Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-25T14:29:27.123Z Has data issue: false hasContentIssue false
  • English
  • Français

MOLECULAR PHYLOGENY OF THE EDELWEISS (LEONTOPODIUM, ASTERACEAE – GNAPHALIEAE)

Published online by Cambridge University Press:  28 May 2010

C. Blöch ,
W. B. Dickoré ,
R. Samuel  and
T. F. Stuessy
C. Blöch*
Affiliation:
Department of Systematic and Evolutionary Botany, Faculty Centre of Biodiversity, University of Vienna, Rennweg 14, 1030 Wien, Austria. E-mail for correspondence: [email protected]
W. B. Dickoré
Affiliation:
Department of Vascular Plants, Botanische Staatssammlung, Menzinger Str. 67, 80638 München, Germany.
R. Samuel
Affiliation:
Department of Systematic and Evolutionary Botany, Faculty Centre of Biodiversity, University of Vienna, Rennweg 14, 1030 Wien, Austria. E-mail for correspondence: [email protected]
T. F. Stuessy
Affiliation:
Department of Systematic and Evolutionary Botany, Faculty Centre of Biodiversity, University of Vienna, Rennweg 14, 1030 Wien, Austria. E-mail for correspondence: [email protected]
Get access

Abstract

Leontopodium is a genus of approximately 30 species with a conspicuous Asian–European disjunct distribution. In this study samples from the Himalayan/Tibetan centre of diversity of the genus, as well as from Europe, were analysed to infer a phylogeny of the genus using sequences of nuclear ribosomal (ITS and ETS) and plastid (matK and trnL/F) DNA. The Southeast Tibetan monotypic Sinoleontopodium [Leontopodium lingianum (Y.L.Chen) Dickoré, comb. nov.] falls into Leontopodium. Monophyly of Leontopodium, including Sinoleontopodium, is supported. Due to low rates of sequence divergence, intrageneric relationships in general are weakly supported, a pattern frequently observed in plant groups centred in the Tibetan Plateau. Three phylogenetic groups can be identified, however, and these are also supported by morphology. The low levels of nucleotide divergence suggest a young age for the group, which has been influenced by the turbulent geological history of the Tibetan Plateau. Leontopodium is a characteristic Sino-Himalayan element that appears to have found its way into the mountains of Europe in geologically recent times. The two European taxa, Leontopodium alpinum and L. nivale, form a genetically distinct group, which, considering the wide geographic disjunction, shows surprisingly little divergence from its Asian relatives.

Keywords

AsteraceaeETSGnaphalieaeITSLeontopodiummatKmolecular phylogenySino-Himalayan floraSinoleontopodiumtrnL/F
Type
Articles
Information
Edinburgh Journal of Botany , Volume 67 , Issue 2 , July 2010 , pp. 235 - 264
Copyright
Copyright © Trustees of the Royal Botanic Garden Edinburgh 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Akiyama, S. (1999). Leontopodium montisganeshii, a new species of Asteraceae from Ganesh Himal, central Nepal. Bull. Natl. Sci. Mus. Tokyo, B 25: 1–4.Google Scholar
Anderberg, A. A. (1991). Taxonomy and phylogeny of the tribe Gnaphalieae (Asteraceae). Opera Bot. 104: 1–195.Google Scholar
Axelrod, D. I., Al-Shehbaz, I. & Raven, P. H. (1998). History of the modern flora of China. In: Zhang, A. L. & Wu, S. G. (eds) Floristic Characteristics and Diversity of East Asian Plants, pp. 43–55. Beijing and Berlin: China Higher Education Press and Springer-Verlag.Google Scholar
