Abstract
Based upon DNA sequences from six plastid regions (rbcL, psbB-psbH, trnL-trnF, rpS16, psbA-trnH, rpS16-trnK) and the internal transcribed spacer (ITS) region of nuclear ribosomal DNA, the phylogenetic relationships in the genus Nitraria and family Nitrariaceae are investigated by using methods of maximum parsimony, maximum likelihood, and Bayesian inference. Our study strongly supports the monophyly of Nitraria. Nitraria can be divided into four parts, namely, the N. sphaerocarpa group, N. retusa group, the N. roborowskii and N. tangutorum group, and a group consisting of N. schoberi, N. komarovii, N. sibirica, and N. billardieri. Ancestral area reconstruction using S-Diva shows that eastern Central Asia is most likely the place of origin, and then dispersals occurred to western Central Asia, Africa, and Australia.
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References
Agnew ADQ (1980) Zygophyllaceae. In: Townsend CC, Guest E (eds) Flora of Iraq, vol 1. Ministry of Agriculture, Baghdad
APG (Angiosperm Phylogeny Group) (1998) An ordinal classification for the families of flowering plants. Ann Missouri Bot Gard 85:531–553
APG (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 141:399–436
APG (Angiosperm Phylogeny Group) (2009) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot J Linn Soc 161:105–121
Bachelier JB, Endress PK, Ronse de Craene L (2011) Comparative floral structure and development of Nitrariaceae (Sapindales) and systematic implications. In: Wantntorp L, Ronse de Craene L (eds) Flowers on the tree of life. Cambridge University Press, Cambridge, pp 181–217
Bakker FR, Vassiliades DD, Morton C, Savolainen V (1998) Phylogenetic relationships of Biebersteinia Stephan (Geraniaceae) inferred from rbcL and atpB sequence comparisons. Bot J Linn Soc 127:149–158
Bobrov EG (1946) About Asian species of the genus Nitraria L. Sovetsk Bot 14:19–30
Bobrov EG (1965) On the origin of the flora of the Old World deserts, as illustrated by the genus Nitraria L. (In Russian with English abstract). Bot Zhurn (Moscow & Leningrad) 50:1053–1067
Cronquist A (1981) An integrated system of classification of flowering plants. Columbia University Press, New York
Dahlgren R (1980) A revised system of classification of the angiosperms. Bot J Linn Soc 80:91–124
Dahlgren R (1983) General aspects of angiosperm evolution and macrosystematics. Nordic J Bot 3:119–149
Dahlgren R (1989) The last Dahlgrenogram. System of classification of the dicotyledons. In: Tan K (ed) The Davis and Hedge Festschrift: Plant taxonomy, Phytogeography and Related Subjects. Edinburgh University Press, Edinburgh, pp 249–260
Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15
El-Hadidi MN (1975) Zygophyllaceae in Africa. Boissiera 24:317–323
El-Hadidi MN (1977) Tribulaceae as a distinct family. Publications from Cairo University Herbarium 7–8:103–110
Engler A (1896a) Uber die geographische Verbreitung der Zygophyllaceen im Verhaltniss zu ihrer systematischen Gliederung. Abhandlungen der Preussischen Akademie der Wissenschaften, Physikalisch-mathematische Klasse, Berlin
Engler A (1896b) Zygophyllaceae. In: Engler A, Prantl K (eds) Die naturlichen Pflanzenfamilien, 1st edn, vol 3, section 4. Engelmann, Leipzig, pp 74–93, 353–357
Engler A (1931) Zygophyllaceae, Rutaceae, Simaroubaceae, Burseraceae. In: Engler A, Prantl K (eds) Die natürlichen Pflanzenfamilien, 2nd edn, vol 19a. Engelmann, Leipzig, pp 144–184, 187–456
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Gadek P, Fernando ES, Quinn CJ, