Skip to main content
SpringerLink
Log in

Status of genetic studies and breeding of Saccharina japonica in China

  • Review
  • Published:
Journal of Oceanology and Limnology Aims and scope Submit manuscript

Abstract

Saccharina japonica is one of the most important economic brown seaweeds. It is intensively cultivated on large scales in a number of Asian countries. The current annual, global production is about 8 million tons valued as about 4 million US dollars. Considerable efforts have been made to S. japonica in China since the 1950s on its cultivation. To further advance the cultivation of this species, detailed research of genetics and breeding studies are required. Recently, with the advancement of sequencing techniques, the genomics and comparative transcriptomics data were yielded, and quantitative trait locus (QTL) mapping has been conducted, along with genetic linkage maps constructed to this species. New strains have been bred and selected, with better characteristics, e.g. higher seawater temperature resistances and higher yields. In this review, we present the current status of genetic and breeding studies that have been performed to S. japonica in China, and provide guidelines for future developments in the areas of genetic selection and breeding for this species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Data Availability Statement

The chloroplast genome analyzed in this study has been submitted to the NCBI database with the accession number NC_018523.1. All seaweed genomic sequences were retrieved from NCBI genome database.

Abbreviations

NGS:

next generation sequencing

QTL:

quantitative trait locus

SSR:

simple sequence repeat

SNP:

single nucleotide polymorphism

References

  • Arimoto A, Nishitsuji K, Higa Y, Arakaki N, Hisata K, Shinzato C, Satoh N, Shoguchi E. 2019. A siphonous macroalgal genome suggests convergent functions of homeobox genes in algae and land plants. DNA Research, 26(2): 183–192, https://doi.org/10.1093/dnares/dsz002.

    Google Scholar 

  • Balakirev E S, Krupnova T N, Ayala F J. 2012. DNA variation in the phenotypically-diverse brown alga Saccharina japonica. BMC Plant Biology, 12(1): 108, https://doi.org/10.1186/1471-2229-12-108.

    Google Scholar 

  • Bartsch I, Wiencke C, Bischof K, Buchholz C M, Buck B H, Eggert A, Feuerpfeil P, Hanelt D, Jacobsen S, Karez R, Karsten U, Molis M, Roleda M Y, Schubert H, Schumann R, Valentin K, Weinberger F, Wiese J. 2008. The genus Laminaria sensu lato: recent insights and developments. European Journal of Phycology, 43(1): 1–86, https://doi.org/10.1080/09670260701711376.

    Google Scholar 

  • Bi Y H, Hu Y J, Zhou Z G. 2011. Genetic variation of Laminaria japonica (Phaeophyta) populations in China as revealed by RAPD markers. Acta Oceanologica Sinica, 30(2): 103–112, https://doi.org/10.1007/s13131-011-0110-y.

    Google Scholar 

  • Billot C, Rousvoal S, Estoup A, Epplen J T, Saumitou-Laprade P, Valero M, Kloareg B. 1998. Isolation and characterization of microsatellite markers in the nuclear genome of the brown alga Laminaria digitata (Phaeophyceae). Molecular Ecology, 7(12): 1778–1780, https://doi.org/10.1046/j.1365-294x.1998.00516.x.

    Google Scholar 

  • 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, Bhattachaya D, Klein A S, Badis Y, Brodie J, Cao Y Y, Collen J, Dittami S M, Gachon C M M, Green B R, Karpowicz S J, Kim J W, Kudahl U J, Lin S J, Michel G, Mittag M, Olsen B J S C, Pangilinan J L, Peng Y, Qiu H, Shu S Q, Singer J T, Smith A G, Sprecher B N, Wagner V, Wang W F, Wang Z Y, Yan J Y, Yarish C, Zäuner-Riek S, Zhuang Y Y, Zou Y, Lindquist E A, Grimwood J, Barry K W, Rokhsar D S, Schmutz J, Stiler 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). Proceedings of the National Academy of Sciences of the United States of America, 114(31): E6361–E6370, https://doi.org/10.1073/pnas.1703088114.

    Google Scholar 

  • Caron L, Douady D, Quinet-Szely M, de Goër S, Berkaloff C. 1996. Gene structure of a chlorophyll a/c-binding protein from a brown alga: presence of an intron and phylogenetic implications. Journal of Molecular Evolution, 43(3): 270–280, https://doi.org/10.1007/BF02338835.

    Google Scholar 

  • Chen Z H, Wang X L, Li S, Yao J T, Shao Z R, Duan D L. 2019. Verification of the Saccharina japonica translocon Tic20 and its localization in the chloroplast membrane in diatoms. International Journal of Molecular Sciences, 20: 4000, https://doi.org/10.3390/ijms20164000.

    Google Scholar 

  • Cock J M, Liu F L, Duan D L, Bourdareau S, Lipinska A P, Coelho S M, Traver J E. 2017. Rapid evolution of microRNA loci in the brown algae. Genome Biology and Evolution, 9(3): 740–749, https://doi.org/10.1093/gbe/evx038.

    Google Scholar 

  • Cock J M, Sterck L, Rouzé P, Scornet D, Allen A E, Amoutzias G, Anthouard V, Artiguenave F, Aury J M, Badger J H, Beszter B, Billiau K, Bonnet E, Bothwell J H, Bowler C, Boyen C, Brownlee C, Carrano C J, Charrier B, Cho G Y, Coelho S M, Collén J, Corre E, Da Silva C, Delage L, Delaroque N, Dittami S M, Doulbeau S, Elias M, Farnham G, Gachon C M M, Gschloessl B, Heesch S, Jabbar K, Jubin C, Kawai H, Kimura K, Kloareg B, Küpper F C, Lang D, Le Bail A, Leblanc C, Lerouge P, Lohr M, Lopez P J, Martens C, Maumus F, Michel G, Miranda-Saavedra D, Morales J, Moreau H, Motomura T, Nagasato C, Napoli C A, Nelson D R, Nyvall-Collén P, Peters A F, Pommier C, Potin P, Poulain J, Quesneville H, Read B, Rensing S A, Ritter A, Rousvoal S, Samanta M, Samson G, Schroeder D C, Ségurens B, Strittmatter M, Tonon T, Tregear J W, Valentin K, von Dassow P, Yamagishi T, van der Peer Y, Wincker P. 2010. The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature, 465(7298): 617–621, https://doi.org/10.1038/nature09016.

    Google Scholar 

  • Collén J, Porcel B, Carré W, Ball S G, Chaparo C, Tonon T, Barbeyron T, Michel G, Noel B, Valentin K, Elias M, Artiguenave F, Arun A, Aury J M, Barbosa-Neto J F, Bothwell J H, Bouget F Y, Brillet L, Cabello-Hurtado F, Capella-Gutiérrez S, Charrier B, Cladière L, Cock J M, Coelho S M, Colleoni C, Czjzek M, Da Silva C, Delage L, Denoeud F, Deschamps P, Dittami S M, Gabaldón T, Gachon C M M, Groisillier A, Hervé C, Jabbari K, Katinka M, Kloareg B, Kowalczyk N, Labadie K, Leblanc C, Lopez P J, McLachlan D H, Meslet-Cladiere L, Moustafa A, Nehr Z, Collén P N, Panaud O, Partensky F, Poulain J, Rensing S A, Rousvoal S, Samson G, Symeonidi A, Weissenbach J, Zambounis A, Wincker P, Boyen C. 2013. Genome structure and metabolic features in the red seaweed Chondrus crispus shed light on evolution of the Archaeplastida. Proceedings of the National Academy of Sciences of the United States of America, 110(13): 5247–5252, https://doi.org/10.1073/pnas.1221259110.

    Google Scholar 

  • Cormier A, Avia K, Sterck L, Derrien T, Wucher V, Andres G, Monsoor M, Godfroy O, Lipinska A, Perrineau M M, van De Peer Y, Hitte C, Corre E, Coelho S M, Cock J M. 2017. Re-annotation, improved large-scale assembly and establishment of a catalogue of noncoding loci for the genome of the model brown alga Ectocarpus. New Phytologist, 214(1): 219–232, https://doi.org/10.1111/nph.14321.

    Google Scholar 

  • Coyer J A, Peters A F, Hoarau G, Staw W T, Olsen J L. 2002. Inheritance paterns of ITS1, chloroplasts and mitochondria in artificial hybrids of the seaweeds Fucus serratus and F. evanescens (Phaeophyceae). European Journal of Phycology, 37(2): 173–178, https://doi.org/10.1017/S0967026202003682.

    Google Scholar 

  • Crépineau F, Roscoe T, Kaas R, Kloareg B, Boyen C. 2000. Characterisation of complementary DNAs from the expressed sequence tag analysis of life cycle stages of Laminaria digitata (Phaeophyceae). Plant Molecular Biology, 43(4): 503–513, https://doi.org/10.1023/A:1006489920808.

    Google Scholar 

  • De Clerck O, Kao S M, Bogaert K A, Blomme J, Foflonker F, Kwantes M, Vancaester E, Vanderstraeten L, Aydogdu E, Boesger J, Califano G, Charrier B, Clewes R, Del Cortona A, D’Hondt S, Fermandez-Pozo N, Gachon C M, Hanikenne M, Lattermann L, Leliaert F, Liu X J, Maggs C A, Popper Z A, Raven J A, van Bel M, Wilhelmsson P K I, Bhattacharya D, Coates J C, Rensing S A, van der Straeten D, Vardi A, Sterck L, Vandepoele K, van de Peer Y, Wichard T, Bothwell J H. 2018. Insights into the evolution of multicellularity from the sea lettuce genome. Current Biology, 28(18): 2921–2933.e5, https://doi.org/10.1016/j.cub.2018.08.015.

    Google Scholar 

  • Deng Y Y, Wang X L, Guo H, Duan D L. 2014b. A trehalose-6-phosphate synthase gene from Saccharina japonica (Laminariales, Phaeophyta). Molecular Biology Reports, 41(1): 529–536, https://doi.org/10.1007/s11033-013-2888-5.

    Google Scholar 

  • Deng Y Y, Yao J T, Fu G, Guo H, Duan D L. 2014a. Isolation, expression, and characterization of blue light receptor AUREOCHROME gene from Saccharina japonica (Laminariales, Phaeophyta). Marine Biotechnology, 16(2): 135–143, https://doi.org/10.1007/s10126-013-9539-7.

    Google Scholar 

  • Deng Y Y, Yao J T, Wang X L, Guo H, Duan D L. 2009. Transcriptome sequencing and comparative analysis of Saccharina japonica (Laminariales, Phaeophyceae) under blue light induction. PLoS One, 7(6): e39704, https://doi.org/10.1371/journal.pone.0039704.

    Google Scholar 

  • Ding H Y, Guo L, Li X J, Yang G P. 2019. Transcriptome analysis of kelp Saccharina japonica unveils its weird transcripts and metabolite shift of main components at different sporophyte developmental stages. Journal of Oceanology and Limnology, 37(2): 640–650, https://doi.org/10.1007/s00343-019-8019-y.

    Google Scholar 

  • Duan D L, Miao G R, Wang X L. 2015. Aquacultural Biology of Saccharina japonica. Scientific press. Beijing. (in Chinese).

    Google Scholar 

  • Dunwell J M, Wetten A C. 2012. Transgenic Plants: Methods and Protocols. 2nd edn. Human Press, Totowa, NJ.

    Google Scholar 

  • Fan X, Han W T, Teng L H, Jiang P, Zhang X W, Xu D, Li C, Pellegrini M, Wu C H, Wang Y T, Kaczurowski M J S, Lin X, Tirichine L, Mock T, Ye N H. 2020. Single-base methylome profiling of the giant kelp Saccharina japonica reveals significant differences in DNA methylation to microalgae and plants. New Phytologist, 225(1): 234–249, https://doi.org/10.1111/nph.16125.

    Google Scholar 

  • Fang T C, Cui J J, Ou Y L, Dai J X, Wang M L, Liu Q S, Yang Q M. 1983. Breeding of the new variety “DanHai No.1” of Laminaria japonica by using a female haploid clone of the kelp. Journal of Shandong College of Oceanology, 13(4): 63–70. (in Chinese with English abstract)

    Google Scholar 

  • Fang T C, Jiang B Y, Li J J. 1965. Further studies of the genetics of Laminaria frond-length. Oceanologia et Limnologia Sinica, 7(1): 59–66. (in Chinese with English abstract)

    Google Scholar 

  • Fang T C, Ou Y L, Cui J J. 1985. Breeding of hybrid Laminaria “DanZa No.10” -an application of the Laminarian haploid cell clones. Journal of Shandong College of Oceanology, 15(1): 64–72. (in Chinese with English abstract)

    Google Scholar 

  • Fang T C, Wu C Y, Jiang B Y, Li J J, Ren G Z. 1963. The breeding of a new variety of Haidai (Laminaria japonica Aresch.). Science in China, Series A, 12(7): 1011–1018.

    Google Scholar 

  • Fang T C, Zhang D M. 1982. Mr. Otuki and the early history of mariculture of Laminaria japonica in China. Journal of Shandong College of Oceanology, 12(3): 97–98. (in Chinese with English abstract)

    Google Scholar 

  • Fang T C. 1983. Genetic studies for Laminaria japonica in China. Acta Oceanologica Sinica, 5(4): 500–506. (in Chinese)

    Google Scholar 

  • FAO. 2018. The state of world fisheries and aquaculture. Rome, Italy, http://www.fao.org/3/i9540en/I9540EN.pdf.

  • Fu W D, Yao J T, Wang X L, Liu F L, Fu G, Duan D L. 2009. Molecular cloning and expression analysis of a cytosolic Hsp70 gene from Laminaria japonica (Laminariaceae, Phaeophyta). Marine Biotechnology, 11(6): 738–747, https://doi.org/10.1007/s10126-009-9188-z.

    Google Scholar 

  • Gu J G, Sun Y P, Liu Y, Bi Y H, Zhou Z G. 2014. Sex identification and genetic variation of Saccharina (Phaeophyta) gametophytes as revealed by inter-simple sequence repeat (ISSR) markers. Journal of Applied Phycology, 26(1): 635–646, https://doi.org/10.1007/s10811-013-0089-1.

    Google Scholar 

  • Greiner S, Lehwark P, Bock R. 2019. OrganellarGenomeDRAW (OGDRAW) version 1.3.1: expanded toolkit for the graphical visualization of organellar genomes. Nucleic Acids Research, 47: W59–W64.

    Google Scholar 

  • Hafting J T, Craigie J S, Stengel D B, Loureiro R R, Buschmann A H, Yarish C, Edwards M D, Critchley A T. 2015. Prospects and challenges for industrial production of seaweed bioactives. Journal of Phycology, 51(5): 821–837, https://doi.org/10.1111/jpy.12326.

    Google Scholar 

  • Hirata R, Takahashi M, Saga N, Mikami K. 2011. Transient gene expression system established in Porphyra yezoensis is widely applicable in Bangiophycean algae. Marine Biotechnology, 13(5): 1038–1047, https://doi.org/10.1007/s10126-011-9367-6.

