Journal of Plant Research

, Volume 123, Issue 2, pp 231–239 | Cite as

Molecular evidence for natural intergeneric hybridization between Liquidambar and Altingia

  • Wei Wu
  • Renchao Zhou
  • Yelin Huang
  • David E. Boufford
  • Suhua Shi
Regular Paper


Since its establishment, a hybrid origin for Semiliquidambar has been proposed based on morphological intermediacy and sympatric distribution with Altingia and Liquidambar. This hypothesis, however, has lacked convincing molecular evidence. In this study, two nuclear genes, pin2 and cab4, and a chloroplast gene, matK, from Semiliquidambar cathayensis and its putative parental species Liquidambar and Altingia in Jianfengling, Hainan, and Heishiding and Nanling, Guangdong, China, were sequenced to test this hypothesis. Our results showed that L. formosana and L. acalycina were closely related and constituted an inseparable clade in the phylogenetic trees of both pin2 and cab4 genes. Phylogenetic analyses revealed two types of sequences for S. cathayensis, which were clustered with its putative parents, L. formosanaL. acalycina and A. obovata in Jianfengling, and with L. formosana–L. acalycina and A. chinensis in Heishiding and Nanling. The partial chloroplast matK gene sequences showed four nucleotide substitutions between L. formosana and A. obovata in Jianfengling; the sequences of the two individuals of S. cathayensis were identical with those of A. obovata. No diagnostic chloroplast markers including matK and three other chloroplast genes were found to distinguish L. formosana and A. chinensis in Heishiding and Nanling. Molecular data clearly demonstrated that S. cathayensis is of intergeneric hybrid origin between L. formosanaL. acalycina and A. obovata or A. chinensis and that A. obovata functions as the maternal parent in the hybridization event in Jianfengling, Hainan.


Altingia Liquidambar matNatural hybridization Nuclear gene Semiliquidambar 



We thank Huangqiang Chen and Judy Chen for helping collect samples. We are grateful to the two anonymous reviewers for their valuable comments. The work was supported by National Natural Science Foundation of China ( 30730008, 30800060, 40976081, 40876075), National Basic Research Program of China (2007CB815701), the Ministry of Education Foundation of China (20070558030), the Natural Science Foundation of Guangdong Province (8451027501001492, 8151027501000089), and the Chang Hungta Science Foundation of Sun Yat-Sen University.

Supplementary material

10265_2009_275_MOESM1_ESM.pdf (31 kb)
Table S1. Fixed sites of pin2 gene between species of Altingia and Liquidambar among populations of Jiangfengling, Heishiding and Nanling. Table S2. Fixed sites of cab4 gene between species of Altingia and Liquidambar among populations of Hainan. Table S3. Pairwise maximum composite likelihood distances between five species of Atlingiaceae based on the pin2 and cab4 genes (PDF 31 kb)


