Skip to main content

Morphological and genetic analyses of the current major cultivars of Undaria pinnatifida at Lvshun, Dalian, the principal farming region in North China

Abstract

Close to 66% of the annual national production of the brown alga Undaria pinnatifida, about 115 thousand tonnes (fresh weight), is produced through farming in Liaoning Province in north China. To clarify the agronomic characters and genetic differences of currently farmed U. pinnatifida, we investigated three major farmed cultivars in combination with other traditional ones focusing specially on sporophylls, one of the principal end products in a typical farm at Lvshun, Dalian city. Results showed that these cultivars differ in timing of maturation and are arranged to be harvested in sequence in the farm to diversify the periods of harvesting and processing. Sporophyll fresh weight and the stipe width are positively correlated with the growth of the plant. Ten neutral microsatellite markers were used to assess relationships among major farmed cultivars. Both genetic distance and Bayesian model-based analyses showed that there was genetic differentiation among C1, C2, and other traditional cultivars. C3 showed the highest genetic variations in major farmed cultivars, with three private alleles and a mean expected heterozygosity of 0.817. In general, prominent genetic divergences were found among different cultivars confirming the effect of consecutive selection, while weak relationships were observed between sporophyll forms and genotypes.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Abbreviations

TL:

Total length

BL:

Blade length

TW:

Total width

UBW:

Undivided blade width

SW:

Stipe width

SPL:

Sporophyll length

SPW:

Sporophyll width

DSB:

Distance between sporophyll and blade

TFW:

Total fresh weight

SFW:

Sporophyll fresh weight

BA:

Blade area

AGR:

Absolute growth rate

References

  1. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 57:289–300

    Google Scholar 

  2. Castric-Fey A, Beaupoil C, Bouchain J, Pradier E, L’Hardy-Halos MT (1999) The introduced alga Undaria pinnatifida (Laminariales, Alariaceae) in the rocky shore ecosystem of the St Malo area: morphology and growth of the sporophyte. Bot Mar 42:71–82

    Google Scholar 

  3. Choi CG, Oh SJ, Kang IJ, Kang IJ (2009) Growth and morphological characteristics of Undaria pinnatifida in the cultivation ground at Busan, Korea. J Fac Agric Kyushu Univ 54:47–51

    Article  Google Scholar 

  4. De Leij R, Epstein G, Brown MP, Smale DA (2017) The influence of native macroalgal canopies on the distribution and abundance of the non-native kelp Undaria pinnatifida in natural reef habitats. Mar Biol 164:156

    Article  Google Scholar 

  5. Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Article  Google Scholar 

  6. Epstein G, Smale DA (2017) Undaria pinnatifida : a case study to highlight challenges in marine invasion ecology and management. Ecol Evol 7:8624–8642

    PubMed  PubMed Central  Article  Google Scholar 

  7. Epstein G, Smale DA (2018) Environmental and ecological factors influencing the spillover of the non-native kelp, Undaria pinnatifida, from marinas into natural rocky reef communities. Biol Invasions 20:1049–1072

    PubMed  Article  PubMed Central  Google Scholar 

  8. 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

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  9. Hunt R (1982) Plant growth curves. The functional approach to plant growth analysis. Edward Arnold Ltd, London

    Google Scholar 

  10. Hurtado AQ, Neish IC, Critchley AT (2019) Phyconomy: the extensive cultivation of seaweeds, their sustainability and economic value, with particular reference to important lessons to be learned and transferred from the practice of eucheumatoid farming. Phycologia 58:472–483

    Article  Google Scholar 

  11. Hwang EK, Yotsukura N, Pang SJ, Su L, Shan TF (2019) Seaweed breeding programs and progress in eastern Asian countries. Phycologia 58:484–495

    CAS  Article  Google Scholar 

  12. James K, Kibele J, Shears NT (2015) Using satellite-derived sea surface temperature to predict the potential global range and phenology of the invasive kelp Undaria pinnatifida. Biol Invasions 17:3393–3408

    Article  Google Scholar 

  13. Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405

    CAS  PubMed  Article  Google Scholar 

  14. Li X, Yang G, Shi Y, Cong Y, Che S, Qu S, Li Z (2008) Prediction of the heterosis of Laminaria hybrids with the genetic distance between their parental gametophyte clones. J Appl Phycol 20:1097–1102

  15. Li X, Pang SJ, Shan TF (2017) Genetic diversity and population structure among cultivars of Saccharina japonica currently farmed in northern China: genetic diversity of Saccharina cultivar. Phycol Res 65:111–117

    CAS  Article  Google Scholar 

  16. Li Q, Shan T, Wang X, Su L, Pang S (2020) Evaluation of the genetic relationship between the farmed populations on a typical kelp farm and the adjacent subtidal spontaneous population of Undaria pinnatifida (Phaeophyceae, Laminariales) in China. J Appl Phycol 32:653–659