    Google Scholar 

  • Hirata R, Uji T, Fukuda S, Mizuta H, Fujiyama A, Tabata S, Saga N. 2014. Development of a nuclear transformation system with a codon-optimized selection marker and reporter genes in Pyropia yezoensis (Rhodophyta). Journal of Applied Phycology, 26(4): 1863–1868, https://doi.org/10.1007/s10811-013-0234-x.

    Google Scholar 

  • Hu Z M, Fraser C. 2015. Seaweed Phylogeography: Adaptation and Evolution of Seaweeds under Environmental Change. Springer Science and Business Media, Dordrecht.

    Google Scholar 

  • Hwang E K, Yotsukura N, Pang S J, Shan T F. 2019. Seaweed breeding programs and progress in eastern Asian countries. Phycologia, 58(5): 484–495, https://doi.org/10.1080/00318884.2019.1639436.

    Google Scholar 

  • Inoue A, Ojima T. 2019. Functional identification of alginate lyase from the brown alga Saccharina japonica. Scientific Reports, 9(1): 4937, https://doi.org/10.1038/s41598-019-41351-6.

    Google Scholar 

  • Inoue A, Satoh A, Morishita M, Tokunaga Y, Miyakawa T, Tanokura M, Ojima T. 2016. Functional heterologous expression and characterization of mannuronan C5-epimerase from the brown alga Saccharina japonica. Algal Research, 16: 282–291, https://doi.org/10.1016/j.algal.2016.03.030.

    Google Scholar 

  • Jiang P, Qin S, Tseng C K. 2002. Expression of hepatitis B surface antigen gene (HBsAg) in Laminaria japonica (Laminariales, Phaeophyta). Chinese Science Bulletin, 47(17): 1438–1440, https://doi.org/10.1360/02tb9317.

    Google Scholar 

  • Kong F N, Zhao H L, Liu W X, Li N, Mao Y X. 2017. Construction of plastid expression vector and development of genetic transformation system for the seaweed Pyropia yezoensis. Marine Biotechnology, 19(2): 147–156, https://doi.org/10.1007/s10126-017-9736-x.

    Google Scholar 

  • Kraan S, Guiry M D. 2000. Molecular and morphological character inheritance in hybrids of Alaria esculenta and A. praelonga (Alariaceae, Phaeophyceae). Phycologia, 39(6): 554–559, https://doi.org/10.2216/i0031-8884-39-6-554.1.

    Google Scholar 

  • Lane C E, Mayes C, Druehl L D, Saunders G W. 2006. A multigene molecular investigation of the kelp (Laminariales, Phaeophyceae) supports substantial taxonomic reorganization. Journal of Phycology, 42(2): 493–512, https://doi.org/10.1111/j.1529-8817.2006.00204.x.

    Google Scholar 

  • Le Corguillé G, Pearson G, Valente M, Viegas C, Gschloess B, Corre E, Bailly X, Peters A F, Jubin C, Vacherie B, Cock J M, Leblanc C. 2009. Plastid genomes of two brown algae, Ectocarpus siliculosus and Fucus vesiculosus: further insights on the evolution of red-algal derived plastids. BMC Evolutionary Biology, 9(1): 253, https://doi.org/10.1186/1471-2148-9-253.

    Google Scholar 

  • Lee J M, Yang E C, Graf L, Yang J H, Qiu H, Zelzion U, Chan C X, Stephens T G, Weber A P M, Boo G H, Boo S M, Kim K M, Shin Y, Jung M, Lee S J, Yim H S, Lee J H, Bhattachara D, Yoon H S. 2018. Analysis of the draft genome of the red seaweed Gracilariopsis chorda provides insights into genome size evolution in Rhodophyta. Molecular Biology and Evolution, 35(8): 1869–1886, https://doi.org/10.1093/molbev/msy081.

    Google Scholar 

  • Lee Y K, Lee H K. 2001. Eukaryotic algal genes and progress in molecular biology of eukaryotic algae. Algae, 16(1): 1–19.

    Google Scholar 

  • Lewis R J, Jiang B Y, Neushul M, Fei X G. 1993. Hapoid parthenogenetic sporophytes of Laminaria japonica (Phaeophyceae). Journal of Phycology, 29(3): 363–369, https://doi.org/10.1111/j.0022-3646.1993.00363.x.

    Google Scholar 

  • Lewis R J. 1996. Chromosomes of the brown algae. Phycologia, 35(1): 19–40, https://doi.org/10.2216/i0031-8884-35-1-19.1.

    Google Scholar 

  • Li D P, Zhou Z G, Liu H H, Wu C Y. 1999. A new method of Laminaria japonica strain selection and sporeling raising by the use of gametophyte clones. Hydrobiologia, 398–399: 473–476, https://doi.org/10.1023/A:1017090130586.

    Google Scholar 

  • Li F C, Qin S, Jiang P, Wu Y, Zhang W. 2009. The integrative expression of GUS gene driven by FCP promoter in the seaweed Laminaria japonica (Phaeophyta). Journal of Applied Phycology, 21(3): 287–293, https://doi.org/10.1007/s10811-008-9366-9.

    Google Scholar 

  • Li Q Y, Wang X L, Zhang J, Yao J T, Duan D L. 2016b. Maternal inheritance of organellar DNA demonstrated with DNA markers in crosses of Saccharina japonica (Laminariales, Phaeophyta). Journal of Applied Phycology, 28(3): 2019–2026, https://doi.org/10.1007/s10811-015-0687-1.

    Google Scholar 

  • Li Q Y, Zhang J, Yao J T, Wang X L, Duan D L. 2016a. Development of Saccharina japonica genomic SSR markers using next-generation sequencing. Journal of AppliedPhycology, 28(2): 1387–1390, https://doi.org/10.1007/s10811-015-0643-0.

    Google Scholar 

  • Li T, Liu F L, Wang F J, Sun X T, Wang W J. 2012. The genetic analysis and evaluate of Saccharina Huangguan No.1. Journal of Qingdao Agricultural University, 29(3): 212–217. (in Chinese with English abstract)

    Google Scholar 

  • Li X J, Cong Y Z, Yang G P, Shi Y Y, Qu S C, Wang G W, Zhang Z Z, Luo S J, Dai H L, Xie J Z, Jiang G L, Liu J L, Wang T Y. 2007a. Trait evaluation and trial cultivation of Dongfang No. 2, the hybrid of a male gametophyte clone of Laminaria longissima (Laminariales, Phaeophyta) and a female one of L. japonica. Journal of Applied Phycology, 19(2): 139–151, https://doi.org/10.1007/s10811-006-9120-0.

    Google Scholar 

  • Li X J, Liu J L, Cong Y Z, Qu S C, Zhang Z Z, Dai H L, Luo S J, Han X B, Huang S S, Wang Q Y, Liang G J, Sun J, Jin Y, Wang D Q, Yang G P. 2008a. Breeding and trial cultivation of Dongfang No.3, a hybrid of Laminaria gametophyte clones with a more than intraspecific but less than interspecific relationship. Aquaculture, 280(1–4): 76–80, https://doi.org/10.1016/j.aquaculture.2008.05.005.

    Google Scholar 

  • Li X J, Yang G P, Shi Y Y, Cong Y Z, Che S, Qu S C, Li Z L. 2008b. Prediction of the heterosis of Laminaria hybrids with the genetic distance between their parental gametophyte clones. Journal of Applied Phycology, 20(6): 1097–1102, https://doi.org/10.1007/s10811-008-9321-9.

    Google Scholar 

  • Li X J, Zhang Z Z, Qu S C, Liang G J, Sun J, Zhao N, Cui C J, Cao Z M, Li Y, Pan J H, Yu S H, Wang Q Y, Li X, Luo S J, Song S F, Guo L, Yang G P. 2016c. Improving seedless kelp (Saccharina japonica) during its domestication by hybridizing gametophytes and seedling-raising from sporophytes. Scientific Reports, 6(1): 21255, https://doi.org/10.1038/srep21255.

    Google Scholar 

  • Li X J, Zhang Z Z, Qu S C, Liang G J, Zhao N, Sun J, Song S F, Cao Z M, Li X, Pan J H, Luo S J, Zhang L, Cui C J, Peng J, Li Y, Wu R N, Zhao J P, Qian R, Wang L Q, Sai S, Yang G P. 2016d. Breeding of an intraspecific kelp hybrid Dongfang No.6 (Saccharina japonica, Phaeophyceae, Laminariales) for suitable processing products and evaluation of its culture performance. Journal of Applied Phycology, 28(1): 439–447, https://doi.org/10.1007/s10811-015-0562-0.

    Google Scholar 

  • Li X, Pang S J, Shan T F. 2017. Genetic diversity and population structure among cultivars of Saccharina japonica currently farmed in northern China. Phycological Research, 65(2): 111–117, https://doi.org/10.1111/pre.12167.

    Google Scholar 

  • Li Y H, Yang Y X, Liu J D, Wang X L, Gao T X, Duan D L. 2007b. Genetic mapping of Laminaria japonica and L. longissima using amplified fragment length polymorphism markers in a “two-way pseudo-testcross” strategy. Journal of Integrative Plant Biology, 49(3): 392–400, https://doi.org/10.1111/j.1744-7909.2007.00397.x.

    Google Scholar 

  • Li Y, Xiao J H, Chen L L, Huang X H, Cheng Z K, Han B, Zhang Q F, Wu C Y. 2018. Rice functional genomics research: past decade and future. Molecular Plant, 11(3): 359–380, https://doi.org/10.1016/j.molp.2018.01.007.

    Google Scholar 

  • Liu F L, Shao Z R, Zhang H N, Liu J D, Wang X L, Duan D L. 2010a. QTL mapping for frond length and width in Laminaria japonica Aresch (Laminarales, Phaeophyta) using AFLP and SSR markers. Marine Biotechnology, 12(4): 386–394, https://doi.org/10.1007/s10126-009-9229-7.

    Google Scholar 

  • Liu F L, Sun X T, Wang F J, Wang W J, Liang Z R, Lin Z L, Dong Z A. 2014a. Breeding, economic traits evaluation, and commercial cultivation of a new Saccharina variety “Huangguan No.1”. Aquaculture International, 22(5): 1665–1675, https://doi.org/10.1007/s10499-014-9772-8.

    Google Scholar 

  • Liu F L, Wang F J, Duan D L. 2012b. EST-SSR markers derived from Laminaria digitata and its transferable application in Saccharina japonica. Journal of Applied Phycology, 24(3): 501–505, https://doi.org/10.1007/s10811-012-9807-3.

    Google Scholar 

  • Liu F L, Wang W J, Sun X T, Liang Z R, Wang F J. 2014b. RNA-seq revealed complex response to heat stress on transcriptomic level in Saccharinajaponica (Laminariales, Phaeophyta). Journal of Applied Phycology, 26(3): 1585–1596, https://doi.org/10.1007/s10811-013-0188-z.

    Google Scholar 

  • Liu F L, Wang W J, Sun X T, Liang Z R, Wang F J. 2015. Conserved and novel heat stress-responsive microRNAs were identified by deep sequencing in Saccharina japonica (Laminariales, Phaeophyta). Plant, Cell & Environment, 38(7): 1357–1367, https://doi.org/10.1111/pce.12484.

    Google Scholar 

  • Liu F L, Wang X L, Liu J D, Fu W D, Duan D L, Yang Y X. 2009a. Genetic mapping of the Laminaria japonica (Laminarales, Phaeophyta) using amplified fragment length polymorphism markers. Journal of Phycology, 45(5): 1228–1233, https://doi.org/10.1111/j.1529-8817.2009.00729.x.

    Google Scholar 

  • Liu F L, Wang X L, Yao J T, Fu W D, Duan D L. 2010b. Development of expressed sequence tag-derived microsatellite markers for Saccharina (Laminaria) japonica. Journal of Applied Phycology, 22(1): 109–111, https://doi.org/10.1007/s10811-009-9426-9.

    Google Scholar 

  • Liu F L, Yao J T, Wang X L, Hu Z M, Duan D L. 2011. Identification of SCAR marker linking to longer frond length of Saccharina japonica (Laminariales, Phaeophyta) using bulked-segregant analysis. Journal of Applied Phycology, 23(4): 709–713, https://doi.org/10.1007/s10811-010-9567-x.

    Google Scholar 

  • Liu F L, Yao J T, Wang X L, Repnikova A, Galanin D A, Duan D L. 2012a. Genetic diversity and structure within and between wild and cultivated Saccharina japonica (Laminariales, Phaeophyta) revealed by SSR markers. Aquaculture, 358-359: 139–145, https://doi.org/10.1016/j.aquaculture.2012.06.022.

    Google Scholar 

  • Liu F, Jin Z, Wang Y, Bi Y P, Melton J T. 2017a. Plastid genome of Dictyopteris divaricata (Dictyotales, Phaeophyceae): understanding the evolution of plastid genomes in brown algae. Marine Biotechnology, 19(6): 627–637, https://doi.org/10.1007/s10126-017-9781-5.

    Google Scholar 

  • Liu F, Pan J, Zhang Z S, Moejes F W. 2018. Organelle genomes of Sargassum confusum (Fucales, Phaeophyceae): mtDNA vs cpDNA. Journal of Applied Phycology, 30(4): 2715–2722, https://doi.org/10.1007/s10811-018-1461-y.

    Google Scholar 

  • Liu F, Pang S J. 2015. Mitochondrial phylogenomics reveals a close relationship between Petalonia fascia (Scytosiphonaceae, Phaeophyceae) and Ectocarpus siliculosus. Journal of Applied Phycology, 27(2): 1021–1028, https://doi.org/10.1007/s10811-014-0386-3.

    Google Scholar 

  • Liu F, Pang S J. 2016. Chloroplast genome of Sargassum horneri (Sargassaceae, Phaeophyceae): comparative chloroplast genomics of brown algae. Journal of Applied Phycology, 28(2): 1419–1426, https://doi.org/10.1007/s10811-015-0609-2.

    Google Scholar 

  • Liu T, Wang X M, Wang G L, Jia S G, Liu G M, Shan G L, Chi S, Zhang J, Yu Y H, Xue T, Yu J. 2019. Evolution of complex thallus alga: genome sequencing of Saccharina japonica. Frontiers in Genetics, 10: 378, https://doi.org/10.3389/fgene.2019.00378.

    Google Scholar 

  • Liu Y S, Li L H, Wu W K, Zhou Z G. 2009b. A SCAR molecular marker specifically related to the female gametophytes of Saccharina (Laminaria) japonica (Phaeophyta). Journal of Phycology, 45(4): 894–897, https://doi.org/10.1111/j.1529-8817.2009.00719.x.

    Google Scholar 

  • Liu Y, Bi Y H, Gu J G, Li L H, Zhou Z G. 2012c. Localization of a female-specific marker on the chromosomes of the brown seaweed Saccharina japonica using fluorescence in situ hybridization. PLoS One, 7(11): e48784, https://doi.org/10.1371/journal.pone.0048784.

