Skip to main content
Log in

Molecular phylogeny and genetic variation in the genus Lilium native to China based on the internal transcribed spacer sequences of nuclear ribosomal DNA

  • Regular Paper
  • Published:
Journal of Plant Research Aims and scope Submit manuscript

Abstract

We present a comprehensive phylogeny derived from nuclear ribosomal DNA (nrDNA) for 214 samples representing 98 species and five varieties, including 44 species and five varieties native to China. Our collection of 25 species and five varieties (44 samples) covering all five sections of the genus (Comber) distributed in China also were included in the internal transcribed spacer (ITS) database. This study incorporates previous research with an emphasis on Chinese species, including the controversial subsection, Sinomartagon 5c Comber. In the phylogenetic tree obtained by maximum parsimony (PAUP) and maximum likelihood (RAxML) analyses, the samples were divided into four major groups. Our results suggest that the subsection (subsect.) 5c Comber should be classified into the true subsect. 5c and the section (sect.) Lophophorum. And the latter was divided into three subsections (subsect. Lophophorum I, subsect. Lophophorum II, and subsect. Lophophorum III). Based on molecular phylogenetic analysis and fluorescence in situ hybridization, we report that L. henryi and L. rosthornii are closely related, and we propose their classification into subsect. Leucolirion 6a. Our results support Comber’s subdivision of sect. Leucolirion, which was primarily based on bulb color. Chinese species were divided into five sections: sect. Martagon, sect. Archelirion, sect. Leucolirion, sect. Sinomartagon, and sect. Lophophorum. These findings contribute to our understanding of the phylogeny, origin, and classification of Lilium.

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

Similar content being viewed by others

References

  • Asano Y (1986) A numerical taxonomic study of the genus Lilium in Japan. J Fac Agr Hokkaido Univ 62:333–341

    Google Scholar 

  • Baker JG (1871) A new synopsis of all the known lilies. Gardeners’ Chron Agric Gazette 28:104

    Google Scholar 

  • Barba-Gonzalez R, Ramanna MS, Visser RGF, Van Tuyl JM (2005) Intergenomic recombination in F1 lily hybrids (Lilium) and its significance for genetic variation in the BC1 progenies as revealed by GISH and FISH. Genome 48:884–894. doi:10.1139/G05-057

    Article  CAS  PubMed  Google Scholar 

  • Comber HF (1949) A new classification of the genus Lilium. Lily Year Book RHS 13:86–105

    Google Scholar 

  • De Jong PC (1974) Some notes on the evolution of lilies. N Am Lily Year Book 27:23–28

    Google Scholar 

  • Dubouzet JG, Shinoda K (1999a) ITS DNA sequence relationships between Lilium concolor Salisb, L. dauricum Ker-Gawl and their putative hybrid, L. maculatum Thunb. Theor Appl Genet 98:213–218

    Article  CAS  Google Scholar 

  • Dubouzet JG, Shinoda K (1999b) Phylogenetic analysis of the internal transcribed spacer region of Japanese Lilium species. Theor Appl Genet 98:954–960

    Article  CAS  Google Scholar 

  • Endlicher SL (1836) Genera Plantarum. F. Beck, Vienna

    Google Scholar 

  • Fay MF et al (2006) Phylogenetic of Liliales: summarized evidence from combined analyses of five plastid and one mitochondrial loci. Aliso 22:559–565

    Google Scholar 

  • Gao YD et al (2009) Karyotypes of four genera in Liliaceae (s.str.) from Hengduan Mountains of southwest China. Acta Bot Yunnan 31:399–405

    Article  Google Scholar 

  • Gao YD, Zhou SD, He XJ (2011) Karyotype studies in thirty-two species of Lilium (Liliaceae) from China. Nord J Bot 29:746–761. doi:10.1111/j.1756-1051.2011.01069.x

    Article  Google Scholar 

  • Gao YD, Markus Hohenegger, Harris AJ, Zhou SD, He XJ, Wan J (2012a) A new species in the genus Nomocharis Franchet (Liliaceae): evidence that brings the genus Nomocharis into Lilium. Plant Syst Evol 298:69–85. doi:10.1007/s00606-011-0524-1

    Article  Google Scholar 

  • Gao YD, Zhou SD, He XJ, Wan J (2012b) Chromosome diversity and evolution in tribe Lilieae (Liliaceae) with emphasis on Chinese species. J Plant Res 125:55–69. doi:10.1007/s10265-011-0422-1

