Skip to main content
Log in

Novel implications on the genetic structure of representative populations of Saccharina japonica (Phaeophyceae) in the Northwest Pacific as revealed by highly polymorphic microsatellite markers

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

Although the original Saccharina japonica populations in China are assumed to have been accidentally introduced from Japan in 1920s, few investigations have been performed to prove it. Genetic structure analysis is expected to shed light on this question. In the present study, 11 highly polymorphic microsatellite markers were employed to analyze the genetic structure of representative populations of S. japonica in the Northwest Pacific, including the four varieties from Japan. Populations from China had a much lower level of genetic diversity than the ones from Japan in terms of the number of alleles, private alleles and locally common alleles, and the values of heterozygosity, suggestive of the founder effect in the introduced populations. Both the Bayesian model-based and genetic distance-based analyses revealed three major clusters: (1) S. japonica var. japonica, var. religiosa, and var. ochotensis from Hokkaido, as well as the populations from Korea and Russia; (2) populations from China; and (3) var. diabolica. Saccharina japonica var. diabolica harbored the highest number of private alleles, with three of them having a frequency of 1.00 at three loci, which have the potential to be used as specific markers to distinguish this variety from others. Significant genetic differentiation was found between almost all the populations except for a few cultivated populations from China. Populations from China were most closely related to S. japonica var. japonica, which was in turn most close to var. religiosa and the Korean population. The microsatellite markers used in this study were shown to be polymorphic enough to decipher the subtle genetic structure of S. japonica, including the different varieties.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Earl DA, vonHoldt BM (2011) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Article  Google Scholar 

  • Emanuelli F, Lorenzi S, Grzeskowiak L, Catalano V, Stefanini M, Troggio M, Myles S, Martinez-Zapater JM, Zyprian E, Moreira FM (2013) Genetic diversity and population structure assessed by SSR and SNP markers in a large germplasm collection of grape. BMC Plant Biol 13:39

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinformatics Online 1:47

    CAS  Google Scholar 

  • Fishery Bureau of Ministry of Agriculture of China (2014) China fishery statistical yearbook, 2014. China Agriculture Press, Beijing, p 29 (in Chinese)

    Google Scholar 

  • Hedgecock D, Sly F (1990) Genetic drift and effective population sizes of hatchery-propagated stocks of the Pacific oyster, Crassostrea gigas. Aquaculture 88:21–38

    Article  Google Scholar 

  • Lane CE, Mayes C, Druehl LD, Saunders GW (2006) A multi-gene molecular investigation of the kelp (Laminariales, Phaeophyceae) supports substantial taxonomic re-organization. J Phycol 42:493–512

    Article  CAS  Google Scholar 

  • Li HJ (1990) Notes on the Laminaria raft cultivation method. Mariculture 1(2):41–48 (in Chinese)

    Google Scholar 

  • Li X, Liu J, Cong Y, Qu S, Zhang Z, Dai H, Luo S, Han X, Huang S, Wang Q, Liang G, Sun J, Jin Y, Wang D, Yang G (2008) 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 280:76–80

    Article  Google Scholar 

  • Li J, Pang S, Liu F, Shan T, Gao S (2013) Spermatozoid life-span of two brown seaweeds, Saccharina japonica and Undaria pinnatifida, as measured by fertilization efficiency. Chin J Oceanol Limnol 31:774–781

    Article  Google Scholar 

  • Li Q, Zhang J, Yao J, Wang X, Duan D (2016a) Development of Saccharina japonica genomic SSR markers using next-generation sequencing. J Appl Phycol 28:1387–1390

    Article  CAS  Google Scholar 

  • Li X, Zhang Z, Qu S, Liang G, Zhao N, Sun J, Song S, Cao Z, Li X, Pan J, Luo S, Zhang L, Cui C, Peng J, Li Y, Wu R, Zhao J, Qian R, Wang L, Sai S, Yang G (2016b) Breeding of an intraspecific kelp hybrid Dongfang no. 6 (Saccharina japonica, Phaeophyceae, Laminariales) for suitable processing products and evaluation of its culture performance. J Appl Phycol 28:439–447

    Article  Google Scholar 

  • Liu ZJ, Cordes JF (2004) DNA marker technologies and their applications in aquaculture genetics. Aquaculture 238:1–37

    Article  CAS  Google Scholar 

  • Liu F, Wang X, Yao J, Fu W, Duan D (2009) Development of expressed sequence tag-derived microsatellite markers for Saccharina (Laminaria) japonica. J Appl Phycol 22:109–111

    Article  Google Scholar 

  • Liu F, Yao J, Wang X, Repnikova A, Galanin DA, Duan D (2012) Genetic diversity and structure within and between wild and cultivated Saccharina japonica (Laminariales, Phaeophyta) revealed by SSR markers. Aquaculture 358–359:139–145

    Article  Google Scholar 

  • Maeda T, Yotsukura N (2013) Development of microsatellite markers for Saccharina japonica by dual-suppression PCR. Algal Res 6:67–71

    Google Scholar 

  • Miyabe K (1902) Laminariaceae. Hokkaido Suisan Chosahokoku. Hokkaido Shokuminbu 3:1–60 (in Japanese)

    Google Scholar 

  • Nei M (1972) Genetic distance between populations. Am Nat 106:283–292

    Article  Google Scholar 

  • Pang SJ, Jin ZH, Sun JZ, Gao SQ (2007) Temperature tolerance of young sporophytes from two populations of Laminaria japonica revealed by chlorophyll fluorescence measurements and short-term growth and survival performances in tank culture. Aquaculture 262:493–503

    Article  Google Scholar 

  • Peakall R, Smouse PE (2006) Genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research--an update. Bioinformatics 28:2537–2539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Samuel AF, Drucker AG, Andersen SB, Simianer H, van Zonneveld M (2013) Development of a cost-effective diversity-maximising decision-support tool for in situ crop genetic resources conservation: the case of cacao. Ecol Econ 96:155–164

    Article  Google Scholar 

  • Shan TF, Liu F, Liu QS, Pang SJ (2011a) An overview of the “summer sporeling” technique of Saccharina japonica in China. J Agric Sci Technol 13(2):129–134 (in Chinese with English abstract)

    Google Scholar 

  • Shan TF, Pang SJ, Zhang YR, Yakovleva IM, Skriptsova AV (2011b) 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

    Article  Google Scholar 

  • Shi Y, Yang G, Liu Y, Liao M, Li X, Cong Y (2007) Development of 18 polymorphic microsatellite DNA markers of Laminaria japonica (Phaeophyceae). Mol Ecol Notes 7:620–622

    Article  CAS  Google Scholar 

  • Sitther V, Zhang D, Harris DL, Yadav AK, Zee FT, Meinhardt LW, Dhekney SA (2014) Genetic characterization of guava (Psidium guajava L.) germplasm in the United States using microsatellite markers. Genet Resour Crop Evol 61:829–839

    Article  CAS  Google Scholar 

  • Tseng CK (2001) Algal biotechnology industries and research activities in China. J Appl Phycol 13:375–380

    Article  Google Scholar 

  • Tseng CK, Zhang JF (1952) Economic seaweeds in the north of China. J Shandong Univ 2:57–82 (in Chinese with English abstract)

    Google Scholar 

  • Wang L, Zhang H, Song L, Guo X (2007) Loss of allele diversity in introduced populations of the hermaphroditic bay scallop Argopecten irradians. Aquaculture 271:252–259

    Article  CAS  Google Scholar 

  • 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 6:6986

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yotsukura N (2005) Molecular phylogeny of advanced kelps (Laminariales, Phaeophyceae) growing in Japan. Nat Hist Res Spec 8:69–81

    Google Scholar 

  • Yotsukura N, Kawai T, Kawashima S, Ebata H, Ichimura T (2006) Nucleotide sequences diversity of the 5S rDNA spacer in the simple blade genera Laminaria, Cymathaere and Kjellmaniella (Laminariales, Phaeophyceae) from northern Japan. Phycol Res 54:269–279