Baldwin, B. G. & Markos, S. (1998). Phylogenetic utility of the external transcribed spacer (ETS) of 18S-26S rDNA: Congruence of ETS and ITS trees of Calycadenia (Compositae). Molec. Phylogenet. Evol. 10: 449–463.CrossRefGoogle ScholarPubMed
Bayer, R. J. & Cross, E. W. (2003). A reassessment of tribal affinities of Craystylis and Haegelia (Asteraceae) based on three chloroplast DNA sequences. Plant Syst. Evol. 236: 207–220.Google Scholar
Bayer, R. J. & Starr, J. R. (1998). Tribal phylogeny of the Asteraceae based on two non-coding chloroplast sequences, the trnL intron and trnL/trnF intergenic spacer. Ann. Missouri Bot. Gard. 85: 242–256.CrossRefGoogle Scholar
Bayer, R. J., Soltis, D. E. & Soltis, P. S. (1996). Phylogenetic inferences in Antennaria (Asteraceae: Gnaphalieae: Cassiniinae) based on sequences from nuclear ribosomal DNA internal transcribed spacers (ITS). Amer. J. Bot. 83: 516–527.CrossRefGoogle Scholar
Bayer, R. J., Puttock, C. F. & Kelchner, S. A. (2000). Phylogeny of South African Gnaphalieae (Asteraceae) based on two noncoding chloroplast sequences. Amer. J. Bot. 87: 259–272.CrossRefGoogle ScholarPubMed
Bayer, R. J., Greber, D. G. & Bagnall, N. H. (2002). Phylogeny of Australian Gnaphalieae (Asteraceae) based on chloroplast and nuclear sequences, the trnL intron, trnL/trnF intergenic spacer, matK, and ETS. Syst. Bot. 27: 801–814.Google Scholar
Beauverd, G. (1909). Nouvelles espèces euroasiatiques du genre Leontopodium. Bull. Soc. Bot. Genève 1: 185–196.Google Scholar
Beauverd, G. (1910). Contribution à l’étude des Composées. Suite IV. Bull. Soc. Bot. Genève 2: 244–252.Google Scholar
Beauverd, G. (1911). Contribution à l’étude des Composées. Suite V. Bull. Soc. Bot. Genève 3: 353–359.Google Scholar
Beauverd, G. (1912). Contribution à l’étude des Composées. Suite VI. Nouveaux Leontopodium et Raoulia. Bull. Soc. Bot. Genève 5: 12–55.Google Scholar
Beauverd, G. (1914). Contribution à l’étude des Composées. Suite IX. Bull. Soc. Bot. Genève 6: 142–148.Google Scholar
Breitwieser, I., Glenny, D. S., Thorne, A. & Wagstaff, S. J. (1999). Phylogenetic relationships in Australasian Gnaphalieae (Compositae) inferred from ITS sequences. N. Zeal. J. Bot. 37: 399–412.Google Scholar
Chen, Y.-L. (1985). Sinoleontopodium, a new genus of Compositae from China. Acta Phytotaxon. Sin. 23: 457–459.Google Scholar
Chen, Y.-S. & Yang, Q.-E. (2009). Validation of the name Sinoleontopodium lingianum (Asteraceae, Gnaphalieae). Novon 19: 23–24.CrossRefGoogle Scholar
Clevinger, J. A. & Panero, J. L. (2000). Phylogenetic analysis of Silphium and subtribe Engelmanniinae (Asteraceae: Heliantheae) based on ITS and ETS sequence data. Amer. J. Bot. 87: 565–572.Google Scholar
Diels, L. (1901). Die Flora von Central-China. Nach der vorhandenen Literatur und neu mitgeteiltem Original-Materiale. Bot. Jahrb. Syst. 29: 169–659.Google Scholar
Dobner, M. J., Ellmerer, E. P., Schwaiger, S., Batsugkh, O., Narantuya, S., Stutz, M. & Stuppner, H. (2003a). New lignan, benzofuran, and sesquiterpene derivatives from the roots of Leontopodium alpinum and L. leontopodioides. Helv. Chim. Acta 86: 733–738.Google Scholar
Dobner, M. J., Schwaiger, S., Jenewein, I. H. & Stuppner, H. (2003b). Antibacterial activity of Leontopodium alpinum (Edelweiss). J. Ethnopharmacol. 89: 301–303.CrossRefGoogle ScholarPubMed
Dobner, M. J., Sosa, S., Schwaiger, S., Altinier, G., Loggia, R. D., Kaneider, N. C. & Stuppner, H. (2004). Anti-inflammatory activity of Leontopodium alpinum and its constituents. Planta Med. 70: 502–508.CrossRefGoogle ScholarPubMed
