Skip to main content
Log in

Molecular analysis of genetic diversity, population structure, and phylogeny of wild and cultivated tulips (Tulipa L.) by genic microsatellites

  • Research Report
  • Published:
Horticulture, Environment, and Biotechnology Aims and scope Submit manuscript

Abstract

Tulip (Tulipa L.) is one of the most important ornamental geophytes in the world. Analysis of molecular variability of tulips is of great importance in conservation and parental lines selection in breeding programs. Of the 70 genic microsatellites, 15 highly polymorphic and reproducible markers were used to assess the genetic diversity, structure, and relationships among 280 individuals of 36 wild and cultivated tulip accessions from two countries: Iran and the Netherlands. The mean values of gene diversity and polymorphism information content were 0.69 and 0.66, respectively, which indicated the high discriminatory power of markers. The calculated genetic diversity parameters were found to be the highest in wild T. systola Stapf (Derak region). Bayesian model-based STRUCTURE analysis detected five gene pools for 36 germplasms which corresponded with morphological observations and traditional classifications. Based on analysis of molecular variance, to conserve wild genetic resources in some geographical locations, sampling should be performed from distant locations to achieve high diversity. The unweighted pair group method with arithmetic mean dendrogram and principal component analysis plot indicated that among wild tulips, T. systola and T. micheliana Hoog exhibited the closest relationships with cultivated tulips. Thus, it can be assumed that wild tulips from Iran and perhaps other Middle East countries played a role in the origin of T. gesneriana, which is likely a tulip species hybrid of unclear origin. In conclusion, due to the high genetic variability of wild tulips, they can be used in tulip breeding programs as a source of useful alleles related to resistance against stresses.

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
Fig. 5

Similar content being viewed by others

References

  • Ballesteros-Mejia L, Lima NE, Lima-Ribeiro MS, Collevatti RG (2016) Pollination mode and mating system explain patterns in genetic differentiation in Neotropical plants. PLoS ONE 11:e0158660. https://doi.org/10.1371/journal.pone.0158660

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brownstein MJ, Carpten JD, Smith JR (1996) Modulation of non-templated nucleotide addition by Taq DNA polymerase: primer modifications that facilitate genotyping. Biotechniques 1004–6:1008–1010

    Google Scholar 

  • Christenhusz MJ, Govaerts R, David JC, Hall T, Borland K, Roberts PS, Tuomisto A, Buerki S, Chas MW et al (2013) Tiptoe through the tulips: cultural history, molecular phylogenetics and classification of Tulipa (Liliaceae). Bot J Linn Soc 172:280–328

    Article  Google Scholar 

  • da Maia LC, Palmieri DA, de Souza VQ, Kopp MM, de Carvalho FIF, de Oliveira AC (2008) SSR locator: tool for simple sequence repeat discovery integrated with primer design and PCR simulation. Int J Plant Genom. https://doi.org/10.1155/2008/412696

    Article  Google Scholar 

  • Daniel HH, Scornavacca C (2012) Dendroscope 3: an interactive tool for rooted phylogenetic trees and networks. Syst Biol http://sysbio.oxfordjournals. Accessed 25 Oct 2017

  • Ellis JR, Burke JM (2007) EST–SSRs as a resource for population genetic analyses. Heredity 99:125–132

    Article  CAS  PubMed  Google Scholar 

  • Eujayl I, Sledge MK, Wang L, May GD, Chekhovskiy K, Zwonitzer JC, Mian MA (2004) Medicago truncatula EST–SSRs reveal cross-species genetic markers for Medicago spp. Theor Appl Genet 108:414–422

    Article  CAS  PubMed  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 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  PubMed  Google Scholar 

  • Fulton T, Chunwongse J, Tanksley S (1995) Microprep protocol for extraction of DNA from tomato and other herbaceous plants. Plant Mol Biol Rep 13:207–209

    Article  CAS  Google Scholar 

  • Ghasemi Ghehsareh M, Salehi H, Khosh-Khui M, Niazi A (2015) Application of ISSR markers to analyze molecular relationships in Iranian jasmine (Jasminum spp.) accessions. Mol Biotechnol 57:65–74

