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Phylogenetic analyses of Spiraea (Rosaceae) distributed in the Qinghai-Tibetan Plateau and adjacent regions: insights from molecular data

Plant Systematics and Evolution volume 302, pages 11–21 (2016)Cite this article

Abstract

The Qinghai-Tibetan Plateau (QTP) and adjacent regions comprise an excellent mountainous system to study plant diversification and speciation within East Asia. The uplift and eco-environmental processes of QTP have had an obvious effect on evolution of organisms in this region. The present study intends to test the potential correlation between evolutionary events (such as speciation and diversification) and orogenetic events (such as the intense uplift of QTP). Sequence data from five plastid DNA regions (trnL–trnF, rpl20–rpl12, rps15–ycf1, psbA–trnH, and trnS–trnG) and one nuclear ribosomal internal transcribed spacer of 19 species of the genus Spiraea L. were used in the study. Maximum parsimony and maximum likelihood trees were constructed in PAUP*, while divergence time was estimated with BEAST v1.7.5. Phylogenetic reconstruction revealed that these species form a single clade and can be divided into three sections. Diversification of Spiraea species began in middle Miocene (ca. 13.38 million years ago) during the first stage of uplifting at QTP. Diversification of Spiraea was further triggered and accelerated during the second stage of QTP uplifting in late Pliocene (ca. Last four million years). The estimated divergences time indicate that this rapid diversification was most likely triggered by the uplifting of QTP in early Pliocene, and accelerated during the Quaternary climatic oscillations.

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References

  • Abbott RJ, Brochmann C (2003) History and evolution of the arctic flora: in the footsteps of Eric Hultén. Molec Ecol 12:299–313

    Article  Google Scholar 

  • Akaike H (1974) A new look at the statistical model identification. IEEE T Automat Cont 19:716–723

    Article  Google Scholar 

  • Chase MW, Fay M, Devey DS, Maurin O, Rønsted N, Davies TJ, Pillon Y, Petersen G, Seberg O, Tamura MN (2006) Multigene analyses of monocot relationships: a summary. Aliso 22:63–75

    Google Scholar 

  • Chen S, Yao H, Han J, Liu C, Song J, Shi L, Zhu Y, Ma X, Gao T, Pang X (2010) Validation of the ITS2 region as a novel DNA barcode for identifying medicinal plant species. PLoS ONE 5:e8613

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Cheng HB, Powell C, An ZS, Zhou J, Dong GR (2000) Pliocene uplift of the northern Tibetan Plateau. Geology 28:715–718

    Article  Google Scholar 

  • Donoghue MJ, Smith SA (2004) Patterns in the assembly of temperate forests around the Northern Hemisphere. Philos T Roy Soc B 359:1633–1644

    Article  Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf material. Phytochemical Bulletin, Bot Soc Amer 19:11–15

    Google Scholar 

  • Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7.5. Molec Biol Evol 29:1969–1973

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Evans RC, Dickinson TA (1999) Floral ontogeny and morphology in subfamily Spiraeoideae Endl. (Rosaceae). Int J Pl Sci 160:981–1012

    Article  Google Scholar 

  • Gao QB, Duan YZ, Zhang FQ, Li YH, Fu PC, Chen SL (2012) Intraspecific divergences of Rhodiola alsia (Crassulaceae) based on plastid DNA and internal transcribed spacer fragments. Bot J Linn Soc 168:204–215

    Article  Google Scholar 

  • Hamilton M (1999) Four primer pairs for the amplification of chloroplast intergenic regions with intraspecific variation. Molec Ecol 8:521–523

    CAS  Google Scholar 

  • Harrison TM, Copeland P, Kidd WSF, Yin A (1992) Raising Tibet. Science 255:1663–1670

    PubMed  Article  CAS  Google Scholar 

  • Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913

    PubMed  Article  CAS  Google Scholar 

  • Hewitt G (2004) Genetic consequences of climatic oscillations in the Quaternary. Philos Trans R Soc Lond B Biol Sci 359:183–195 discussion 195

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Hutchinson J (1964) The genera of flowering plants. Dicotylédones, Vol. 1. II, 12th ed. Gebru¨ der Borntraeger, Berlin, pp 209–218

  • Kaellersjoe M, Farris JS, Chase MW, Bremer B, Fay MF, Humphries CJ, Petersen G, Seberg O, Bremer K (1998) Simultaneous parsimony jackknife analysis of 2538rbcL DNA sequences reveals support for major clades of green plants, land plants, seed plants and flowering plants. Pl Syst Evol 213:259–287

    Article  Google Scholar 

  • Kårehed J, Groeninckx I, Dessein S, Motley TJ, Bremer B (2008) The phylogenetic utility of chloroplast and nuclear DNA markers and the phylogeny of the Rubiaceae tribe Spermacoceae. Molec Phylogen Evol 49:843–866

    Article  CAS  Google Scholar 

  • Klootwijk C, Conaghan P, Powell CM (1985) The Himalayan arc: large-scale continental subduction, oroclinal bending and back-arc spreading. Earth Planet Sci Lett 75:167–183

    Article  Google Scholar 

  • Kranz HD, Mikš D, Siegler ML, Capesius I, Sensen CW, Huss VA (1995) The origin of land plants: phylogenetic relationships among charophytes, bryophytes, and vascular plants inferred from complete small-subunit ribosomal RNA gene sequences. J Molec Evol 41:74–84

    PubMed  Article  CAS  Google Scholar 

  • Li JJ, Fang XM (1998) Research on the uplift of the Qinghai-Xizang Plateau and environmental changes. China Sci Bull 43:1569–1574

    Google Scholar 

  • Li JJ, Wen SW, Zhang QS, Wang FB, Zheng BX, Li BY (1979) A discussion on the period, amplitude and type of the uplift of the Qinghai-Xizang Plateau. Sci Sin 22:1314–1328

    Google Scholar 

  • Li JJ, Shi YF, Li BY (1995) Uplift of the Qinghai-Xizang (Tibet) plateau and global change. Lanzhou Univ Press, Lanzhou

    Google Scholar 

  • Liu JQ, Gao TG, Chen ZD, Lu AM (2002) Molecular phylogeny and biogeography of the Qinghai-Tibet Plateau endemic Nannoglottis (Asteraceae). Molec Phylogen Evol 23:307–325

    Article  CAS  Google Scholar 

  • Liu JQ, Wang YJ, Wang AL, Hideaki O, Abbott RJ (2006) Radiation and diversification within the Ligularia-Cremanthodium-Parasenecio complex (Asteraceae) triggered by uplift of the Qinghai-Tibetan Plateau. Molec Phylogen Evol 38:31–49

    Article  CAS  Google Scholar 

  • Liu JQ, Sun YS, Ge XJ, Gao LM, Qiu YX (2012) Phylogeographic studies of plants in China: advances in the past and directions in the future. J Syst Evol 50:267–275

    Article  Google Scholar 

  • Liu JQ, Duan WY, Hao G, Ge XJ, Sun H (2014) Evolutionary history and underlying adaptation of alpine plants on the Qinghai-Tibet Plateau. J Syst Evol 52(3):241–249

    Article  Google Scholar 

  • Mes THM, Brederode VJ, Hart H (1996) Origin of the woody Macaronesian Sempervivoideae and the phylogenetic position of the east African species of Aeonium. Bot Act 109:477–491

    Article  CAS  Google Scholar 

  • Morgan DR, Soltis DE, Robertson KR (1994) Systematic and evolutionary implications of rbcL sequence variation in Rosaceae. Amer J Bot 81:890–903

    Article  CAS  Google Scholar 

  • Muellner A, Schaefer H, Lahaye R (2011) Evaluation of candidate DNA barcoding loci for economically important timber species of the mahogany family (Meliaceae). Molec Ecol Res 11:450–460

    Article  CAS  Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CG, Fonseca DGA, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    PubMed  Article  CAS  Google Scholar 

  • Patriat P, Achache J (1984) India-Eurasia collision chronology has implications for crustal shortening and driving mechanism of plates. Nature 311:615–621

    Article  Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818

    PubMed  Article  CAS  Google Scholar 

  • Potter D, Gao F, Esteban PB, Oh SH, Baggett S (2002) Phylogenetic relationship in Rosaceae inferred from chloroplast matK and trnL-trnF nucleotide sequence data. Pl Syst Evol 231:77–89