    Article  PubMed  Google Scholar 

  • Gerlach WL, Bedbrook JR (1979) Cloning and characterization of ribosomal RNA genes from wheat and barley. Nucleic Acids Res 7:1869–1885

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acid Symposium Series 41: 95–98

  • Harrison GE, Heslop-Harrison JS (1995) Centromeric repetitive DNA sequences in the genus Brassica. Theor Appl Genet 90:157–165

    Article  CAS  PubMed  Google Scholar 

  • Haw SG (1986) The lilies of China. BT Batsford Ltd, London

    Google Scholar 

  • I˙kinci N, Oberprieler C, Gu¨ner A (2006) On the origin of European lilies: phylogenetic analysis of Lilium section Liriotypus (Liliaceae) using sequences of the nuclear ribosomal transcribed spacers. Willdenowia 36:647–656. doi:10.3372/wi.36.36201

    Article  Google Scholar 

  • Lee JS, Lee PO, Lim YP, Shin EM, Park SY (1996) Classification of lilies using random amplified polymorphic DNA (RAPD) analysis. Acta Hort 414:137–144

    CAS  Google Scholar 

  • Lee CS, Kim SC, Yeau SH, Lee NS (2011) Major lineages of the genus Lilium (Liliaceae) based on nrDNA ITS sequences, with special emphasis on the Korean species. J Plant Biol 54:159–171. doi:10.1007/s12374-011-9152-0

    Article  Google Scholar 

  • Liang SY (1980) Flora reipublicae popularis sinicae. Anagiospermae, Monocotyledoneae Liliaceae (I), vol 14. Science Press, Beijing, pp 116–157

  • Liang SY, Tamura M (2000) In: Wu ZY, Raven PH (eds) Flora of China, vol 24. Science Press/Missouri Botanical Garden Press, Beijing/St. Louis, pp 118–152

    Google Scholar 

  • Liang SY, Zhang WX (1984) Pollen tetrads in Lilium with a discussion on the delimitation between L.sempervivoideum and its ally. Acta Phytotaxonomica Sinica 22:297–300

    Google Scholar 

  • Light RW (1960) Cytological and interspecific hybridization studies in Lilium L. and their significance for classification. Thesis: (Ph. D.) Cornell University

  • McRae EA (1998) Lily species. In: Lilies. Timber Press, Portland, pp 105–204

  • Mitchell RM (1998) Species DNA research report. The NALS Quarterly Bulletin 52:8–9

    Google Scholar 

  • Muratović E, Bogunić F, Šoljan D, Siljak-Yakovlev S (2005) Does Lilium bosniacum merit species rank? A classical and molecular-cytogenetic analysis. Plant Syst Evol 252:97–109

    Google Scholar 

  • Muratović E, Robin O, Bogunić F, Šoljan D, Siljak-Yakovlev S (2010) Karyotype evolution and speciation of European lilies from Lilium sect. Liriotypus. Taxon 59:165–175

    Google Scholar 

  • Nishikawa T, Okazaki K, Uchino T, Arakawa K, Nagamine T (1999) A molecular phylogeny of Lilium in the internal transcribed spacer region of nuclear ribosomal DNA. J Mol Evol 49:238–249

    Article  CAS  PubMed  Google Scholar 

  • Nishikawa T, Okazaki K, Arakawa K, Nagamine T (2001) Phylogenetic analysis of section Sinomartagon in genus Lilium using sequences of the internal transcribed spacer region in nuclear ribosomal DNA. Breed Sci 51:39–46

    Article  CAS  Google Scholar 

  • Page RMD (1996) Treeview: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358

    CAS  PubMed  Google Scholar 

  • Patterson TB, Givnish TJ (2002) Phylogeny, concerted convergence, and phylogenetic niche conservatism in the core Liliales: insights from rbcL and ndhF sequence data. Evolution 56:233–252. doi:10.1111/j.0014-3820.2002.tb01334.x

    CAS  PubMed  Google Scholar 

  • Peterson A, Peterson J (1999) Genotypic differentiation on an individual level in Gagea villosa (M. Bieb.) Duby, Gagea lutea (L.) Ker-Gawler and Gagea bohemica subsp. saxatilis (Koch) Pascher in Saxony-Anhalt using RAPD markers. J Appl Bot 73:228–233

    Google Scholar 

  • Peterson A, Bartish IV, Peterson J (2002) Genetic structure detected in a small population of the endangered plant Anthericum liliago L. (Anthericaceae) by RAPD analysis. Ecography 25:677–684