    Article  CAS  PubMed  Google Scholar 

  • Hildebrand CE, Torney DC, Wagner RP (1992) Informativeness of polymorphic DNA markers. Los Alamos Sci 20:100–102

    CAS  Google Scholar 

  • Hoog MH (1973) On the Origin of Tulipa. Lilies and other Liliaceae. The Royal Horticulture Society, London, pp 47–64

    Google Scholar 

  • Kiani M, Memariani F, Zarghami H (2012) Molecular analysis of species of Tulipa L. from Iran based on ISSR markers. Plant Syst Evol 298:1515–1522

    Article  CAS  Google Scholar 

  • Killingback S (1990) Tulips: an illustrated identifier and guide to their cultivation. Apple Press, London, pp 9–13

    Google Scholar 

  • Kimura M, Crow JF (1964) The number of alleles that can be maintained in a finite population. Genetics 49:725–738

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kutlunina NA, Polezhaeva MA, Permyakova MV (2013) Morphologic and AFLP analysis of relationships between tulip species Tulipa biebersteiniana (Liliaceae). Russ J Genet 49:401–410

    Article  CAS  Google Scholar 

  • Leigh F, Lea V, Law J, Wolters P, Powell W, Donini P (2003) Assessment of EST- and genomic microsatellite markers for variety discrimination and genetic diversity studies in wheat. Euphytica 133:359–366

    Article  CAS  Google Scholar 

  • Lewontin RC (1972) Testing the theory of natural selection. Nature 236:181–182

    Article  Google Scholar 

  • Liu KJ, Muse SV (2005) PowerMarker: an integrated analysis environment for genetic marker analysis. Bioinformatics 21:2128–2129

    Article  CAS  PubMed  Google Scholar 

  • Marasek-Ciolakowska A, Ramanna MS, Arens P, Van Tuyl JM (2012) Breeding and cytogenetics in the genus Tulipa. Floricult Ornam Biotechnol 6:90–97

    Google Scholar 

  • MINITAB (2010) Minitab 16 statistical software. Minitab Inc., State College

    Google Scholar 

  • Montalvo AM, Williams SL, Rice KJ, Buchmann SL, Cory C, Handel SN, Nabhan GP, Primack R, Robichaux RH (1997) Restoration biology: a population biology perspective. Restor Ecol 5:277–290

    Article  Google Scholar 

  • Nam BE, Nam JM, Kim JG (2016) Effects of habitat differences on the genetic diversity of Persicaria thunbergii. J Ecol Environ 40:11

    Article  Google Scholar 

  • Olivia BI, Pamfil D, van Heusden S, van Tuyl J, Meijer-Dekens F, Bondrea M, Sestras R, Rusu AR, Lucaci M et al (2007) AFLP as a modern technique for DNA fingerprinting and identification Tulipa cultivars. Bull Univ Agric Sci Vet Med. https://doi.org/10.15835/buasvmcn-asb:64:1-2:1931

    Article  Google Scholar 

  • Pashley CH, Ellis JR, McCauley DE, Burke JM (2006) EST databases as a source for molecular markers: lessons from Helianthus. J Hered 97:381–388

    Article  CAS  PubMed  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 

  • Qi-fu L, Tong O, Yan-cheng J, Cai-xia W (2008) Tulip RAPD analysis of cultivars and wild species in Xinjiang. Acta Agricult Univ Jiangxiensis 30:656–660

    Google Scholar 

  • Rosenberg NA (2004) Distruct: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138

    Article  Google Scholar 

  • Rungis D, Berube Y, Zhang J, Ralph S, Ritland CE, Ellis BE, Douglas C, Bohlmann J, Ritland K (2004) Robust simple sequence repeat markers for spruce (Picea spp.) from expressed sequence tags. Theor Appl Genet 109:1283–1294

    Article  CAS  PubMed  Google Scholar 

  • Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18:233–234

    Article  CAS  PubMed  Google Scholar 

  • Shahin A, van Gurp T, Peters S, Visser R, van Tuyl J, Arens P (2012) Generation and analysis of expressed sequence tags in the extreme large genomes Lilium and Tulipa. BMC Genom 13:640