    Google Scholar 

  • Liu Y, Bi Y H, Zhou Z G. 2012d. Karyological observation on Saccharina japonica chromosomes stained with DAPI. Journal of Fisheries of China, 36(1): 50–54. (in Chinese with English abstract)

    Google Scholar 

  • Liu Y, Yang Q F, Dong W S, Bi Y H, Zhou Z G. 2017b. Characterization and physical mapping of nuclear ribosomal RNA (rRNA) genes in the haploid gametophytes of Saccharina japonica (Phaeophyta). Journal of Applied Phycology, 29(5): 2695–2706, https://doi.org/10.1007/s10811-017-1206-3.

    Google Scholar 

  • Luan H X, Yao J T, Chen Z H, Duan D L. 2019. The 40s ribosomal protein s6 response to blue light by interaction with SjAUREO in Saccharina japonica. International Journal of Molecular Sciences, 20(10): 2414, https://doi.org/10.3390/ijms20102414.

    Google Scholar 

  • Luttikhuizen P C, van den Heuvel F H M, Rebours C, Witte H J, van Bleijswijk J D L, Timmermans K. 2018. Strong population structure but no equilibrium yet: Genetic connectivity and phylogeography in the kelp Saccharina latissima (Laminariales, Phaeophyta). Ecology and Evolution, 8(8): 4265–4277, https://doi.org/10.1002/ece3.3968.

    Google Scholar 

  • Mikami K. 2014. A technical breakthrough close at hand: feasible approaches toward establishing a gene-targeting genetic transformation system in seaweeds. Frontier in Plant Science, 5: 498, https://doi.org/10.3389/fpls.2014.00498.

    Google Scholar 

  • Morris C A. Nicolaus B, Sampson V, Harwood J L, Kille P. 1999. Identification and characterization of a recombinant metallothionein protein from a marine alga, Fucus vesiculosus. Biochemical Journal, 338(2): 553–560, https://doi.org/10.1042/bj3380553.

    Google Scholar 

  • Nakahara H. 1984. Alternation of generations of some brown algae in unialgal and axenic cultures. Scientific Papers of the Institute of Algological Research, Hokkaido University, 7(2): 77–194.

    Google Scholar 

  • Nakamura Y, Sasaki N, Kobayashi M, Ojima N, Yasuike M, Shigenobu Y, Satomi M, Fukuma Y, Shiwaku K, Tsujimoto A, Kobayashi T, Nakayama I, Ito F, Nakajima K, Sano M, Wada T, Kuhara S, Inouye K, Gojobori T, Ikeo K. 2013. The first symbiont-free genome sequence of marine red alga, Susabi-nori (Pyropia yezoensis). PLoS One, 8(3): e57122, https://doi.org/10.1371/journal.pone.0057122.

    Google Scholar 

  • Neefus C D, Allen B P, Baldwin H P, Mathieson A C, Eckert R T, Yarish C, Miller M A. 1993. An examination of the population genetics of Laminaria and other brown algae in the Laminariales using starch gel electrophoresis. Hydrobiologia, 260-261: 67–79, https://doi.org/10.1007/BF00049005.

    Google Scholar 

  • Nishitsuji K, Arimoto A, Higa Y, Mekaru, M, Kawamitus M, Satoh N, Shoguchi E. 2019. Draft genome of the brown alga, Nemacystus decipiens, Onna-1 strain: fusion of genes involved in the sulfated fucan biosynthesis pathway. Scientific Reports, 9: 4607, https://doi.org/10.1038/s41598-019-40955-2.

    Google Scholar 

  • Nishitsuji K, Arimoto A, Iwai K, Sudo Y, Hisata K, Fujie M, Arakaki N, Kushiro T, Konish T, Shinzato C, Satoh N, Shoguchi E. 2016. A draft genome of the brown alga, Cladosiphon okamuranus, S-strain: a platform for future studies of’ mozuku’ biology. DNA Research, 23(6): 561–570, https://doi.org/10.1093/dnares/dsw039.

    Google Scholar 

  • Nishiyama T, Sakayama H, de Vries J, Bushchmann H, Saint-Marcoux D, Ullrich K K, Haas F B, Vanderstraeten L, Becker D, Lang D, Vosolsobë, Rombauts S, Wihelmsson P K I, Janitza P, Kem R, Heyl A, Rümpler F, Villalobos L A C, Clay J M, Skokan R, Toyoda A, Suzuki Y, Kagoshima H, Schijlen E, Tajeshwar N, Catarino B, Hetherington A J, Saltykova A, Bonnot C, Breuninger H, Symeonidi A, Radhakrishnan G V, van Nieuwerburgh F, Deforce D, Chang C, Karol K G, Hedrich R, Ulvskov P, Glöckner G, Delwiche C F, Petrášek J, van de Peer Y, Friml J, Beilby M, Dolan L, Kohara Y, Sugano S, Fujiyama A, Delaux P M, Quint M, Theiβen G, Hagemann M, Harholt J, Dunand C, Zachgo S, Langdale J, Maumus F, Van Der Straeten D, Gould S B, Rensing S A. 2018. The Chara genome: secondary complexity and implications for plant terretrialization. Cell, 174(2): 448–464.e24, https://doi.org/10.1016/j.cell.2018.06.033.

    Google Scholar 

  • Oertel W, Wichard T, Weissgerber A. 2015. Transformation of Ulva mutabilis (Chlorophyta) by vector plasmids integrating into the genome. Journal of Phycology, 51(5): 963–979, https://doi.org/10.1111/jpy.12336.

    Google Scholar 

  • Oudot-Le Secq M P, Fontaine J M, Rousvoal S, Kloareg B, Loiseaux-de Goër S. 2001. The complete sequence of a brown algal mitochondrial genome, the Ectocarpale Pylaiella littoralis (L.) Kjellm. Journal of Molecular Evolution, 53(2): 80–88, https://doi.org/10.1007/s002390010196.

    Google Scholar 

  • Pang S J, Liu F, Liu Q S, Wang J Q, Sun C B. 2015. Breeding and genetic stability evaluation of the new Saccharina variety “205”. China Fisheries, (10): 59–60.(in Chinese)

  • Pang S J, Wu C Y. 1996. Study on gametophyte vegetative growth of Undaria pinnatifida and its applications. Chinese Journal of Oceanology and Limnology, 14(3): 205–210, https://doi.org/10.1007/BF02850381.

    Google Scholar 

  • Pang Y L, Li Y, Liu Z Y, Cui Y L, Qin S. 2019. Transient expression of the enhanced green fluorescent protein (egfp) gene in Sargassum horneri. Journal of Oceanology and Limnology, 37(2): 651–656, https://doi.org/10.1007/s00343-019-8014-3.

    Google Scholar 

  • Patwary M, van der Meer J P. 1992. Genetics and breeding of cultivated seaweeds. The Korea Journal of Phycology, 7(2): 281–318.

    Google Scholar 

  • Peng J, Zhang L, Li X J, Cui C J, Wu R N, Tian P P, Li Y, Liu Y L. 2016. Development of genic SSR markers from an assembled Saccharina japonica genome. Journal of Applied Phycology, 28(4): 2479–2484, https://doi.org/10.1007/s10811-015-0747-6.

    Google Scholar 

  • Prochnik S E, Umen J, Nedelcu A M, Hallman A, Miller S M, Nishii I, Ferris P, Kuo A, Mitros T, Fritz-Laylin L K, Hellsten U, Chapman J, Simakov O, Rensing S A, Terry A, Pangilinan J, Kapitonov V, Jurka J, Salamov A, Shapiro H, Schmutz J, Grimwood J, Lindquist E, Lucas S, Grigoriev I V, Schmitt R, Kirk D, Rokhsar D S. 2010. Genomic analysis of organismal complexity in the multicellular green alga Volvox carteri. Science, 329(5988): 223–226, https://doi.org/10.1126/science.1188800.

