Annals of Forest Science

, 75:74 | Cite as

Low within-population genetic diversity and high genetic differentiation among populations of the endangered plant Tetracentron sinense Oliver revealed by inter-simple sequence repeat analysis

  • Shan Li
  • Xiaohong Gan
  • Hongyan Han
  • Xuemei Zhang
  • Zhongqiong Tian
Research Paper


Key message

Tetracentron sinense Oliver, an endangered species from China, displays a low within-population genetic diversity and high genetic differentiation among populations, and the existing populations could be divided into three conservation and management units.


The endangered tree Tetracentron sinense Oliver has great value; however, little is known regarding the within-population genetic diversity and differentiation among T. sinense populations.


We examined the genetic diversity and differentiation of T. sinense wild populations, and we tested the effect of small-size population on the level of genetic diversity within these populations.


Using inter-simple sequence repeat (ISSR), we assessed the genetic variation and structure among 174 individuals from 26 natural populations of T. sinense sampled across its distribution range in China.


The ISSR primers yielded 180 amplified loci (123 were polymorphic). At the species level, the percentage of polymorphic loci (PPL), Nei’s gene diversity (H), and Shannon’s information index (I) were 68.3%, 0.196 and 0.300, respectively. The average population level PPL was 20.0%, and the Na, Ne, H, and I were 1.20, 1.13, 0.076, and 0.112, respectively. AMOVA revealed high genetic differentiation among populations (52.0% of total variance, P = 0.001), consistent with the gene differentiation coefficient (Gst = 0.607) and gene flow (Nm = 0.326). The 174 individuals of the 26 T. sinense populations clustered into three groups, and T. sinense geographic and genetic distance were significantly correlated.


T. sinense exhibited intermediate within-species genetic diversity, indicating preserved evolutionary potential. The low within-population genetic diversity and high genetic differentiation among T. sinense populations may be one of important factors causing endangerment. Three conservation units were determined based on genetic difference and structure. Inter-population introduction of individuals within units via appropriate propagation and seedling management might be an effective strategy for increasing T. sinense within-population genetic diversity and population size.


Tetracentron sinense Oliver Genetic variation Genetic structure Molecular marker ISSR Conservation strategy, China 



amplified fragment length polymorphisms


chroloplast DNA


coefficient of genetic differentiation


Nei’s gene diversity


gene diversity within populations


total gene diversity


Shannon’s information index


inter-simple sequence repeat


observed number of alleles


effective number of alleles


gene flow among populations


the percentage of polymorphic loci


random amplified polymorphic DNA


spatial genetic structure


simple sequence repeat



We thank the following peoples in each Nature Reserve Authority (NRA) for sample collecting: Zhirong Gu and Guorong Wei in Badagongshan NRA and Longping Tang in Sunhuangshan NRA of Hunan province, Shuanzhu Dong in Taibaishan NRA of Shanxi province, Liming Chen in Tangjiahe NRA and Dahai Zhu in Longxi-Hongkou NRA of Sichuan province, Aicai Nie in Wufeng Houhe NRA of Hubei province, and Ma in Baishuijiang NRA of Gansu province.


This work was supported by National Natural Science Foundation of China (NO.31370367), the Applied Basic Research Project of Sichuan Province, China (No.2017JY0164) and the Meritocracy Research Funds of China West Normal University (No. 17YC325).

Compliance with ethical standards

The State Forestry Administration of the People’s Republic of China granted permissions to Professor Xiaohong Gan for using the endangered species of plant (Tetracentron sinense).

