phycologia 49:235-248. https://doi.org/10.2216/PH09-36.1
  58. Nakayama, T., Watanabe, S., Mitsui, K., Uchida, S. & Inouye, I. 1996. The phylogenetic relationships between Chlamydomonadales and Chlorococcales inferred from the 18S rDNA sequence data. Phycol. Res. 44:47-55. https://doi.org/10.1111/j.1440-1835.1996.tb00037.x
  59. Neushul, M. 1980. Approaches to yield studies and an assessment of foreign macroalgal farming technology. In Proc. Bio-Energy: '80 World Congr. Exp. Bio-Energy Council, Washington, DC, pp. 59-75.
  60. Neushul, M. 1986. Marine farming: macroalgal production and genetics. Final technical report (May 1980-December 1986). Gas Research Institute, Chicago, IL, 185 pp.
  61. North, W. J., Gerard, V. A. & Kuwabara, J. 1982. Farming Macrocystis at coastal and oceanic sites. In Srivastava, L. M. (Ed.) Synthetic and Degradative Processes in Marine Macrophytes. Walter de Gruyter, Berlin, pp. 247-262.
  62. Ortega, A., Geraldi, N. R., Alam, I., Kamau, A. A., Acinas, S. G., Logares, R., Gasol, J. M., Massana, R., Krause-Jensen, D. & Duarte, C. M. 2019. Important contribution of macroalgae to oceanic carbon sequestration. Nat. Geosci. 12:748-754. https://doi.org/10.1038/s41561-019-0421-8
  63. Park, C. -W., Choi, K. -J., Soh, E. -H. & Koh, H. -J. 2016. Study on the future development direction of plant variety protection system in Korea. Korean J. Breed. Sci. 48:11-21. https://doi.org/10.9787/KJBS.2016.48.1.011
  64. Park, J. -S., Shin, S. K., Wu, H., Yarish, C., Yoo, H. I. & Kim, J. K. 2021a. Evaluation of nutrient bioextraction by seaweed and shellfish aquaculture in Korea. J. World Aquac. Soc. 52:1118-1134. https://doi.org/10.1111/jwas.12786
  65. Park, M., Shin, S. K., Do, Y. H., Yarish, C. & Kim, J. K. 2018. Application of open water integrated multi-trophic aquaculture to intensive monoculture: a review of the current status and challenges in Korea. Aquaculture 497:174-183. https://doi.org/10.1016/j.aquaculture.2018.07.051
  66. Park, M. S., Kim, J. K., Shin, S., Min, B. H. & Samanta, P. 2021b. Trophic fractionation in an integrated multi-trophic aquaculture off Tongyoung Coast: a stable isotope approach. Aquaculture 536:736-454.
  67. Saunders, G. W. & Druehl, L. D. 1992. Nucleotide sequences of the small-subunit ribosomal RNA genes from selected Laminariales (Phaeophyta): implications for kelp evolution. J. Phycol. 28:544-549. https://doi.org/10.1111/j.0022-3646.1992.00544.x
  68. Saunders, G. W. & Druehl, L. D. 1993. Revision of the kelp family Alariaceae and the taxonomic affinities of Lessoniopsis Reinke (Laminariales, Phaeophyta). Hydrobiologia 260/261:689-697. https://doi.org/10.1007/BF00049089
  69. Setchell, W. A. 1893. On the classification and geographical distribution of the Laminariaceae. Trans. Conn. Acad. Arts Sci. 9:333-375.
  70. Setchell, W. A. & Gardner, N. L. 1925. The marine algae of the Pacific coast of North America. Part III. Melanophyceae. Univ. Calif. Publ. Bot. 8:383-898.