    Article  CAS  Google Scholar 

  • Yotsukura N, Kawashima S, Kawai T, Abe T, Druehl L (2008) A systematic re-examination of four Laminaria species: L. japonica, L. religiosa, L. ochotensis and L. diabolica. J Jpn Bot 83:165–176

    Google Scholar 

  • Yotsukura N, Shimizu T, Katayama T, Druehl LD (2010) Mitochondrial DNA sequence variation of four Saccharina species (Laminariales, Phaeophyceae) growing in Japan. J Appl Phycol 22:243–251

    Article  CAS  Google Scholar 

  • Yu Z, Guo X (2004) Genetic analysis of selected strains of eastern oyster (Crassostrea virginica Gmelin) using AFLP and microsatellite markers. Mar Biotechnol 6:575–586

    Article  CAS  PubMed  Google Scholar 

  • Zane L, Bargelloni L, Patarnello T (2002) Strategies for microsatellite isolation: a review. Mol Ecol 11:1–16

    Article  CAS  PubMed  Google Scholar 

  • Zhang QS, Tang XX, Cong YZ, Qu SC, Luo SJ, Yang GP (2007) Breeding of an elite Laminaria variety 90–1 through inter-specific gametophyte crossing. J Appl Phycol 19:303–311

    Article  Google Scholar 

  • Zhang QS, Yuan SY, Cong YZ, Qu SC, Yang GP (2008) AFLP analysis of the gametophyte clones derived from introduced Laminaria (Phaeophyta) and cultured varieties of China. Periodical Ocean Univ China 3:016

    Google Scholar 

  • Zhang J, Li W, Qu J, Wang X, Liu C, Liu T (2014a) Development and characterization of microsatellite markers from an enriched genomic library of Saccharina japonica. J Appl Phycol 27:479–487

    Article  Google Scholar 

  • Zhang L, Peng J, Li X, Liu Y, Cui C, Wu H, Wu R, Tian P, Li Y (2014b) Development of 27 trinucleotide microsatellite markers for Saccharina japonica using next generation sequencing technology. Conserv Genet Resour 6:341–344

    Article  CAS  Google Scholar 

  • Zhang J, Yao JT, Sun ZM, Fu G, Galanin DA, Nagasato C, Motomura T, Hu ZM, Duan DL (2015) Phylogeographic data revealed shallow genetic structure in the kelp Saccharina japonica (Laminariales, Phaeophyta). BMC Evol Biol 15:237

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao XB, Pang SJ, Liu F, Shan TF, Li J, Gao SQ, Kim HG (2016) Intraspecific crossing of Saccharina japonica using distantly related unialgal gametophytes benefits kelp farming by improving blade quality and productivity at Sanggou Bay, China. J Appl Phycol 28:449–455

    Article  Google Scholar 

  • Zonneveld M, Scheldeman X, Escribano P, Viruel MA, Van Damme P, Garcia W, Tapia C, Romero J, Siguenas M, Hormaza JI (2012) Mapping genetic diversity of cherimoya (Annona cherimola Mill.): application of spatial analysis for conservation and use of plant genetic resources. PLoS One 7(1):e29845

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

The authors would like to thank Nobu Nagai for his patient assistance in microsatellite genotyping procedure and Masumi Kounoe, Hiromi Kato, Seiko Tamano, and Tadashi Kawai for their kind help in sample collection and handling. Special thanks go to Xia Li for her constructive suggestions in data analysis. This study was supported by a Fellowship Program for Overseas Researchers granted to Tifeng Shan by Hokkaido University, the scientific and technological innovation project from Qingdao National Laboratory for Marine Science and Technology (No. 2015ASKJ01), the Open Fund of Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology (No. OF2015N010), the STS program from the Chinese Academy of Sciences, and a project from the National Infrastructure of Fishery Germplasm Resource (2016DKA30470).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shaojun Pang.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Table S1

(DOCX 41 kb)

Table S2

(DOCX 17 kb)

Table S3

(DOCX 16 kb)

Table S4

(DOCX 17 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shan, T., Yotsukura, N. & Pang, S. 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 (2017). https://doi.org/10.1007/s10811-016-0888-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-016-0888-2

Keywords

Navigation