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Balloux F, Lugonmoulin N (2002) The estimation of population differentiation with microsatellite markers. Mol Ecol 11(2):155–165CrossRefPubMedGoogle Scholar
  2. Cao LL, Gan XH, He S (2012) Effect of different geographical provenances and matrix on seed germination and seeding initial growth of Tetracentron sinense. Guihaia 32:656–662Google Scholar
  3. Culley TM, Wolfe AD (2001) Population genetic structure of the cleistogamous plant species Viola pubescens Aiton (Violaceae), as indicated by allozyme and ISSR molecular markers. Heredity 86(5):545–556CrossRefPubMedGoogle Scholar
  4. Ellstrand NC, Elam DR (1993) Population genetic consequences of small population size: implications for plant conservation. Annu Rev Ecol Syst 24:217–242CrossRefGoogle Scholar
  5. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14(8):2611–2620CrossRefPubMedGoogle Scholar
  6. Excoffier L, Smouse PE, Quattro JM. (1992) Analysis of molecular variance inferred from metricdistances among DNA haplotypes:application to human mitochondrial-DNA restriction data. Genetics, 131:479–491Google Scholar
  7. Frankel OH, Soulé ME (1981) Conservation and evolution. Cambridge University Press, CambridgeGoogle Scholar
  8. Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  9. Freeland JR (2005) Molecular ecology. John Wiley& Sons Ltd., West Sussex, pp 299–310Google Scholar
  10. Fu LG (1992) Plant red book in China-rare and endangered plants (Book I). China Science Press, Beijing, pp 452–453–682–683Google Scholar
  11. Fu DZ, Bruce B (1992) Tetracentron in Wu ZY and Raven PH. Flora of China. Science Press, Beijing, pp 590–591Google Scholar
  12. Gaafar ARZ, AI-Qurainy F, Khan S (2014) Assessment of genetic diversity in the endangered population of Breonadia salicina (Rubiaceae) growing in The Kingdom of Saudi Arabia using inter-simple sequence repeat markers. BMC Genet 15:109CrossRefPubMedPubMedCentralGoogle Scholar
  13. Gan X, Xie D, Cao L (2012) Sporogenesis and development of gametophytes in an endangered plant, Tetracentron sinense Oliv. Biol Res 45(4):393–398CrossRefPubMedGoogle Scholar
  14. Gan XH, Cao LL, Zhang XM, Li H (2013) Floral biology, breeding system and pollination ecology of an endangered tree Tetracentron sinense Oliv. (Trochodendraceae). Bot Stud 54:50CrossRefPubMedPubMedCentralGoogle Scholar
  15. Gong W, Gu L, Zhang D (2010) Low genetic diversity and high genetic divergence caused by inbreeding and geographical isolation in the populations of endangered species Loropetalum subcordatum (Hamamelidaceae) endemic to China. Conserv Genet 11:2281–2288CrossRefGoogle Scholar
  16. Gordon SP, Sloop CM, Davis HG, Cushman JH (2012) Population genetic diversity and structure of two rare vernal pool grasses in central California. Conserv Genet 13(1):117–130CrossRefGoogle Scholar
  17. Guo B, Lu D, Liao WB, Merilä J (2016) Genomewide scan for adaptive differentiation along altitudinal gradient in the Andrew’s toad Bufo andrewsi. Mol Ecol 25(16):3884–3900CrossRefPubMedGoogle Scholar
  18. Hamrick JL, Godt MJW (1990) Allozyme diversity in plant species. In: AHD B, Clegg MT, Kahler AL, Weir BS (eds) Plant population genetics, breeding, and genetic resources. Sinauer Associates, Sunderland, pp 43–63Google Scholar
  19. Hamrick JL, Godt MJW, Sherman-Broyles SL (1995) Gene flow among plant population: evidence from genetic markers. In: Hoch PC, Stephenson AG (eds) Experimental and Molecular Approaches to Plant Biosystematics. Missouri Botanical Garden Press, Saint Louis, pp 215–232Google Scholar
  20. Han HY, Xu N, Li S et al (2015) The effect of low temperature during imbibition on germination characteristics of Tetracentron sinense (Tetracentraceae) seeds. Plant Div Res 37(5):586–594Google Scholar