    Article  CAS  Google Scholar 

  • Sharma R, Chowdhury VK, Jain S, Jain RK (2009) A comparative study of genetic relationships among and within male and female genotypes of dioecious Jojoba (Simmondsia chinensis L. Schneider) using RAPD and ISSR markers. Asian J Hortic 4:184–193

    Google Scholar 

  • Shaw J, Lickey EB, Schilling EE, Small RL (2007) Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III. Am J Bot 94:275–288

    Article  CAS  PubMed  Google Scholar 

  • Tabin Sh, Kamili AN, Ganie SA, Zargar O, Sharma V, Gupta RG (2016) Genetic diversity and population structure of Rheum species in Kashmir Himalaya based on ISSR markers. Flora 223:121–128

    Article  Google Scholar 

  • Tang J, Vosman B, Voorrips RE, van der Linden CG, Leunissen JAM (2006) QualitySNP: a pipeline for detecting single nucleotide polymorphisms and insertions/deletions in EST data from diploid and polyploid species. BMC Bioinform 7:438

    Article  Google Scholar 

  • Tang N, Shahin A, Bijman P, Liu J, van Tuyl J, Arens P (2013) Genetic diversity and structure in a collection of tulip cultivars assessed by SNP markers. Sci Hortic 161:286–292

    Article  CAS  Google Scholar 

  • Tang N, Mo G, van Tuyl J, Arens P, Liu J, Tang D (2014) Genetic diversity and structure of Lilium pumilum DC in southeast of Qinghai–Tibet plateau. Plant Syst Evol 300:1453–1464

    Google Scholar 

  • van Raamsdonk LWD, de Vries T (1996) Cultivar classification in Tulipa L. (Liliaceae). Acta Bot Neerl 45:183–198

    Article  Google Scholar 

  • Wang F, Yang T, Burlyaeva M, Li L, Jiang J, Fang L, Redden R, Zong X (2015) Genetic diversity of grasspea and its relative species revealed by SSR markers. PLoS One. https://doi.org/10.1371/journal.pone.0118542

    Article  PubMed  PubMed Central  Google Scholar 

  • Wilford R (2006) Tulips: Species and Hybrids for the Gardener. Timber Press

  • Williamson VM (1999) Plant nematode resistance genes. Curr Opin Plant Biol 2:327–331

    Article  CAS  PubMed  Google Scholar 

  • Woodhead M, Russell J, Squirrell J, Hollingsworth M, Cardle L, Ramsay L, Gibby M, Powell W (2003) Development of EST–SSRs from the alpine lady-fern, Athyrium distentifolium. Mol Ecol Notes 3:287–290

    Article  CAS  Google Scholar 

  • World Checklist of Selected Plant Families (2009) The Board of Trustees of the Royal Botanic Gardens, Kew. http://www.kew.org/wcsp

  • Yanagisawa R, Kuhara T, Nishikawa T, Sochacki D, Marasek-Ciolakowska A, Okazaki K (2012) Phylogenetic analysis of wild and garden tulips using sequences of chloroplast DNA. Acta Hortic 953:103–110

    Article  Google Scholar 

  • Yeh FC, Yang RC, Boyle TBJ (1999) Popgene version 1.31: Microsoft Windows-based freeware for population genetic analysis. Molecular Biology and Biotechnology Centre, University of Alberta, and Centre for International Forestry Research, Canada

  • Zonneveld B (2009) The systematic value of nuclear genome size for all species of Tulipa L. (Liliaceae). Plant Syst Evol 281:217–245

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors gratefully acknowledge the financial support of the Iranian Ministry of Science, Shiraz University, and Wageningen University and research center. The whole staff of the molecular biology lab in Department of Plant Breeding of Wageningen University are very much appreciated for their support and skillful assistance.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Morteza Khosh-Khui.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pourkhaloee, A., Khosh-Khui, M., Arens, P. et al. Molecular analysis of genetic diversity, population structure, and phylogeny of wild and cultivated tulips (Tulipa L.) by genic microsatellites. Hortic. Environ. Biotechnol. 59, 875–888 (2018). https://doi.org/10.1007/s13580-018-0055-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13580-018-0055-6

Keywords

Navigation