Doyle, J. J. & Dickson, E. (1987). Preservation of plant samples for DNA restriction: A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Taxon 36: 715–722.CrossRefGoogle Scholar
Erhardt, A. (1993). Pollination of the Edelweiss, Leontopodium alpinum. Bot. J. Linn. Soc. 111: 229–240.Google Scholar
Fazekas, A. J., Burgess, K. S., Kesanakurti, P. R., Graham, S. W., Newmaster, S. G., Husband, B. C. et al. . (2008). Multiple multilocus DNA barcodes from the plastid genome discriminate plant species equally well. PLoS ONE 3: E2802.CrossRefGoogle ScholarPubMed
Felsenstein, J. (1985). Confidence-limits on phylogenies – an approach using the bootstrap. Evolution 39: 783–791.CrossRefGoogle ScholarPubMed
Fitch, W. M. (1971). Toward defining course of evolution – minimum change for a specific tree topology. Syst. Zool. 20: 406–416.CrossRefGoogle Scholar
Franchet, A. R. (1892). Observations sur le groupe des Leontopodium. Bull. Soc. Bot. France 39: 126–136.Google Scholar
Galbany-Casals, M., Garcia-Jacas, N., Susanna, A., Saez, L. & Benedi, C. (2004a). Phylogenetic relationships in the Mediterranean Helichrysum (Asteraceae, Gnaphalieae) based on nuclear rDNA ITS sequence data. Aust. Syst. Bot. 17: 241–253.Google Scholar
Galbany-Casals, M., Saez, L. & Benedi, C. (2004b). Taxonomy of Castroviejoa, a new genus of Gnaphalieae (Asteraceae), endemic to the Mediterranean islands Corsica and Sardinia. Aust. Syst. Bot. 17: 581–591.Google Scholar
Glenny, D. (1997). A revision of the genus Anaphalioides (Asteraceae: Gnaphalieae). N. Zeal. J. Bot. 35: 451–477.Google Scholar
Glenny, D. S. & Wagstaff, S. J. (1997). Evolution and biogeography of New Zealand Anaphalis DC. (Asteraceae: Gnaphalieae) inferred from rDNA sequences. N. Zeal. J. Bot. 35: 441–449.CrossRefGoogle Scholar
Good, R. (1974). The Geography of the Flowering Plants. London: Longman.Google Scholar
Greuter, W. (2003). The Euro+Med treatment of Gnaphalieae and Inuleae (Compositae) – generic concepts and required new names. Willdenowia 33: 239–244.CrossRefGoogle Scholar
Grey, A. I., Hook, I. L., James, P. & Sheridan, H. (1999). Sesquiterpenes from Leontopodium alpinum. Phytochemistry 50: 1057–1060.Google Scholar
Grichuk, V. P. (1992). Main Types of Vegetation (Ecosystems) during the Maximum Cooling of the Last Glaciation. Budapest: INQUA/Hungarian Academy of Sciences.Google Scholar
Grierson, A. J. C. & Long, D. G. (2001). Flora of Bhutan (including a record of plants from Sikkim & Darjeeling), Vol. 2(3), pp. 1508–1515. Edinburgh: Royal Botanic Garden Edinburgh and Royal Government of Bhutan.Google Scholar
Grisebach, A. (1872). Die Vegetation der Erde nach ihrer klimatischen Anordnung: Ein Abriss der vergleichenden Geographie der Pflanzen. Leipzig: Verlag von Wilhelm Engelmann.Google Scholar
Grubov, V. (2003). Conspectus generis Leontopodium (Pers.) R. Br. (Compositae) Asiae centralis [in Russian]. Sist. Vyssh. Rast. 35: 188–197.Google Scholar
Hajra, P. K., Rao, R. R., Singh, D. K. & Uniyal, B. P. (1995). Flora of India, Vol. 13, pp. 103–111. Calcutta: Botanical Survey of India.Google Scholar
Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids. Symp. Ser. 41: 95.Google Scholar
Handel-Mazzetti, H. (1927). Systematische Monographie der Gattung Leontopodium. Beih. Bot. Centralbl. 44: 1–178.Google Scholar