  21. Han H, Li S, Gan X, Zhang X (2017) Phenotypic diversity in natural populations of an endangered plant Tetracentron sinense. Bot Sci 95(2):283–294Google Scholar
  22. Li YY, Guan SM, Yang SZ, Luo Y, Chen XY (2012) Genetic decline and inbreeding depression in an extremely rare tree. Conserv Genet 13:343–347CrossRefGoogle Scholar
  23. Li XH, Zhang H, Wang DY et al (2013) The genetic structure of endemic plant Pteroceltis tatarinowii by ISSR markers. Acta Ecol Sin 33(16):4892–4901CrossRefGoogle Scholar
  24. Li HC, Gan XH, Zhang ZP et al (2015) Effects of altitudes and the DBH of seed trees on biological characteristics of Tetracentron sinense (Tetracentraceae) seeds. Plant Div Res 37(2):177–183Google Scholar
  25. Lopes MS, Mendonça D, Bettencourt SX, Borba AR, Melo C, Baptista C, da Câmara Machado A (2014) Genetic diversity of an Azorean endemic and endangered plant species inferred from inter-simple sequence repeat markers. AoB Plants 6:2016 (2014–6-26), 6CrossRefGoogle Scholar
  26. Loveless MP, Hamrick JL (1984) Ecological determinant of genetic structure in plant populations. Annu Rev Ecol Syst 15:65–95CrossRefGoogle Scholar
  27. Lu ZX, Wang YH, Peng YH, Korpelainen H, Li C (2006) Genetic diversity of Populus cathayana Rehd populations in southwestern China revealed by ISSR markers. Plant Sci 170:407–412CrossRefGoogle Scholar
  28. Luo JD, Gan XH, Jia XJ et al (2010) Biological characteristic of seeds of endangered plant Tetracentron sinense (Tetracentraceae). Acta Bot Yunnanica 32(3):204–210CrossRefGoogle Scholar
  29. Miller MP (1997) Tools for population genetic analysis. Version 1.3. Department of Biological Sciences, Northern Arizona University, FlagstaffGoogle Scholar
  30. Muir G, Filatov D (2007) A selective sweep in the chloroplast DNA of dioecious Silene (Section Elisanthe). Genetics 177:1239–1247CrossRefPubMedPubMedCentralGoogle Scholar
  31. Nei M (1974) Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci 70(12):3321–3323CrossRefGoogle Scholar
  32. Nybom H, Bartish IV (2000) Effects of life history traits and sampling strategies on genetic diversity estimates obtained with RAPD markers in plants. Perspect Plant Ecol 3(2):93–114CrossRefGoogle Scholar
  33. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155(2):945–959PubMedPubMedCentralGoogle Scholar
  34. Reddy MP, Sarla N, Siddiq EA (2002) Inter simple sequence repeat (ISSR) polymorphism and its application in plant breeding. Euphytica 128:9–17CrossRefGoogle Scholar
  35. Rohlf J (2000) NTSYS pc numerical taxonomy and multivariate analysis system, Version 2.1. Exeter publication, SetauketGoogle Scholar
  36. Shingo K, Yuji I, Fuyuo N (2010) Genetic differentiation among populations of an oceanic island: the case of Metrosideros boninensis, an endangered endemic tree species in the Bonin Islands. Plant Spec Biol 23(2):119–128Google Scholar
  37. Slatkin M (1985) Rare alleles as indicators of gene flow. Evolution 39:53–65CrossRefPubMedGoogle Scholar
  38. Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science (New York, NY) 236(4803):787–792CrossRefGoogle Scholar
  39. Stockwell CA, Hendry AP, Kinnison MT (2003) Contemporary evolution meets conservation biology. Trends Ecol Evol 18:94–101CrossRefGoogle Scholar
  40. Sun YX, Moore MJ, Yue LL, Feng T, Chu H, Chen S, Ji Y, Wang H, Li J (2014) Chloroplast phylogeography of the east Asian arcto-tertiary relict Tetracentron sinense (Trochodendraceae). J Biogeogr 41:1721–1732CrossRefGoogle Scholar
  41. Thriveni HN, Sumangala RC, Shivaprakash KN, Ravikanth G, Vasudeva R, Ramesh Babu HN (2014) Genetic structure and diversity of Coscinium fenestratum: a critically endangered liana of Western Ghats, India. Plant Syst Evol 300:403–413CrossRefGoogle Scholar
  42. Tileye F, Hilde N, Igorv B et al (2007) Analysis of genetic diversity in the endangered tropical tree species Hagenia abyssinica using ISSR markers. Genet Resour Crop Evol 54(5):947–958CrossRefGoogle Scholar