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  18. Milano I, Babbucci M, Cariani A, Atanassova M, Bekkevold D, Carvalho GR, Espiñeira M, Fiorentino F, Garofalo G, Geffen AJ, Hansen JH, Helyar SJ, Nielsen EE, Ogden R, Patarnello T, Stagioni M, FishPopTrace Consortium, Tinti F, Bargelloni L (2014) Outlier SNP markers reveal fine-scale genetic structuring across European hake populations (Merluccius merluccius). Mol Ecol 23:118–135

    PubMed  Article  PubMed Central  Google Scholar 

  19. Morita T, Kurashima A, Maegawa M (2003) Temperature requirements for the growth of young sporophytes of Undaria pinnatifida and Undaria undarioides (Laminariales, Phaeophyceae). Phycol Res 51:266–270

    Article  Google Scholar 

  20. Nanba N, Fujiwara T, Kuwano K, Ishikawa Y, Ogawa H, Kado R (2011) Effect of water flow velocity on growth and morphology of cultured Undaria pinnatifida sporophytes (Laminariales, Phaeophyceae) in Okirai Bay on the Sanriku coast, Northeast Japan. J Appl Phycol 23:1023–1030

    Article  Google Scholar 

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

    Article  Google Scholar 

  22. Niwa K, Kobiyama A, Fuseya R, Sakamoto T (2017) Morphological and genetic differentiation of cultivated Undaria pinnatifida (Laminariales, Phaeophyta). J Appl Phycol 29:1473–1482

    Article  Google Scholar 

  23. Okamura K (1915) Undaria and its species. Shokubutsugaku Zasshi 29:266–278

    Article  Google Scholar 

  24. Park K-J, Kim B-Y, Park S-K, Lee J-H, Kim Y-S, Choi H-G, Nam K-W (2012) Morphological and biochemical differences in three Undaria pinnatifida populations in Korea. Algae 27:189–196

    CAS  Article  Google Scholar 

  25. Perez R, Kaas R, Barbaroux O, Arbault S, Le Bayon N, Moigne J (1991) Undaria, une japonaise en Bretagne: nouvelle technique de culture d’une algue alimentaire. Equinoxe 36:19–30

    Google Scholar 

  26. Peteiro C, Freire Ó (2011) Effect of water motion on the cultivation of the commercial seaweed Undaria pinnatifida in a coastal bay of Galicia, Northwest Spain. Aquaculture 314:269–276

    Article  Google Scholar 

  27. Phull AR, Kim SJ (2018) Undaria pinnatifida a rich marine reservoir of nutritional and pharmacological potential: insights into growth signaling and apoptosis mechanisms in cancer. Nutr Cancer 70:956–970

    CAS  PubMed  Article  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  29. Qu Y, Cao Z, Wang W, Wang N, Li X, Pan J (2019) Monthly variations of fucoidan content and its composition in the farmed brown alga Saccharina sculpera (Laminariales, Phaeophyceae). J Appl Phycol 31:2623–2628

    CAS  Article  Google Scholar 

  30. Russello MA, Kirk SL, Frazer KK, Askey PJ (2012) Detection of outlier loci and their utility for fisheries management. Evol Appl 5:39–52

    PubMed  Article  PubMed Central  Google Scholar 

  31. Schneider S, Roessli D, Excoffier L (2000) Arlequin: a software for population genetics data analysis. User Manual Ver 2:2496–2497

    Google Scholar 

  32. Shan TF, Pang SJ, Li J, Gao SQ (2016) Breeding of an elite cultivar Haibao No. 1 of Undaria pinnatifida (Phaeophyceae) through gametophyte clone crossing and consecutive selection. J Appl Phycol 28:2419–2426

    CAS  Article  Google Scholar 

  33. 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

    Article  Google Scholar 

  34. Shan T, Yuan J, Su L, Li J, Leng X, Zhang Y, Gao H, Pang S (2020) First genome of the brown alga Undaria pinnatifida: chromosome-level assembly using PacBio and Hi-C technologies. Front Genet 11:140

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  35. Shibneva SY, Skriptsova AV, Shan TF, Pang SJ (2013) The different morphs of Undaria pinnatifida (Phaeophyceae, Laminariales) in Peter the Great Bay (Sea of Japan) are phenotypic variants: direct evidence. J Appl Phycol 25:1909–1916

    Article  Google Scholar 

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

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  37. Stuart MD, Hurd CL, Brown MT (1999) Effects of seasonal growth rate on morphological variation of Undaria pinnatifida (Alariaceae, Phaeophyceae). In: Kain JM, Brown MT, Lahaye M (eds) Sixteenth International Seaweed Symposium. Springer, Dordrecht, pp 191–199