    Article  CAS  Google Scholar 

  • Potter D, Still SM, Grebenc T, Ballian D, Božič G, Franjiæ J, Kraigher H (2007) Phylogenetic relationships in tribe Spiraeeae (Rosaceae) inferred from nucleotide sequence data. Pl Syst Evol 266:105–118

    Article  CAS  Google Scholar 

  • Qiu YL, Palmer JD (1999) Phylogeny of early land plants: insights from genes and genomes. Trends Pl Sci 4:26–30

    Article  Google Scholar 

  • Rehder A (1940) Manual of cultivated trees and shrubs. Dioscorides Press, Portland

    Google Scholar 

  • Scarcelli N, Barnaud A, Eiserhardt W, Treier UT, Seveno M, d’Anfray A, Vigouroux Y, Pintaud JC (2011) A set of 100 chloroplast DNA primer pairs to study population genetics and phylogeny in monocotyledons. PLoS ONE 6:e19954

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Schultz J, Wolf M (2009) ITS2 sequence–structure analysis in phylogenetics: a how-to manual for molecular systematics. Molec Phylogen Evol 52:520–523

    Article  CAS  Google Scholar 

  • Schultz J, Maisel S, Gerlach D, Müller T, Wolf M (2005) A common core of secondary structure of the internal transcribed spacer 2 (ITS2) throughout the Eukaryota. RNA 11:361–364

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Schulze-Menz GK (1964) Rosaceae. In: Melchior H (ed) Engler’s Syllabus der Pflanzenfamilien II, Gebrüder Borntraeger, Berlin, pp 209–218

  • Shaw J, Lickey EB, Beck JT, Farmer SB, Liu W et al (2005) The tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. Amer J Bot 92:142–166

    Article  CAS  Google Scholar 

  • Shi Y (2002) Characteristics of late quaternary monsoonal glaciation on the Tibetan Plateau and in East Asia. Quaternary Int 97:79–91

    Article  Google Scholar 

  • Shi YF, Tang MC, Ma YZ (1998) The relation of second rising in Qinghai-Xizang Plateau and Asia Monsoon. Sci Chi D 28:263–271

    Google Scholar 

  • Simmons MP (2004) Independence of alignment and tree search. Molec Phylogen Evol 31:874–879

    Article  Google Scholar 

  • Spicer RA, Harris NB, Widdowson WM, Herman AB, Guo S, Valdes PJ, Wolfe JA, Kelley SP (2003) Constant elevation of southern Tibet over the past 15 million years. Nature 421:622–624

    PubMed  Article  CAS  Google Scholar 

  • Swofford DL (2007) PAUP*: phylogenetic analysis using parsimony (* and other methods). Version 4. Sinauer Associates, Sunderland

  • Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Pl Molec Biol 17:1105–1109

    Article  CAS  Google Scholar 

  • Takhtadzhian AL (1997) Diversity and classification of flowering plants. Columbia University Press, New York

    Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molec Biol Evol 28:2731–2739

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Tao JR, Xiong XZ (1986) The latest Cretaceous flora of Heilongjiang Province and the floristic relationship between East Asia and North America. Acta Phytotaxon Sin 24:1–15

    Google Scholar 

  • Tapponnier P, Xu ZQ, Roger F, Meyer B, Arnaud N, Wittlinger G, Yang JS (2001) Geology—oblique stepwise rise and growth of the Tibet plateau. Science 294:1671–1677

    PubMed  Article  CAS  Google Scholar 

  • Tate JA, Simpson BB (2003) Paraphyly of Tarasa (Malvaceae) and diverse origins of the polyploid species. Syst Bot 28:723–737

    Google Scholar 

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

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Tripati AK, Roberts CD, Eagle RA (2009) Coupling of CO2 and ice sheet stability over major climate transitions of the last 20 million years. Science 326:1394–1397

    PubMed  Article  CAS  Google Scholar 

  • Wang A, Yang M, Liu J (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 (Oxford) 96:489–498

    Article  CAS  Google Scholar 

  • Wang L, Abbott RJ, Zheng W, Chen P, Wang Y, Liu J (2009a) History and evolution of alpine plants endemic to the Qinghai-Tibetan Plateau: aconitum gymnandrum (Ranunculaceae). Molec Ecol 18:709–721

    Article  CAS  Google Scholar 

  • Wang L, Ikeda Liu TL, Wang YJ, Liu JQ (2009b) Repeated range expansion and glacial endurance of Potentilla glabra (Rosaceae) in the Qinghai-Tibetan plateau. J Integr Pl Biol 51:698–706

    Article  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis M, Gelfand D, Sninsky J, White T (eds) PCR protocols. Academic Press, San Diego, pp 315–322

    Google Scholar 

  • Wu ZY (ed) (1980) Vegetation of China. Academic Press, Beijing

    Google Scholar 

  • Xu T, Abbott RJ, Milne RI, Mao K, Du FK, Wu G, Ciren Z, Miehe G, Liu J (2010) Phylogeography and allopatric divergence of Cypress species (Cupressus L.) in the Qinghai-Tibetan Plateau and adjacent regions. BMC Evol Biol 10:194

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Yang FS, Li YF, Ding X, Wang XQ (2008) Extensive population expansion of Pedicularis longiflora (Orobanchaceae) on the Qinghai-Tibetan Plateau and its correlation with the quaternary climate change. Molec Ecol 17:5135–5145

    Article  Google Scholar 

  • Zhang D, Fengquan L, Jianmin B (2000) Eco-environmental effects of the Qinghai-Tibet Plateau uplift during the quaternary in China. Environm Geol 39:1352–1358

    Article  Google Scholar 

  • Zhang ML, Kang Y, Zhong Y, Sanderson SC (2012) Intense uplift of the Qinghai-Tibetan Plateau triggered rapid diversification of Phyllolobium (Leguminosae) in the Late Cenozoic. Pl Ecol Divers 5:491–499

    Article  Google Scholar 

  • Zheng BX, Xu QQ, Shen YP (2002) The relationship between climate change and quaternary glacial cycles on thee Qinghai-Tibetan Plateau: review and speculation. Quaternary Int 97–98:93–101

    Article  Google Scholar 

  • Zhisheng A, Kutzbach JE, Prell WL, Porter SC (2001) Evolution of Asian monsoons and phased uplift of the Himalaya-Tibetan plateau since Late Miocene times. Nature 411:62–66

    PubMed  Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was financially supported by the National Natural Science Foundation of China (Grants Nos. 31270270, 31200281, and 31110103911); the Chinese Academy of Sciences Fellowship for Young International Scientists (No. 2013Y2SB0005); West Light Foundation of the Chinese Academy of Sciences; the Main Direction Program of Knowledge Innovation of Chinese Academy of Sciences (Grant No. KSCX2-EW-Z-1); and the international scientific and technological cooperation projects of Qinghai Province (No. 2014-HZ-812).

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Authors and Affiliations

  1. Key Laboratory of Adaptation and Evolution of Plateau Biota, Northwest Institute of Plateau Biology, Chinese Academy of Sciences, Xining, 810001, People’s Republic of China

    Gulzar Khan, Fa-Qi Zhang, Qing-Bo Gao, Rui Xing, Jiu-Li Wang, Hai-Rui Liu & Shi-Long Chen

  2. School of Life Sciences, Southwest University, Chongqing, 400715, China

    Fa-Qi Zhang

  3. University of Chinese Academy of Sciences, Beijing, 100039, People’s Republic of China

    Gulzar Khan, Rui Xing, Jiu-Li Wang & Hai-Rui Liu

  4. Luoyang Normal University, Luoyang, 471022, People’s Republic of China

    Peng-Cheng Fu

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  1. Gulzar Khan
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Khan, G., Zhang, FQ., Gao, QB. et al. Phylogenetic analyses of Spiraea (Rosaceae) distributed in the Qinghai-Tibetan Plateau and adjacent regions: insights from molecular data. Plant Syst Evol 302, 11–21 (2016). https://doi.org/10.1007/s00606-015-1238-6

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Keyword

  • Climatic oscillations
  • Phylogenetics
  • Qinghai-Tibetan Plateau
  • Speciation
  • Spiraea L