  1. Angiosperm Phylogeny Group (2003) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG II. Bot J Linn Soc 141:399–436CrossRefGoogle Scholar
  2. Bentham G, Hooker JD (1865) Genera Plantarum, vol 1. Reeve, LondonGoogle Scholar
  3. Blume CL (1828) Flora Javae. Brussels, BelgiumGoogle Scholar
  4. Bogle AL (1986) The flora morphology and vascular anatomy of the Hamamelidaceae: subfamily Liquidambaroideae. Ann Mo Bot Gard 73:325–347CrossRefGoogle Scholar
  5. Chang HT (1962) Semiliquidambar, novum Hamamelidacearum genus Sinicum. Sunyatsen Univ Bull Nat Sci 1:35–44Google Scholar
  6. Chang HT (1979) Hamamelidaceae. In: Chang HT (ed) Flora Reipublicae Popularis Sinicae, vol 35/1. Science, Beijing, pp 36–116Google Scholar
  7. Chen SH, Liu XW, Du Q (2002) Study on tissue culture of Altingia chingii. J Chin Med Mater 25:82–83Google Scholar
  8. Chun WY (1965) Hamamelidaceae. In: Chun WY (ed) Flora of Hainanica, vol 2. Science, Beijing, pp 333–334Google Scholar
  9. de Candolle A (1830) Prodromus systematis naturalis regni vegetabilis. Treuttel et Würtz, ParisGoogle Scholar
  10. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15Google Scholar
  11. Ferguson DK (1989) A survey of the Liquidambaroideae (Hamamelidaceae) with a view to elucidating its fossil record. In: Crane PR, Black S (eds) Evolution, systematics, and fossil history of the Hamamelidae, vol 1. Systematics Association Special Volume No 40A. Clarendon, Oxford, UK, pp 249–272Google Scholar
  12. Ferguson D, Sang T (2001) Speciation through homoploid hybridization between allotetraploids in peonies (Paeonia). Proc Natl Acad Sci USA 98:3915–3919CrossRefPubMedGoogle Scholar
  13. Gaskin JF, Schaal BA (2002) Hybrid Tamarix widespread in U.S. invasion and undetected in native Asian range. Pro Natl Acad Sci USA 99:11256–11259CrossRefGoogle Scholar
  14. He ZY, Li LG, Luan S (2004) Immunophilins and parvulins. Superfamily of peptidyl prolyl isomerases in Arabidopsis. Plant Physiol 134:1248–1267CrossRefPubMedGoogle Scholar
  15. Ickert-Bond SM, Wen J (2006) Phylogeny and biogeography of Altingiaceae: evidence from combined analysis of five non-coding chloroplast regions. Mol Phylogenet Evol 39:512–528CrossRefPubMedGoogle Scholar
  16. Ickert-Bond SM, Pigg KB, Wen J (2005) Comparative infructescence morphology in Liquidambar (Altingiaceae) and its evolutionary significance. Am J Bot 92:1234–1255CrossRefGoogle Scholar
  17. Ickert-Bond SM, Pigg KB, Wen J (2007) Comparative infructescence morphology in Altingia (Altingiaceae) and discordance between morphological and molecular phylogenies. Am J Bot 94:1094–1115CrossRefGoogle Scholar
  18. Kamiya K, Moritsuka E, Yoshida T, Yahara T, Tachida H (2008) High population differentiation and unusual haplotype structure in a shade-intolerant pioneer tree species, Zanthoxylum ailanthoides (Rutaceae) revealed by analysis of DNA polymorphism at four nuclear loci. Mol Ecol 17:2329–2338CrossRefPubMedGoogle Scholar
  19. Leroy JF (1982) Origine et evolution du genre Platanus (Platanaceae). Compt Rend Hebd Séances Acad Sci Sér 295:251–254Google Scholar
  20. Lindley J (1836) A natural system of botany. Longman, LondonGoogle Scholar
  21. Liu JQ, Chen ZD, Lu AM (2002) Molecular evidence for the sister relationship of the eastern Asia-North American intercontinental species pair in the Podophyllum group (Berberidaceae). Bot Bull Acad Sin 43:147–154Google Scholar
  22. Martin DP, Williamson C, Posada D (2005) RDP2: recombination detection and analysis from sequence alignments. Bioinformatics 21:260–262CrossRefPubMedGoogle Scholar
  23. Morrell P, Rieseberg LH (1998) Molecular tests of the proposed diploid hybrid origin of Gilia achilleifolia (Polemoniaceae). Am J Bot 85:1439–1453CrossRefGoogle Scholar
  24. Oken L (1841) Allgemeine Naturgeschichte für alle Stānde 3(3):1539. Hovman’sche, StuttgartGoogle Scholar
  25. Pan J, Zhang D, Sang T (2007) Molecular phylogenetic evidence for the origin of a diploid hybrid of Paeonia (Paeoniaceae). Am J Bot 94:400–408CrossRefGoogle Scholar
  26. Park KR, Pak JH, Seo BB (2003) Allozyme variation in Paraixeris: a test for the diploid hybrid origin of Paraixeris koidzumiana (Compositae). Bot Bull Acad Sin 44:13–122Google Scholar
  27. Qiu S, Zhou RC, Li YQ, Havanond S, Jaengjai C, Shi SH (2008) Molecular evidence for natural hybridization between Sonneratia alba and S. griffithii. J Syst Evol 46:391–395Google Scholar
  28. Rieseberg LH (1997) Hybrid origins of plant species. Annu Rev Ecol Syst 28:359–389CrossRefGoogle Scholar
  29. Sang T (2002) Utility of low-copy nuclear gene sequences in plant phylogenetics. Crit Rev Biochem Mol Biol 37:121–147CrossRefPubMedGoogle Scholar
  30. Sang T, Crawford DJ, Stuessy TF, Silva OM (1995) ITS sequences and the phylogeny of the genus Robinsonia (Asteraceae). Syst Bot 20:55–64CrossRefGoogle Scholar
  31. Schmitt D, Perry TO (1964) Self-sterility in sweetgum. Forest Sci 10:302–305Google Scholar
  32. Shi S, Huang Y, Zhong Y, Du Y, Chang H, Boufford DE (2001) Phylogeny of the Altingiaceae based on cpDNA matK, PY-IGS and nrDNA ITS sequences. Plant Syst Evol 230:13–24CrossRefGoogle Scholar
  33. Stephens M, Scheet P (2005) Accounting for decay of linkage disequilibrium in haplotype inference and missing data imputation. Am J Hum Genet 76:449–462CrossRefPubMedGoogle Scholar
  34. Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989CrossRefPubMedGoogle Scholar
  35. Swofford DL (1998) PAUP. Phylogenetic analysis using parsimony (*and Other Methods), ver 4. Sinauer, Sunderland, MAGoogle Scholar
  36. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882CrossRefGoogle Scholar
  37. Wu CA, Campbell DR (2005) Cytoplasmic and nuclear markers reveal contrasting patterns of spatial genetic structure in a natural Ipomopsis hybrid zone. Mol Ecol 14:781–792CrossRefPubMedGoogle Scholar
  38. Xiang LL, Werth CR, Emery SN, McCauley DE (2000) Population-specific gender-biased hybridization between Dryopteris intermedia and D. carthusiana: evidence from chloroplast DNA. Am J Bot 87:1175–1180CrossRefPubMedGoogle Scholar
  39. Zhang H, Hanley S, Goodman HM (1991) Isolation, characterization, and chromosomal location of a new cab gene from Arabidopsis thaliana. Plant Physiol 96:1387–1388CrossRefPubMedGoogle Scholar
  40. Zhou R, Zeng K, Wu W, Chen X, Yang Z, Shi S, Wu CI (2007) Population genetics of speciation in nonmodel organisms: I. Ancestral polymorphism in mangroves. Mol Biol Evol 24:2746–2754CrossRefPubMedGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer 2009

Authors and Affiliations

  • Wei Wu
    • 1
  • Renchao Zhou
    • 1
  • Yelin Huang
    • 1
  • David E. Boufford
    • 2
  • Suhua Shi
    • 1
  1. 1.State Key Laboratory of Biocontrol, Key Laboratory of Gene Engineering of the Ministry of Education, School of Life ScienceSun Yat-Sen UniversityGuangzhouChina
  2. 2.Harvard University HerbariaCambridgeUSA

Personalised recommendations