  71. Shan, T. & Pang, S. 2009. Assessing genetic identity of sporophytic offspring of the brown alga Undaria pinnatifida derived from monocrossing of gametophyte clones by use of amplified fragment length polymorphism and microsatellite markers. Phycol. Res. 57:36-44. https://doi.org/10.1111/j.1440-1835.2008.00519.x
  72. Shan, T., Pang, S., Liu, F., Xu, N., Zhao, X. & Gao, S. 2012. High genetic diversity in gametophyte clones of Undaria pinnatifida from Vladivostok, Dalian and Qingdao revealed using microsatellite analysis. Chin. J. Oceanol. Limnol. 30:225-230. https://doi.org/10.1007/s00343-012-1098-7
  73. Shan, T., Pang, S., Wang, X., Li, J. & Su, L. 2018. Assessment of the genetic connectivity between farmed and wild populations of Undaria pinnatifida (Phaeophyceae) in a representative traditional farming region of China by using newly developed microsatellite markers. J. Appl. Phycol. 30:2707-2714. https://doi.org/10.1007/s10811-018-1449-7
  74. Shan, T., Pang, S., Wang, X., Li, J., Su, L., Schiller, J., Lackschewitz, D., Hall-Spencer, J. M. & Bischof, K. 2019. Genetic analysis of a recently established Undaria pinnatifida (Laminariales: Alariaceae) population in the northern Wadden Sea reveals close proximity between drifting thalli and the attached population. Eur. J. Phycol. 54:154-161. https://doi.org/10.1080/09670262.2018.1532116
  75. Shan, T., Yotsukura, N. & Pang, S. J. 2017. Novel implications on the genetic structure of representative populations of Saccharina japonica (Phaeophyceae) in the Northwest Pacific as revealed by highly polymorphic microsatellite markers. J. Appl. Phycol. 29:631-638. https://doi.org/10.1007/s10811-016-0888-2
  76. Shan, T. F., Pang, S. J., Zhang, Y. R., Yakovleva, I. M. & Skriptsova, A. V. 2011. An AFLP-based survey of genetic diversity and relationships of major farmed cultivars and geographically isolated wild populations of Saccharina japonica (Phaeophyta) along the northwest coasts of the Pacific. J. Appl. Phycol. 23:35-45. https://doi.org/10.1007/s10811-010-9530-x
  77. Silberfeld, T., Leigh, J. W., Verbruggen, H., Cruaud, C., de Reviers, B. & Rousseau, F. 2010. A multi-locus timecalibrated phylogeny of the brown algae (Heterokonta, Ochrophyta, Phaeophyceae): Investigating the evolutionary nature of the "brown algal crown radiation". Mol. Phylogenet. Evol. 56:659-675. https://doi.org/10.1016/j.ympev.2010.04.020
  78. Sohn, C. -H. 1996. Historical review on seaweed cultivation of Korea. Algae 11:357-364.
  79. Sohn, C. H. 1998. The seaweed resources of Korea. In Critchley, A. T. & Masao, O. (Eds.) Seaweed Resources of the World. Japan International Cooperation Agency, Yokosuka, pp. 15-33.
  80. Starko, S., Boo, G. H., Martone, P. T. & Lindstrom, S. 2018. A molecular investigation of Saccharina sessilis from the Aleutian Islands reveals a species complex, necessitating the new combination Saccharina subsessilis. Algae 33:157-166. https://doi.org/10.4490/algae.2018.33.4.2
  81. Starko, S., Gomez, M. S., Darby, H., Demes, K. W., Kawai, H., Yotsukura, N., Lindstrom, S. C., Keeling, P. J., Graham, S. W. & Martone, P. T. 2019. A comprehensive kelp phylogeny sheds light on the evolution of an ecosystem. Mol. Phylogenet. Evol. 136:138-150 https://doi.org/10.1016/j.ympev.2019.04.012
  82. Tajima, F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585-595. https://doi.org/10.1093/genetics/123.3.585
  83. Uwai, S., Arai, S., Morita, T. & Kawai, H. 2007. Genetic distinctness and phylogenetic relationships among Undaria species (Laminariales, Phaeophyceae) based on mitochondrial cox3 gene sequences. Phycol. Res. 55: 263-271. https://doi.org/10.1111/j.1440-1835.2007.00469.x
  84. Uwai, S., Nelson, W., Neill, K., Wang, W. D., Aguilar-Rosas, L. E., Boo, S. M., Kitayama, T. & Kawai, H. 2006. Genetic diversity in Undaria pinnatifida (Laminariales, Phaeophyceae) deduced from mitochondria genes: origins and succession of introduced populations. Phycologia 45:687-695. https://doi.org/10.2216/05-66.1
  85. van den Burg, S. W. K., Rockmann, C., Banach, J. L. & van Hoof, L. 2020. Governing risks of multi-use: seaweed aquaculture at offshore wind farms. Front. Mar. Sci. 7:60. https://doi.org/10.3389/fmars.2020.00060
  86. van den Burg, S. W. K., van Duijn, A. P., Bartelings, H., van Krimpen, M. M. & Poelman, M. 2016. The economic feasibility of seaweed production in the North Sea. Aquac. Econ. Manag. 20:235-252. https://doi.org/10.1080/13657305.2016.1177859
  87. Voisin, M., Engel, C. R. & Viard, F. 2005. Differential shuffling of native genetic diversity across introduced regions in a brown alga: aquaculture vs. maritime traffic effects. Proc. Natl. Acad. Sci. U. S. A. 102:5432-5437. https://doi.org/10.1073/pnas.0501754102
  88. Wever, L., Krause, G. & Buck, B. H. 2015. Lessons from stakeholder dialogues on marine aquaculture in offshore wind farms: perceived potentials, constraints and research gaps. Mar. Policy 51:251-259. https://doi.org/10.1016/j.marpol.2014.08.015
  89. Wood, G., Marzinelli, E. M., Verges, A., Campbell, A. H., Steinberg, P. D. & Coleman, M. A. 2020. Using genomics to design and evaluate the performance of underwater forest restoration. J. Appl. Ecol. 57:1988-1998. https://doi.org/10.1111/1365-2664.13707
  90. Wu, J., Keller, D. P. & Oschlies, A. 2022. Carbon dioxide removal via macroalgae open-ocean mariculture and sinking: an earth system modeling study. Earth Syst. Dynam. Discuss. Preprint at: https://doi.org/10.5194/esd-2021-104.