  43. Trindade H, Sena I, Goncalves S et al (2012) Genetic diversity of wild populations of Tuberaria major (Cistaceae), an endangered species endemic to the Algarve region (Portugal), using ISSR marker. Biochem Syst Ecol 45:9–16CrossRefGoogle Scholar
  44. Troupin D, Nathan R, Vendramin GG (2006) Analysis of spatial genetic structure in an expanding Pinus halepensis population reveals development of fine-scale genetic clustering over time. Mol Ecol 15:3617–3630CrossRefPubMedGoogle Scholar
  45. Wang YF, Lai GF, Efferth T, Cao JX, Luo SD (2006) New glycosides from Tetracentron sinense and their cytotoxic activity. Chem Biodivers 3(9):1023–1030CrossRefPubMedGoogle Scholar
  46. Wang J, Li Z, Guo Q, Ren G, Wu Y (2011) Genetic variation within and between populations of a desert poplar (Populus euphratica) revealed by SSR markers. Ann For Sci 68(6):1143–1149CrossRefGoogle Scholar
  47. Willi Y, Van Buskirk J, Hoffmann AA (2006) Limits to the adaptive potential of small populations. Annu Rev Ecol Evol Syst 37:433–458CrossRefGoogle Scholar
  48. Wright S (1978) Evolution and the genetics of populations. University of Chicago Press, ChicagoGoogle Scholar
  49. Wu ZY (2004) Flora of China (book 1). Science Press, BeijingGoogle Scholar
  50. Xu GB, Wu XQ, Jiang GX et al (2014) Genetic diversity and population structure of an endangered species: Tsoongiodendron odorum Chun. J Plant Gen Res 15(2):255–261Google Scholar
  51. Yang Q, Fu Y, Wang YQ, Wang Y, Zhang WH, Li XY, Reng YQ, Zhang J (2014) Genetic diversity and differentiation in the critically endangered orchid (Amitostigma hemipilioides): implications for conservation. Plant Syst Evol 300:871–879CrossRefGoogle Scholar
  52. Yeh FC, Yang RC, Boyle T (1997) POPGENE, version 1.32 ed. Software Microsoft Window-based freeware for population genetic analysis. University of Alberta, EdmontonGoogle Scholar
  53. Zhang P, Gao SZ (1990) Wood anatomy of Tetracentraceae. Acta Botan Boreali-Occiden Sin 10(3):185–189Google Scholar
  54. Zhang FM, Ge S (2002) Data analysis in population genetics. I. Analysis of RAPD data with AMOVA. Biodivers Sci 10(4):438–444Google Scholar
  55. Zhang DD, Bai GH, Zhu CS, Yu J, Carver BF (2010) Genetic diversity, population structure, and linkage disequilibrium in U.S. elite winter wheat. Plant Genome 3(2):117CrossRefGoogle Scholar
  56. Zhang QX, Shen YK, Shao RX, Fang J, He YQ, Ren JX, Zheng BS, Chen GJ (2013) Genetic diversity of natural Miscanthus sinense populations in China revealed by ISSR markers. Biochem Syst Ecol 48:248–256CrossRefGoogle Scholar
  57. Zhou YX (2007) Light requirement characteristics for the germination of Tetracention sinense Oliv seeds. J Cent South Univ For Technol27:54–57Google Scholar
  58. Zhou ZM, Newman C, Buesching CD, Meng X, Macdonald DW, Zhou Y (2016) Revised taxonomic binomials jeopardize protective wildlife legislation. Conserv Lett 9(5):313–315CrossRefGoogle Scholar
  59. Zietkiewicz E, Rafalski A, Labuda D (1994) Genome fingerprinting by simple sequence repeat (SSR)-anchored polymerase chain reaction amplification. Genomics 20:176–183CrossRefPubMedGoogle Scholar

Copyright information

© INRA and Springer-Verlag France SAS, part of Springer Nature 2018

Authors and Affiliations

  • Shan Li
    • 1
    • 2
  • Xiaohong Gan
    • 1
    • 2
  • Hongyan Han
    • 1
    • 2
  • Xuemei Zhang
    • 1
    • 2
  • Zhongqiong Tian
    • 1
    • 2
  1. 1.Key Laboratory of Southwest China Wildlife Resources Conservation (Ministry of Education), College of Life ScienceChina West Normal UniversityNanchongChina
  2. 2.Institute of Plant Adaptation and Utilization in Southwest MountainChina West Normal UniversityNanchongChina

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