Abstract
Saccharina japonica is an important cultured marine brown alga and it has been the subject of intensive genetic improvement during its domestication and farming. However, there are limited credible and effective sex markers to identify the sex of gametophytes and sporophytes derived from normal hybridization or monogenesis. In the present study, the transcriptomic and genomic sequences of S. japonica were screened by 15 sex-determining region (SDR) genes from a model brown alga (Ectocarpus), and six cDNA sequences and their corresponding genomic sequences were identified. Thirteen primer pairs were designed from the coding region of six genomic sequences and subsequently tested on gametophytes of S. japonica. From these regions, four novel male-specific markers were developed, which derived from S. japonica genomic sequences JXRI01001736 and JXRI01002827, corresponding to a male-specific SDR gene and a gametologue SDR gene in Ectocarpus, respectively. In addition, an existing female marker (M_68_58_2) for Macrocystis pyrifera and Undaria pinnatifida, derived from the Ectocarpus SDR gene, could also be used as a female-specific marker for S. japonica. The results of the present study not only demonstrate an important new tool to determine the sex of gametophytes and distinguish between diploid sporophytes and partheno-sporophytes in breeding programmes but also provide insight into the sex-determination system for S. japonica, including the identification of sex chromosomes, SDR, and SDR genes and evolution of sex chromosomes.
Similar content being viewed by others
References
Ahmed S, Cock JM, Pessia E, Luthringer R, Cormier A, Robuchon M, Sterck L, Peters AF, Dittami SM, Corre E, Valero M, Aury JM, Roze D, Van de Peer Y, Bothwell J, Marais GA, Coelho SM (2014) A haploid system of sex determination in the brown alga Ectocarpus sp. Curr Biol 24:1945–1957
Bartsch I, Wiencke C, Bischof K, Buchholz CM, Buck BH, Eggert A, Feuerpfeil P, Hanelt D, Jacobsen S, Karez R, Karsten U, Molis M, Roleda MY, Schubert H, Schumann R, Valentin K, Weinberger F, Wiese J (2008) The genus Laminaria sensu lato: recent insights and developments. Eur J Phycol 43:1–86
Bello N, Sánchez A (1999) The identification of a sex-specific DNA marker in the ostrich using a random amplified polymorphic DNA (RAPD) assay. Mol Ecol 8:667–669
Bull J (1978) Sex chromosomes in haploid dioecy: a unique contrast to Muller’s theory for diploid dioecy. Am Nat 112:245–250
Chen SL, Deng SP, Tian YS, Wang QY, Zhuang ZM, Sha ZX, JY X (2007) Isolation of female-specific AFLP markers and molecular identification of genetic sex in half-smooth tongue sole (Cynoglossus semilaevis). Mar Biotechnol 9:273–280
Chen SL, Ji XS, Shao CW, Li WL, Yang JF, Liang Z, Liao XL, GB X, Xu Y, Song WT (2012) Induction of mitogynogenetic diploids and identification of WW super-female using sex-specific SSR markers in half-smooth tongue sole (Cynoglossus semilaevis). Mar Biotechnol 14:120–128
Elmeer K, Mattat I (2012) Marker-assisted sex differentiation in date palm using simple sequence repeats. 3 Biotech 2:241–247
Fang TC, WU CY, Jiang BY, Li JJ, Ren KZ (1962) The breeding of a new breed of Haidai (Laminaria japonica Aresch) and its preliminary genetic analysis. Acta Bot Sinica 10:197–209 (in Chinese with English abstract)
Fang Z, Ou Y, Cui J, Dai J (1978) Success in culturing clones of the gametophytes of Laminaria japonica. Trans Sci 2:115–116 (in Chinese with English abstract)
Fowler BLS, Buonaccorsi VP (2016) Genomic characterization of sex-identification markers in Sebastes carnatus and S. chrysomelas rockfish. Mol Ecol 25:2165–2175
Gamble T, Zarkower D (2014) Identification of sex-specific molecular markers using restriction site associated DNA sequencing. Mol Ecol Resour 14:902–913
Griffiths R, Orr K (1999) The use of amplified fragment length polymorphism (AFLP) in the isolation of sex-specific markers. Mol Ecol 8:671–674
Griffiths R, Orr K, Adam A (2000) DNA sex identification in the three-spined stickleback. J Fish Biol 57:1331–1334
Koressaar T, Remm M (2007) Enhancements and modifications of primer design program Primer3. Bioinformatics 23:1289–1291
Korpelainen H, Bisang I, Hedenäs L, Kolehmainen J (2008) The first sex-specific molecular marker discovered in the moss Pseudocalliergon trifarium. J Hered 99:581–587
Lamatsch DK, Adolfsson S, Senior AM, Christiansen G, Pichler M, Ozaki Y, Smeds L, Schartl M, Nakagawa S (2015) A transcriptome derived female-specific marker from the invasive Western mosquitofish (Gambusia affinis). PLoS One 10(2):e0118214
Lee B, Penman D, Kocher T (2003) Identification of a sex-determining region in Nile tilapia (Oreochromis niloticus) using bulked segregant analysis. Anim Genet 34:379–383