  91. Ye, N., Zhang, X., Miao, M., Fan, X., Zheng, Y., Xu, D., Wang, J., Zhou, L., Wang, D., Gao, Y., Wang, Y., Shi, W., Ji, P., Li, D., Guan, Z., Shao, C., Zhuang, Z., Gao, Z., Qi, J. & Zhao, F. 2015. Saccharina genomes provide novel insight into kelp biology. Nat. Commun. 6:69-86.
  92. Yong, W. T. L., Thien, V. Y., Rupert, R. & Rodrigues, K. F. 2022. Seaweed: a potential climate change solution. Renew. Sustain. Energy Rev. 159:112222. https://doi.org/10.1016/j.rser.2022.112222
  93. Yoo, C. I., Payuda, T., Kim, H. T. & Ryu, C. R. 2011. A study of conceptual design for constructing offshore biomass culturing and production management system. In Annu. Conf. Korea Assoc. Ocean Sci. Technol. Soc., Korea Association of Ocean Science and Technology Societies, Daejeon, pp. 803-805.
  94. Yoo, H. I., Lee, K. H., Kim, S. H., Ha, D. S. & Hwang, E. K. 2018. Regeneration and the maturation induction of free-living gametophytes of a kelp Saccharina sculpera (Phaeophyceae). Korean J. Environ. Biol. 36:576-583. https://doi.org/10.11626/KJEB.2018.36.4.576
  95. Yoon, H. S. & Boo, S. M. 1999. Phylogeny of Alariaceae (Phaeophyta) with special reference to Undaria based on sequences of the RuBisCo spacer region. Hydrobiologia 398/399:47-55. https://doi.org/10.1023/A:1017068119119
  96. Yoon, H. S., Hackett, J. D. & Bhattacharya, D. 2002. A single origin of the peridinin- and fucoxanthin-containing plastids in dinoflagellates through tertiary endosymbiosis. Proc. Natl. Acad. Sci. U. S. A. 99:11724-11729. https://doi.org/10.1073/pnas.172234799
  97. Yoon, H. S., Lee, J. Y., Boo, S. M. & Bhattacharya, D. 2001. Phylogeny of Alariaceae, Laminariaceae, and Lessoniaceae (Phaeophyceae) based on plastid-encoded RuBisCo spacer and nuclear-encoded ITS sequence comparisons. Mol. Phylogenet. Evol. 21:231-243. https://doi.org/10.1006/mpev.2001.1009
  98. Zhang, J., Yao, J., Hu, Z. -M., Jueterbock, A., Yotsukura, N., Krupnova, T. N., Nagasato, C. & Duan, D. 2019. Phylogeographic diversification and postglacial range dynamics shed light on the conservation of the kelp Saccharina japonica. Evol. Appl. 12:791-803. https://doi.org/10.1111/eva.12756
  99. Zhang, J., Yao, J. -T., Sun, Z. -M., Fu, G., Galanin, D. A., Nagasato, C., Motomura, T., Hu, Z.-M. & Duan, D. -L. 2015. Phylogeographic data revealed shallow genetic structure in the kelp Saccharina japonica (Laminariales, Phaeophyta). BMC Evol. Biol. 15:237. https://doi.org/10.1186/s12862-015-0517-8