Hook, I. (1994). Secondary metabolites in hairy root cultures of Leontopodium alpinum Cass. (Edelweiss). Pl. Cell Tiss. Org. 38: 321–326.Google Scholar
Iwatsuki, K., Yamazaki, T., Boufford, D. E. & Ohba, H. (1995). Flora of Japan, Vol. 3b, pp. 106–108. Tokio: Kondasha.Google Scholar
Jen, H. (1982). The uplift of the Qinghai-Xizang (Tibet) Plateau in relation to the vegetational changes in the past. Acta Phytotaxon. Sin. 20: 385–391.Google Scholar
Kimball, R. T. & Crawford, D. J. (2004). Phylogeny of Coreopsideae (Asteraceae) using ITS sequences suggests lability in reproductive characters. Molec. Phylogenet. Evol. 33: 127–139.Google Scholar
Kubitzki, K. & Krutzsch, W. (1998). Origins of east and southeast Asian plant diversity. In: Zhang, A. L. & Wu, S. G. (eds) Floristic Characteristics and Diversity of East Asian Plants, pp. 56–70. Beijing and Berlin: China Higher Education Press and Springer-Verlag.Google Scholar
Liu, J. Q., Gao, T. G., Chen, Z. D. & Lu, A. M. (2002). Molecular phylogeny and biogeography of the Qinghai-Tibet Plateau endemic Nannoglottis (Asteraceae). Molec. Phylogenet. Evol. 23: 307–325.Google Scholar
Liu, J. Q., Wang, Y. J., Wang, A. L., Hideaki, O. & Abbott, R. J. (2006). Radiation and diversification within the Ligularia–Cremanthodium–Parasenecio complex (Asteraceae) triggered by uplift of the Qinghai-Tibetan Plateau. Molec. Phylogenet. Evol. 38: 31–49.CrossRefGoogle ScholarPubMed
Maugini, E. (1962). Morfologia fiorale, embriologia ed embriogenesi in Leontopodium alpinum Cass. var. α typicum Fiori e Paoletti. Giorn. Bot. Ital. 96: 1–18.Google Scholar
Merxmüller, H., Leins, P. & Roessler, H. (1977). Inuleae – systematic review. In: Heywood, V. H., Harborne, J. B. & Turner, B. L. (eds) The Biology and Chemistry of the Compositae, Vol. 1, pp. 577–602. London: Academic Press.Google Scholar
Meusel, H. & Jäger, E. J. (1992). Vergleichende Chorologie der zentraleuropäischen Flora. Jena, Stuttgart, New York: Fischer Verlag.Google Scholar
Müller, K. (2005). SeqState – primer design and sequence statistics for phylogenetic DNA data sets. Appl. Bioinformatics 4: 65–69.Google Scholar
Müller, K. (2006). Incorporating information from length-mutational events into phylogenetic analysis. Molec. Phylogenet. Evol. 38: 667–676.CrossRefGoogle ScholarPubMed
Ngamriabsakul, C., Newman, M. F. & Cronk, Q. C. B. (2000). Phylogeny and disjunction in Roscoea (Zingiberaceae). Edinburgh J. Bot. 57: 39–61.Google Scholar
Noyes, R. D. (2007). Apomixis in Asteraceae: diamonds in the rough. Funct. Plant Sc. Biotechn. 1: 207–222.Google Scholar
Noyes, R. D. & Rieseberg, L. H. (1999). ITS sequences support a single origin for the North American Astereae (Asteraceae) and reflect deep geographic divisions in Aster s.l. Amer. J. Bot. 86: 398–412.Google Scholar
Nylander, J. A. A. (2005). MrModeltest v.2.2 [Program distributed by the author]. Uppsala University, Uppsala: Department of Systematic Zoology.Google Scholar
Panero, J. & Funk, V. (2008). The value of sampling anomalous taxa in phylogenetic studies: Major clades of the Asteraceae revealed. Molec. Phylogenet. Evol. 47: 757–782.Google Scholar
Plovanich, A. E. & Panero, J. L. (2004). A phylogeny of the ITS and ETS for Montanoa (Asteraceae: Heliantheae). Molec. Phylogenet. Evol. 31: 815–821.Google Scholar
Qaiser, M. & Abid, R. (2003). Flora of Pakistan, Vol. 210, pp. 147–161. Karachi and St Louis: Department of Botany, University of Karachi and Missouri Botanical Press.Google Scholar
Rechinger, K. H. (1980). Flora Iranica. Compositae IV – Inuleae, Vol. 145, pp. 28–30. Graz: Akademischer Drucks- und Verlagsgesellschaft.Google Scholar
Ronquist, F. & Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574.CrossRefGoogle ScholarPubMed
Royden, L. H., Burchfiel, B. C. & van der Hilst, R. D. (2008). The geological evolution of the Tibetan Plateau. Science 321: 1054–1058.CrossRefGoogle ScholarPubMed
Samuel, R., Stuessy, T. F., Tremetsberger, K., Baeza, C. M. & Siljak-Yakovlev, S. (2003). Phylogenetic relationships among species of Hypochaeris (Asteraceae, Cichorieae) based on ITS, plastid trnL intron, trnL-F spacer, and matK sequences. Amer. J. Bot. 90: 496–507.CrossRefGoogle ScholarPubMed
Samuel, R., Kathriarachchi, H., Hoffmann, P., Barfuss, M. H. J., Wurdack, K. J., Davis, C. C. & Chase, M. W. (2005). Molecular phylogenetics of Phyllanthaceae: evidence from plastid matK and nuclear phyC sequences. Amer. J. Bot. 92: 132–141.Google Scholar
Samuel, R., Gutermann, W., Stuessy, T. F., Ruas, C. F., Lack, H. W., Tremetsberger, K. et al. . (2006). Molecular phylogenetics reveals Leontodon (Asteraceae, Lactuceae) to be diphyletic. Amer. J. Bot. 93: 1193–1205.CrossRefGoogle ScholarPubMed
Schwaiger, S., Adams, M., Seger, C., Ellmerer, E. P., Bauer, R. & Stuppner, H. (2004). New constituents of Leontopodium alpinum and their in vitro leukotriene biosynthesis inhibitory activity. Planta Med. 70: 978–985.CrossRefGoogle ScholarPubMed
Searle, M. P. (1991). Geology and Tectonics of the Karakoram Mountains. Chichester: John Wiley & Sons.Google Scholar
Shishkin, B. K. (1999). Flora of the USSR, Vol. 25, pp. 318–337. Washington: Bishen Singh Mahendra Pal Singh and Koeltz Scientific Books.Google Scholar
Smissen, R. D., Breitwieser, I., Ward, J. M., McLenachan, P. A. & Lockhart, P. J. (2003). Use of ISSR profiles and ITS-sequences to study the biogeography of alpine cushion plants in the genus Raoulia (Asteraceae). Plant Syst. Evol. 239: 79–94.Google Scholar
Smissen, R. D., Breitwieser, I. & Ward, J. M. (2004). Phylogenetic implications of transspecific chloroplast DNA sequence polymorphisms in New Zealand Gnaphalieae. Plant Syst. Evol. 249: 37–53.CrossRefGoogle Scholar
Sokolowska-Kulczycka, A. (1959). Apomiksja u Leontopodium alpinum Cass. [Apomixis in Leontopodium alpinum Cass.]. Acta Biol. Cracov., Ser. Bot. 2: 51–63.Google Scholar
Stuppner, H., Ellmerer, E. P., Ongania, K. H. & Dobner, M. (2002). Bisabolane derivatives from Leontopodium alpinum. Helv. Chim. Acta 85: 2982–2989.Google Scholar
Sun, Y., Skinner, D. Z., Liang, G. H. & Hulbert, S. H. (1994). Phylogenetic analysis of Sorghum and related taxa using internal transcribed spacers of nuclear ribosomal DNA. Theor. Appl. Genet. 89: 26–32.CrossRefGoogle ScholarPubMed
Swofford, D. L. (2002). PAUP*: Phylogenetic Analysis Using Parsimony (*and other Methods), Version 4. Sunderland, MA: Sinauer Associates.Google Scholar
Taberlet, P., Gielly, L., Pautou, G. & Bouvet, J. (1991). Universal primers for amplification of 3 noncoding regions of chloroplast DNA. Plant Mol. Biol. 17: 1105–1109.Google Scholar
Takhtajan, A. (1969). Flowering Plants: Origin and Dispersal. Edinburgh: Oliver and Boyd.Google Scholar
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. & Higgins, D. G. (1997). The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl. Acids Res. 24: 4876–4882.CrossRefGoogle Scholar