    Google Scholar 

  • Selivanova O N, Levenetz I R, Ogorodnikov V S. 2006. Seaweed resources of the far east of Russia. In: Seaweed resources of the world, Critchley A T, Ohno M, Largo D, et al. eds.

  • Shan T F, Li Q X, Wang X M, Su L, Pang S J. 2019. Assessment of the genetic connectivity between farmed populations on a typical kelp farm and adjacent spontaneous populations of Saccharina japonica (Phaeophyceae, Laminariales) in China. Frontiers in Marine Science, 6: 494, https://doi.org/10.3389/fmars.2019.00494.

    Google Scholar 

  • 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 cultivare and geographically isolated wild populations of Saccharina japonica (Phaeophyta) along the northwest coasts of the pacific. Journal of Applied Phycology, 23(1): 35–45, https://doi.org/10.1007/s10811-010-9530-x.

    Google Scholar 

  • Shan T F, 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. Journal of Applied Phycology, 29(1): 631–638, https://doi.org/10.1007/s10811-016-0888-2.

    Google Scholar 

  • Shao Z R, Liu F L, Li Q Y, Yao J T, Duan D L. 2014b. Characterization of ribulose-1,5-bisphosphate carboxylase/oxygenase and transcriptional analysis of its related genes in Saccharina japonica (Laminariales, Phaeophyta). Chinese Journal of Oceanology and Limnology, 32(2): 377–389, https://doi.org/10.1007/s00343-014-3130-6.

    Google Scholar 

  • Shao Z R, Wang W L, Zhang P Y, Yao J T, Wang F H, Duan D L. 2019a. Genome-wide identification of genes involved in carbon fixation in Saccharina japonica and responses of putative C4-related genes to bicarbonate concentration and light intensity. Plant Physiology & Biochemistry, 137: 75–83, https://doi.org/10.1016/j.plaphy.2019.01.032.

    Google Scholar 

  • Shao Z R, Zhang P Y, Li Q Y, Wang X L, Duan D L. 2014a. Characterization of mannitol-2-dehydrogenase in Saccharina japonica: evidence for a new polyol-specific long-chain dehydrogenases/reductase. PLoS One, 9(5): e97935, https://doi.org/10.1371/journal.pone.0097935.

    Google Scholar 

  • Shao Z R, Zhang P Y, Lu C, Li S X, Chen Z H, Wang X L, Duan D L. 2019b. Transcriptome sequencing of Saccharina japonica sporophytes during whole developmental periods reveals regulatory networks underlying alginate and mannitol biosynthesis. BMC Genomics, 20(1): 975, https://doi.org/10.1186/s12864-019-6366-x.

    Google Scholar 

  • Shendure J, Ji H. 2008. Next-generation DNA sequencing. Nature Biotechnology, 26(10): 1135–1145, https://doi.org/10.1038/nbt1486.

    Google Scholar 

  • Shi W W, Wang L L, Chen J, Ouyang L L, Zhou Z G. 2010. Characterization and differential expression of cbbX gene between female and male gametophytes of Laminaria japonica. Journal of Fisheries of China, 34(1): 80–88. (in Chinese with English abstract)

    Google Scholar 

  • Shi Y Y, Yang G P, Liao M J, Li X J, Cong Y Z, Qu S C, Wang T Y. 2008. Parentage analysis of Dongfang No. 2, a hybrid of a female gametophyte clone of Laminaria japonica (Laminariales, Phaeophyta) and a male clone of L. longissima. Journal of Ocean University of China, 7(2): 193–198, https://doi.org/10.1007/s11802-008-0193-z

    Google Scholar 

  • Shi Y Y, Yang G P, Liu Y J, Liao M J, Cong Y Z. 2007. Development of 18 polymorphic microsatellite DNA markers of Laminaria japonica (Phaeophyceae). Molecular Ecology Notes, 7(4): 620–622, https://doi.org/10.1111/j.1471-8286.2006.01652.x.

    Google Scholar 

  • Shin Y J, Lim J M, Park J H, Choi D W, Hwang M S, Park E J, Min S R, Kim S W, Jeong W J. 2016. Characterization of PyGUS gene silencing in the red macroalga, Pyropia yezoensis. Plant Biotechnology Reports, 10(6): 359–367, https://doi.org/10.1007/s11816-016-0408-5.

    Google Scholar 

  • Speicher M R, Ballard S G, Ward D C. 1996. Karyotyping human chromosomes by combinatorial multi-fluor FISH. Nature Genetics12(4): 368–375, https://doi.org/10.1038/ng0496-368.

    Google Scholar 

  • Su L, Pang S J, Shan T F, Li X. 2017. Large-scale hatchery of the kelp Saccharina japonica: a case study experience at Lvshun in northern China. Journal of Applied Phycology, 29(6): 3003–3013, https://doi.org/10.1007/s10811-017-1154-y.

    Google Scholar 

  • Sun X, Wu J, Wang G C, Kang Y N, Ooi H S, Shen T T, Wang F J, Yang R, Xu N J, Zhao X D. 2018. Genomic analyses of unique carbohydrate and phytohormone metabolism in the macroalga Gracilariopsis lemaneiformis (Rhodophyta). BMC Plant Biology, 18(1): 94, https://doi.org/10.1186/s12870-018-1309-2.

    Google Scholar 

  • Tai S H, Fang T C. 1977. The chromosomes of Laminaria japonica Aresch. Acta Genetica Sinica, 4(4): 325–329. (in Chinese with English abstract)

    Google Scholar 

  • Tseng C K, Sun K Y, Wu C Y. 1955. On the cultivation of Haitai (Laminaria japonica Aresch.) by summering young sporophytes at low temperature. Acta Botanica Sinica, 4(3): 255–264. (in Chinese with English abstract)

    Google Scholar 

  • Tseng C K, Wu C Y, Ren K Z. 1962. The influence of temperature on the growth and development of the Haidai (Laminaria japonica) gametophytes. Oceanologia et Limnologia Sinica, 4(1–2): 22–28. (in Chinese with English abstract)

    Google Scholar 

  • Tseng C K, Wu C Y, Sun K Y. 1957. The effect of temperature on the growth and development of Haitai (Laminaria japonica Aresch.). Acta Botanica Sinica, 6(2): 103–130. (in Chinese with English abstract)

    Google Scholar 

  • Tseng C K. 1981. Commercial cultivation. In: Lobban C S, Wynne M J eds. The Biology of Seaweeds. Blackwell Scientific Publications, Oxford. p.680–725.

    Google Scholar 

  • Wang G L, Tan X L, Shen J L, Li J, Zhang L, Sun J W, Wang B, Weng M L, Liu T. 2011. Development of EST-SSR primers and their practicability test for Laminaria. Acta Oceanologica Sinica, 30(3): 112–117, https://doi.org/10.1007/s13131-011-0125-4.

    Google Scholar 

  • Wang J F, Jiang P, Cui Y L, Deng X Y, Li F C, Liu J G, Qin S. 2010. Genetic transformation in Kappaphycus alvarezii using micro-particle bombardment: a potential strategy for germplasm improvement. Aquaculture International, 18(6): 1027–1034, https://doi.org/10.1007/s10499-010-9320-0.

    Google Scholar 

  • Wang W J, Wang F J, Sun X T, Liu F L, Liang Z R. 2013a. Comparison of transcriptome under red and blue light culture of Saccharina japonica (Phaeophyceae). Planta, 237(4): 1123–1133, https://doi.org/10.1007/s00425-012-1831-7.