    Chapter  Google Scholar 

  38. Takezaki N, Nei M, Tamura K (2014) POPTREEW: web version of POPTREE for constructing population trees from allele frequency data and computing some other quantities. Mol Biol Evol 31:1622–1624

    CAS  PubMed  Article  Google Scholar 

  39. Van der Sluis S, Posthuma D, Dolan CV (2013) TATES: efficient multivariate genotype-phenotype analysis for genome-wide association studies. PLoS Genet 9:e1003235

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  40. Watanabe T, Nisizawa K (1984) The utilization of wakame (Undaria pinnatifida) in Japan and manufacture of ‘haiboshi wakame’and some of its biochemical and physical properties. In: Bird CJ, Ragan MA (eds) Eleventh International Seaweed Symposium. Dr W. Junk Publishers, Dordrecht, pp 106–111

    Chapter  Google Scholar 

  41. Wickham H (2011) ggplot2. Wiley Interdiscip Rev Comput Stat 3:180–185

    Article  Google Scholar 

  42. Wu J, Wang L, Fu J, Chen J, Wei S, Zhang S, Zhang J, Tang Y, Chen M, Zhu J, Lei L, Gneg Q, Liu C, Wu L, Li X, Wang L, Wang Q, Wang Z, Xing S, Zhang H, Blari M, Wang S (2020) Resequencing of 683 common bean genotypes identifies yield component trait associations across a north–south cline. Nat Genet 52:118–125

    CAS  PubMed  Article  Google Scholar 

  43. Yendo K (1911) The development of Costaria, Undaria, and Laminaria. Ann Bot 25:691–715

    Article  Google Scholar 

  44. Yu L, Liu Y, Liu J (2020) Gene-associated microsatellite markers confirm panmixia and indicate a different pattern of spatially varying selection in the endangered Japanese eel Anguilla japonica. J Oceanol Limnol 38:1572–1583

    Article  Google Scholar 

  45. Zhang H, Gao S, Lercher MJ, Hu S, Chen W (2012) EvolView, an online tool for visualizing, annotating and managing phylogenetic trees. Nucleic Acids Res 40:W569–W572

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  46. Zhao XB, Pang SJ, Liu F, Shan T, Li J, Gao S, Kim H (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 

  47. Zhao Y, Zheng Y, Wang J, Ma S, Yu Y, White W, Yang S, Yang F, Lu J (2018) Fucoidan extracted from Undaria pinnatifida: source for nutraceuticals/functional foods. Mar Drugs 16:321

    PubMed Central  Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors are grateful to M.F. Zhang for his kind help in collecting samples in the chilly winter.

Availability of data and material (data transparency)

All data generated or analyzed during this study are included in this published article and its supplementary information files.

Funding

Supported by China Agriculture Research System of MOF and MARA, special supporting programs from the Chinese Academy of Sciences (KFJ-BRP-017-27, KFJ-BRP-017-53, CZBZX-1), a program from National Marine Genetic Resource Center and the Taishan Scholar Program of Shandong Province.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Shaojun Pang.

Ethics declarations

Conflict of interest

The authors have no conflicts of interest to declare that are relevant to the content of this article.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Fig. S1
figure7

Comparisons of morphological characteristics among three cultivars (C1, C2 and C3). Different small letters indicate significant differences in morphological features among cultivars in the same month (p<0.05) (PNG 2081 kb)

Fig. S2
figure8

Spearman rank correlation coefficients of measurements in C1 (a), C2 (b), and C3 (c) (PNG 8950 kb)

Fig. S3
figure9

(PNG 5179 kb)

Fig. S4
figure10

The values of deltaK (PNG 3920 kb)

Fig. S5
figure11

Scatter plots of discriminant analyses of principal components (DAPC) that reveal the genetic relationships among the elite cultivars, the traditional cultivars, and new cultivars of Undaria pinnatifida (PNG 709 kb)

High resolution image (TIF 1.96 mb)

High resolution image (TIF 1.26 mb)

High resolution image (TIFF 134 kb)

High resolution image (TIF .99 mb)

High resolution image (TIF 1.16 mb)

Table S1

(DOCX 23.4 kb)

Table S2

(DOCX 24.5 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Li, X., Pang, S., Shan, T. et al. Morphological and genetic analyses of the current major cultivars of Undaria pinnatifida at Lvshun, Dalian, the principal farming region in North China. J Appl Phycol 33, 3251–3260 (2021). https://doi.org/10.1007/s10811-021-02489-x

Download citation

Keywords

  • Undaria pinnatifida
  • Phaeophyceae
  • Seaweed cultivation
  • Sporophyll
  • Morphological characteristics
  • Microsatellite
  • Genetic structure