Li XJ, Cong YZ, Yang GP, Shi Y, Qu S, Li Z, Wang G, Zhang Z, Luo S, Dai H, Xie J, Jiang G, Liu J, Wang T (2007) 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. J Appl Phycol 19:139–151
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 less than interspecific relationship. Aquaculture 280:76–80
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 (2015) 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
Li X, Zhang Z, Qu S, Liang G, Sun J, Zhao N, Cui C, Cao Z, Li Y, Pan J, Yu S, Wang Q, Li X, Luo S, Song S, Guo L, Yang G (2016) Improving seedless kelp (Saccharina japonica) during its domestication by hybridizing gametophytes and seedling-raising from sporophytes. Sci Rep UK 6:21255
Li YH, Wang HP, Yao H, O’Bryant P, Rapp D, Guo L, Wly EA et al (2017) De novo transcriptome sequencing and analysis of male, pseudo-male and female yellow perch, Perca flavescens. PLoS One 12:e0171187
Lipinska A, Cormier A, Luthringer R, Peters AF, Corre E, Gachon CMM, Cock JM, Coelho SM (2015a) Sexual dimorphism and the evolution of sex-biased gene expression in the brown alga Ectocarpus. Mol Biol Evol 32:1581–1597
Lipinska A, Ahmed S, Peters AF et al (2015b) Development of PCR-based markers to determine the sex of kelps. PLoS One 10:e0140535
Liu YS, Li LH, WK W, Zhou ZG (2009) A scar molecular marker specifically related to the female gametophytes of Saccharia (Laminaria) japonica (Phaeophyta). J Phycol 45:894–897
Liu Y, Bi YH, JG G, Faugeron S, Cock JM, Coelho SM (2012) Localization of a female-specific marker on the chromosomes of the brown seaweed Saccharina japonica using fluorescence in situ hybridization. PLoS One 7:e48784
Petrella V, Aceto S, Musacchia F, Colonna V, Robinson M, Benes V, Cicotti G, Bongiorno G, Gradoni L, Volf P, Salvemini M (2015) De novo assembly and sex-specific transcriptome profiling in the sand fly Phlebotomus perniciosus (Diptera, Phlebotominae), a major old world vector of Leishmania infantum. BMC Genomics 16:847
Scoggan J, Zhuang Z, Wang F (1989) Laminaria seafarming in China: training manual 89/5 (RAS/86/024). Qingdao, China
Sim MC, Lim PE, Gan SY, Phang SM (2007) Identification of random amplified polymorphic DNA (RAPD) marker for differentiating male from female and sporophytic thalli of Gracilaria changii (Rhodophyta). J Appl Phycol 19:763–769
Stehlik I, Blattner FR (2004) Sex-specific SCAR markers in the dioecious plant Rumex nivalis (Polygonaceae) and implications for the evolution of sex chromosomes. Theor Appl Genet 108:238–242
Tai CH, Fang TC (1976) Some preliminary observations on the parthenogenesis in Laminaria japonica Aresch. Acta Genet Sin 3:32–38 (in Chinese with English abstract)
Tian ZP, Yuan BJ (1989) Test report of breeding of a new kelp variety “Zaohoucheng no. 1”. Mariculture 1:7–16 (in Chinese)
Tseng CK (2001) Algal biotechnology industries and research activities in China. J Appl Phycol 13:375–380
Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3—new capabilities and interfaces. Nucleic Acids Res 40(15):e115
Yabu H, Yasui H (1991) Chromosome number in four species of Laminaria (Phaeophyta). Jpn J Phycol 39:185–187
Yang G, Sun Y, Shi Y, Zhang L, Guo S, Li B, Li X, Li Z, Cong Y, Zhao Y, Wang W (2009) Construction and characterization of a tentative amplified fragment length polymorphism-simple sequence repeat linkage map of Laminaria (Laminariales, Phaeophyta). J Phycol 45:873–878
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 6:7986. https://doi.org/10.1038/ ncomms7986
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. J Appl Phycol 19:303–311
Zhang L, Cui C, Li X, Zhang Z, Luo S, Liang G, Liu Y, Yang G (2013) Effect of temperature on the development of Saccharina japonica gametophytes. J Appl Phycol 25:261–267
Zhang N, Zhang LN, Tao Y, Guo L, Sun J, Li X, Zhao N, Peng J, Li X, Zeng L, Chen J, Yang G (2015) 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 16:189
Zhou LR, Dai JX, Shen SD (2004) An improve chromosome preparation from male gametophyte of Laminaria japonica (Heterokontophyta). Hydrobiologia 512:141–144
Funding
This study was supported by the National Natural Sciences Foundation of China (Grant No.: 41606184), Shandong Province Higher Educational Science and Technology Program (Grant No.: J15LE14), Qingdao Applied Basic Research Project (Grant No.: 14-2-4-71-jch), Shandong Province Agriculture Seed Project (Grand No.: 2016LZGC024), and Agricultural Scientific and Technological Innovation Project of Shandong Academy of Agricultural Sciences (Grant No.: CXGC2016B10).
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
Zhang, L., Cui, C., Li, Y. et al. A genome screen for the development of sex-specific DNA markers in Saccharina japonica . J Appl Phycol 30, 1239–1246 (2018). https://doi.org/10.1007/s10811-017-1295-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10811-017-1295-z