    Google Scholar 

  • Wang X L, Chen Z H, Li Q Y, Zhang J, Liu S, Duan D L. 2018. High-density SNP-based QTL mapping and candidate gene screening for yield-related blade length and width in Saccharina japonica (Laminariales, Phaeophyta). Scientific Reports, 8(1): 13591, https://doi.org/10.1038/s41598-018-32015-y.

    Google Scholar 

  • Wang X L, Shao Z R, Fu W D, Yao J T, Hu Q P, Duan D L. 2013b. Chloroplast genome of one brown seaweed, Saccharina japonica (Laminariales, Phaeophyta): its structural features and phylogenetic analyses with other photosynthetic plastids. Marine Genomics, 10: 1–9, https://doi.org/10.1016/j.margen.2012.12.002.

    Google Scholar 

  • Wang X L, Yang Y X, Cong Y Z, Duan D L. 2004. DNA fingerprinting of selected Laminaria (Phaeophyta) gametophytes by RAPD markers. Aquaculture, 238(1–4): 143–153, https://doi.org/10.1016/j.aquaculture.2004.05.007.

    Google Scholar 

  • Wattier R, Maggs C A. 2001. Intraspecific variation in seaweeds: the application of new tools and approaches. Advances in Botanical Research, 35: 171–212, https://doi.org/10.1016/S0065-2296(01)35007-3.

    Google Scholar 

  • Wu C H, Jiang P, Guo Y, Liu J G, Zhao J, Fu H H. 2018. Isolation and characterization of Ulva prolifera actin1 gene and function verification of the 5’ flanking region as a strong promoter. Bioengineered, 9(1): 124–133, https://doi.org/10.1080/21655979.2017.1325041.

    Google Scholar 

  • Wu C Y, Lin G H. 1987. Progress in the genetics and breeding of economic seaweeds in China. Hydrobiologia, 151-152: 57–61, https://doi.org/10.1007/BF00046105.

    Google Scholar 

  • Xu Y B. 2010. Molecular Plant Breeding. CABI, Cambridge, USA.

    Google Scholar 

  • Xuan J S, Feng Y B, Weng M L, Zhao G, Shi J F, Yao J T, Wang X L, Guo B T, Qiao L X, Duan D L, Wang B. 2012. Expressed sequence tag analysis and cloning of trehalose-6-phosphate synthase gene from marine alga Laminaria japonica (Phaeophyta). Acta Oceanologica Sinica, 31(6): 139–148, https://doi.org/10.1007/s13131-012-0260-6.

    Google Scholar 

  • Yabu H, Yasui H. 1991. Chromosome number in four species of Laminaria (Phaeophyta). Japanese Journal of Phycology, 39(2): 185–187.

    Google Scholar 

  • Yabu H. 1973. Alternation of chromosomes in the life history of Laminaria japonica Aresch. Bulletin of the Faculty of Fisheries Hokkaido University, 23(4): 171–176.

    Google Scholar 

  • Yang G P, Sun Y, Shi Y Y, Zhang L, Guo S S, Li B J, Li X J, Li Z L, Cong Y Z, Zhao Y S, Wang W Q. 2009. Construction and characterization of a tentative amplified fragment length polymorphism-simple sequence repeat linkage map of Laminaria (Laminariales, Phaeophyta). Journal of Phycology, 45(4): 873–878, https://doi.org/10.1111/j.1529-8817.2009.00720.x.

    Google Scholar 

  • Yang Q F, Liu L, Liu Y, Zhou Z G. 2017. Telomeric localization of the Arabidopsis-type heptamer repeat, (TTTAGGG)n, at the chromosome ends in Saccharina japonica (Phaeophyta). Journal of Phycology, 53(1): 235–240, https://doi.org/10.1111/jpy.12497.

    Google Scholar 

  • Yang X Q, Li L, Wang X L, Yao J T, Duan D L. 2020. Non-Coding RNAs participate in the regulation of CRY-DASH in the growth and early development of Saccharina japonica (Laminariales, Phaeophyceae). International Journal of Molecular Sciences, 21(1): 309, https://doi.org/10.3390/ijms21010309.

    Google Scholar 

  • Ye N H, Zhang X W, Miao M, Fan X, Zheng Y, Xu D, Wang J F, Zhou L, Wang D S, Gao Y, Wang Y T, Shi W Y, Ji P F, Li D M, Guan Z, Shao C W, Zhuang Z M, Gao Z Q, Qi J, Zhao F Q. 2015. Saccharina genomes provide novel insight into kelp biology. Nature Communications, 6(1): 6986, https://doi.org/10.1038/ncomms7986.

    Google Scholar 

  • Ye R, Yu Z, Shi W W, Gao H J, Bi Y H, Zhou Z G. 2014. Characterization of a-type carbonic anhydrase (CA) gene and subcellular localization of a-CA in the gametophytes of Saccharina japonica. Journal of Applied Phycology, 26(2): 881–890, https://doi.org/10.1007/s10811-013-0221-2.

    Google Scholar 

  • 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. Molecular Phylogenetics and Evolution, 21(2): 231–243, https://doi.org/10.1006/mpev.2001.1009.

    Google Scholar 

  • Yotsukura N, Kawai T, Motomura T, Ichimura T. 2001. Random amplified polymorphic DNA markers for three Japanese Laminarian species. Fisheries Science, 67(5): 857–862, https://doi.org/10.1046/j.1444-2906.2001.00333.x.

    Google Scholar 

  • Yotsukura N, Maeda T, Abe T, Nakaoka M, Kawai T. 2016. Genetic differences among varieties of Saccharina japonica in northern Japan as determined by AFLP and SSR analyses. Journal of Applied Phycology, 28(5): 3043–3055, https://doi.org/10.1007/s10811-016-0807-6.

    Google Scholar 

  • Yotsukura N, Shimizu T, Katayama T, Druehl L D. 2010. Mitochondrial DNA sequence variation of four Saccharina species (Laminariales, Phaeophyceae) growing in Japan. Journal of Applied Phycology, 22(3): 243–251, https://doi.org/10.1007/s10811-009-9452-7.

    Google Scholar 

  • Zhang J, Li W, Qu J Q, Wang X M, Liu C, Liu T. 2015a. Development and characterization of microsatellite markers from an enriched genomic library of Saccharina japonica. Journal of Applied Phycology, 27(1): 479–487, https://doi.org/10.1007/s10811-014-0301-y.

    Google Scholar 

  • Zhang J, Liu T, Bian D P, Zhang L, Li X B, Liu D T, Liu C, Cui J J, Xiao L Y. 2016a. Breeding and genetic stability evaluation of the new Saccharina variety “Ailunwan” with high yield. Journal of Applied Phycology, 28(6): 3413–3421, https://doi.org/10.1007/s10811-016-0810-y.

    Google Scholar 

  • Zhang J, Liu T, Feng R F, Liu C, Chi S. 2015b. Genetic map construction and quantitative trait locus (QTL) detection of six economic traits using an F2 population of the hybrid from Saccharina longissima and Saccharina japonica. PLoS One, 10(5): e0128558, https://doi.org/10.1371/journal.pone.0128588.

    Google Scholar 

  • Zhang J, Liu T, Feng R F, Liu C, Jin Y M, Jin Z H, Song H Z. 2018a. Breeding of the new Saccharina variety “Sanhai” with high yield. Aquaculture, 485: 59–65, https://doi.org/10.1016/j.aquaculture.2017.11.015.

    Google Scholar 

  • Zhang J, Liu T, Rui F P. 2018b. Development of EST-SSR markers derived from transcriptome of Saccharina japonica and their application in genetic diversity analysis. Journal of Applied Phycology, 30(3): 2101–2109, https://doi.org/10.1007/s10811-017-1354-5.