Tira, S., Galeffi, C. & Dimodica, G. (1970). Flavonoids of Gnaphalieae – Leontopodium alpinum Cass. Experientia 26: 1192.Google Scholar
Tremetsberger, K., Weiss-Schneeweiss, H., Stuessy, T., Samuel, R., Kadlec, G., Ortiz, M. A. & Talavera, S. (2005). Nuclear ribosomal DNA and karyotypes indicate a NW African origin of South American Hypochaeris (Asteraceae, Cichorieae). Molec. Phylogenet. Evol. 35: 102–116.Google Scholar
Tutin, T. G. (1973). Flora Europaea. Notulae systematicae. No. 14. Bot. J. Linn. Soc. 67: 283.Google Scholar
Uexküll-Gyllenband, M. (1901). Phylogenie der Blütenformen und Geschlechterverteilung bei den Compositen. Biblioth. Bot. 52: 27–32.Google Scholar
Unsworth, M. J., Jones, A. G., Wei, W., Marquis, G., Gokarn, S. G. & Spratt, J. E. (2005). Crustal rheology of the Himalaya and Southern Tibet inferred from magnetotelluric data. Nature 438: 78–81.CrossRefGoogle ScholarPubMed
Voroshilov, V. N. (1979). Novyi vid edel’veisa [A new species of the genus Leontopodium L.]. Byull. Mosk. Obshch. Ispyt. Prir. Biol. 84: 102–104.Google Scholar
Wang, A. L., Yang, M. H. & Liu, J. Q. (2005). Molecular phylogeny, recent radiation and evolution of gross morphology of the rhubarb genus Rheum (Polygonaceae) inferred from chloroplast DNA trnL-F sequences. Ann. Bot. 96: 489–498.Google Scholar
Wang, Y. J. & Liu, J. Q. (2004). Phylogenetic analyses of Saussurea sect. Pseudoeriocoryne (Asteraceae: Cardueae) based on chloroplast DNA trnL-F sequences. Biochem. Syst. Ecol. 32: 1009–1023.Google Scholar
Wang, Y. J., Li, X. J., Hao, G. & Liu, J. Q. (2004). Molecular phylogeny and biogeography of Androsace (Primulaceae) and the convergent evolution of cushion morphology. Acta Phytotaxon. Sin. 42: 481–499.Google Scholar
Wang, Y. J., Liu, J. Q. & Miehe, G. (2007). Phylogenetic origins of the Himalayan endemic Dolomiaea, Diplazoptilon and Xanthopappus (Asteraceae: Cardueae) based on three DNA regions. Ann. Bot. 99: 311–322.Google Scholar
Ward, F. K. (1921). The Mekong–Salween divide as a geographical barrier. Geogr. J. 1: 385–404.Google Scholar
Ward, J., Bayer, R. J., Breitwieser, I., Smissen, R., Galbany-Casals, M. & Unwin, M. (2009). Gnaphalieae. In: Funk, V. A., Susanna, A., Stuessy, T. E. & Bayer, R. J. (eds) Systematics, Evolution and Biogeography of Compositae, pp. 539–588. Vienna: International Association for Plant Taxonomy.Google Scholar
White, T. J., Bruns, T., Lee, S. & Taylor, J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Inis, M. A., Gelfand, D. H., Sninsky, J. J. & White, T. J. (eds) PCR Protocols: A Guide to Methods and Applications, pp. 315–322. San Diego, CA: Academic Press.Google Scholar
Wolfe, K. H. (1991). Protein-coding Genes in Chloroplast DNA: Compilation of Nucleotide Sequences, Data Base Entries and Rates of Molecular Evolution. San Diego, CA: Academic Press.Google Scholar
Wu, Z. Y. & Wu, S. K. (1998). A proposal for a new floristic kingdom (realm) – the Asiatic kingdom, its delineation and characteristics. In: Zhang, A. L. & Wu, S. G. (eds) Floristic Characteristics and Diversity of East Asian Plants, pp. 3–42. Beijing and Berlin: China Higher Education Press and Springer-Verlag.Google Scholar
Zhou, S., Wang, X., Wang, J. & Xu, L. (2006). A preliminary study on timing of the oldest Pleistocene glaciation in Qinghai-Tibetan Plateau. Quatern. Int. 154/155: 44–51.CrossRefGoogle Scholar