    Article  Google Scholar 

  • Peterson A, John H, Koch E, Peterson J (2004) A molecular phylogeny of the genus Gagea (Liliaceae) in Germany inferred from non-coding chloroplast and nuclear DNA sequences. Plant Syst Evol 245:145–162

    Article  CAS  Google Scholar 

  • Rešetnik I, Liber Z, Satovic Z, Cigić P, Nikolić T (2007) Molecular phylogeny and systematics of the Lilium carniolicum group (Liliaceae) based on nuclear ITS sequences. Plant Syst Evol 265:45–58. doi:10.1007/s00606-006-0513-y

    Article  Google Scholar 

  • Sealy JR (1950) Nomocharis and Lilium. Kew Bull 5:273–297

    Article  Google Scholar 

  • Shimizu M (1971) Lilies of Japan. Seibundo Shinko-sha, Tokyo (in Japanese)

    Google Scholar 

  • Siljak-Yakovlev S, Peccenini S, Muratovic E, Zoldos V, Robin O, Vallés J (2003) Chromosomal differentiation and genome size in three European mountain Lilium species. Plant Syst Evol 236:165–173

    Google Scholar 

  • Smyth DR, Kongsuwan K, Wisudharomn S (1989) A survey of C-band patterns in chromosomes of Lilium (Liliaceae). Plant Syst Evol 163:53–69

    Article  Google Scholar 

  • Song NH (1987) Analysis of C-banded karyotypes and chromosomal relationships of Lilium species. Ph.D. thesis, Kyungpook Natl. Univ. Daegu, Korea

  • Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690

    Article  CAS  PubMed  Google Scholar 

  • Stewart RN (1947) The morphology of somatic chromosomes in Lilium. Am J Bot 34:9–26

    Article  CAS  PubMed  Google Scholar 

  • Swofford DL (2000) PAUP* 4.0: phylogenetic analysis using parsimony (* and other methods). Version 4.0 b10. Sinauer Associates, Sunderland

    Google Scholar 

  • Synce PM (1980) Lilies. Batsford, London

    Google Scholar 

  • Takaiwa F, Oono K, Sugiura M (1985) Nucleotide sequence of the 17S-25S spacer region from rice rDNA. Plant Mol Biol 4:355–364

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M, Sudhir K (2007) MEGA 4: molecular evolutionary genetics analysis (MEGA) software version 4.0. In: The Society for Molecular Biology and Evolution. Oxford University Press, UK, pp 1596–1560

  • Terry RG, Nowak RS, Tausch RJ (2000) Genetic variation in chloroplast and nuclear ribosomal DNA in Utah Juniper (Juniperus osteosperma, Cupressaceae): evidence for interspecific gene flow. Amer J Bot 87:250–258

    Article  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang FZ, Tang J (1980) Lilium L. In: Flora Reipublicae Popularis Sinicae, vol 14. Science Press, Beijing, pp 116–157

  • Wilson EH (1925) The lilies of Eastern Asia. Dulau, London

    Google Scholar 

  • Woodcock HBD, Stearn WT (1950) Lilies of the world. Country Life/Scribner, London/New York

    Google Scholar 

  • Yamagishi M (1995) Detection of section-specific random amplified polymorphic DNA (RAPD) markers in Lilium. Theor Appl Genet 91:830–835

    CAS  PubMed  Google Scholar 

  • Zhou SD (2008) The phylogenetic classification and evolution of trib. Lilieae (Liliaceae s.str.) in China. PhD thesis, Sichuan Univ

Download references

Acknowledgments

This research was supported by the National Natural Science Foundation of China (Project No. 31071819), the Fundamental Research Funds for the Central Universities (Project No. BLYJ201207), special Fund for Forestry Scientific Research in the Public Interest (Project No. 201204609). We express our gratitude to Prof Shi-liang Zhou and Dr. Wen-pan Dong for providing technical assistance (LSEB Lab, Institute of Botany, Chinese Academy of Sciences), Prof. Shou-yu Guo and Dr. Qing Ding (Chinese Academy of Microbiology) for their suggestions on the earlier version and improving the English of this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gui-xia Jia.

Additional information

Y. Du and H. He contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Du, Yp., He, Hb., Wang, Zx. et al. Molecular phylogeny and genetic variation in the genus Lilium native to China based on the internal transcribed spacer sequences of nuclear ribosomal DNA. J Plant Res 127, 249–263 (2014). https://doi.org/10.1007/s10265-013-0600-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-013-0600-4

Keywords

Navigation