    Google Scholar 

  • Zhang J, Liu Y, Yu D, Song H Z, Cui J J, Liu T. 2011. Study on high-temperature-resistant and high-yield Laminaria variety “Rongfu”. Journal of Applied Phycology, 23(2): 165–171, https://doi.org/10.1007/s10811-011-9650-y.

    Google Scholar 

  • Zhang J, Wang X L, Yao J T, Li Q Y, Liu F L, Yotsukura N, Krupnova T N, Duan D L. 2017. Effect of domestication on the genetic diversity and structure of Saccharina japonica populations in China. Scientific Reports, 7(1): 42158, https://doi.org/10.1038/srep42158.

    Google Scholar 

  • Zhang J, Wang X L, Yao J T, Yotsukura N, Duan D L. 2019a. Screening of polymorphic microsatellites and their application for Saccharina angustata and Saccharina longissima population genetic analysis. Journal of Applied Phycology, 31(5): 3295–3301, https://doi.org/10.1007/s10811-019-01798-6.

    Google Scholar 

  • Zhang J, Yao J T, Hu Z M, Jueterbock A, Yotsukura N, Krupnova T N, Nagasato C, Duan D L. 2019b. Phylogeographic diversification and postglacial range dynamics shed light on the conservation of the kelp Saccharina japonica. Evolutionary Applications, 12(4): 791–803, https://doi.org/10.1111/eva.12756.

    Google Scholar 

  • Zhang J, Yao J T, Sun Z M, Fu G, Galanin D A, Nagasato C, Motomura T, Hu Z M, Duan D L. 2015c. Phylogeographic data revealed shallow genetic structure in the kelp Saccharina japonica (Laminariales, Phaeophyta). BMC Evolutionary Biology, 15(1): 237, https://doi.org/10.1186/s12862-015-0517-8.

    Google Scholar 

  • Zhang L, Cui C J, Li Y, Wu H, Li X J. 2018c. A genome screen for the development of sex-specific DNA markers in Saccharina japonica. Journal of Applied Phycology, 30(2): 1239–1246, https://doi.org/10.1007/s10811-017-1295-z.

    Google Scholar 

  • Zhang L, Li J K, Wu H, Li Y X. 2019c. Isolation and expression analysis of a candidate gametophyte sex determination gene (SJHMG) of kelp (Saccharina japonica). Journal of Phycology, 55(2): 343–351, https://doi.org/10.1111/jpy.12821.

    Google Scholar 

  • Zhang L, Peng J, Li X J, Cui C J, Sun J, Yang G P. 2016b. Characterization of genome-wide microsatellites of Saccharina japonica based on a preliminary assembly of Illumina sequencing reads. Journal of Ocean University of China, 15(3): 523–532, https://doi.org/10.1007/s11802-016-2945-5.

    Google Scholar 

  • Zhang L, Peng J, Li X J, Liu Y L, Cui C J, Wu H, Wu R N, Tian P P, Li Y. 2014. Development of 27 trinucleotide microsatellite markers for Saccharina japonica using next generation sequencing technology. Conservation Genetics Resource, 6(2): 341–344, https://doi.org/10.1007/s12686-013-0089-0.

    Google Scholar 

  • Zhang L, Wang X M, Liu T, Wang G L, Chi S, Liu C, Wang H Y. 2015d. Complete plastid genome sequence of the brown alga Undaria pinnatifida. PLoS One, 10(10): e0139366, https://doi.org/10.1371/journal.pone.0139366.

    Google Scholar 

  • Zhang L, Wang X M, Liu T, Wang H Y, Wang G L, Chi S, Liu C. 2015e. Complete plastid genome of the brown alga Costaria costata (Laminariales, Phaeophyceae). PLoS One, 10(10): e0140144, https://doi.org/10.1371/journal.pone.0140144.

    Google Scholar 

  • Zhang N, Zhang L N, Tao Y, Guo L, Sun J, Li X, Zhao N, Peng J, Li X J, Zeng L, Chen J S, Yang G P. 2015f. Construction of a high density SNP linkage map of kelp (Saccharina japonica) by sequencing Taq I site associated DNA and mapping of a sex determining locus. BMC Genomics, 16(1): 189, https://doi.org/10.1186/s12864-015-1371-1.

    Google Scholar 

  • Zhang P Y, Shao Z R, Jin W H, Duan D L. 2016c. Comparative characterization of two GDP-mannose dehydrogenase genes from Saccharina japonica (Laminariales, Phaeophyceae). BMC Plant Biology, 16(1): 62, https://doi.org/10.1186/s12870-016-0750-3.

    Google Scholar 

  • Zhang P Y, Shao Z R, Li L, Liu S, Yao J L, Duan D L. 2018d. Molecular characterisation and biochemical properties of phosphomannomutase/phosphoglucomutase (PMM/ PGM) in the brown seaweed Saccharina japonica. Journal of Applied Phycology, 30(4): 2687–2696, https://doi.org/10.1007/s10811-018-1460-z.

    Google Scholar 

  • Zhang Q S, Qu S C, Cong Y Z, Luo S J, Tang X X. 2008a. High throughput culture and gametogenesis induction of Laminaria japonica gametophyte clones. Journal of Applied Phycology, 20(2): 205–211, https://doi.org/10.1007/s10811-007-9220-5.

    Google Scholar 

  • Zhang Q S, Tang X X, Cong Y Z, Qu S C, Luo S J, Yang G P. 2007. Breeding of an elite Laminaria variety 90-1 through inter-specific gametophyte crossing. Journal of Applied Phycology, 19(4): 303–311, https://doi.org/10.1007/s10811-006-9137-4.

    Google Scholar 

  • Zhang Y C, Jiang P, Gao J T, Liao J M, Sun S J, Shen Z L, Qin S. 2008b. Recombinant expression of rt-PA gene (encoding reteplase) in gametophytes of the seaweed Laminaria japonica (Laminariales, Phaeophyta). Science in China Series C: Life Sciences, 51(12): 1116–1120, https://doi.org/10.1007/s11427-008-0143-4.

    Google Scholar 

  • Zhou L R, Dai J X, Shen S D. 2004. An improved chromosome preparation from male gametophyte of Laminaria japonica (Heterokontophyta). Hydrobiologia, 512(1–3): 141–144, https://doi.org/10.1007/978-94-007-0944-7_18.

    Google Scholar 

  • Zhou W, Hu Y Y, Sui Z H, Fu F, Wang J G, Chang L P, Guo W H, Li B B. 2013. Genome survey sequencing and genetic background characterization of Gracilariopsis lemaneiformis (Rhodophyta) based on next-generation sequencing. PLoS One, 8(7): e69909, https://doi.org/10.1371/journal.pone.0069909.

    Google Scholar 

Download references

Acknowledgment

We thank anonymous reviewers for their critical comments and suggestions for this paper, and Dr. Alan T Critchley for the help in English revision.

Author information

Authors and Affiliations

  1. Key Lab of Experimental Marine Biology, Institute of Oceanology, Center for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao, 266071, China

    Xiuliang Wang, Jianting Yao, Jie Zhang & Delin Duan

  2. Lab for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266071, China

    Xiuliang Wang, Jianting Yao, Jie Zhang & Delin Duan

Authors
  1. Xiuliang Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jianting Yao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jie Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Delin Duan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Delin Duan.

Additional information

Supported by the National Natural Science Foundation of China (Nos. 31772848, 31900279) and the Joint Research Project between China and Japan (No. 2017YFE0130900)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, X., Yao, J., Zhang, J. et al. Status of genetic studies and breeding of Saccharina japonica in China. J. Ocean. Limnol. 38, 1064–1079 (2020). https://doi.org/10.1007/s00343-020-0070-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00343-020-0070-1

Keyword

Search

Navigation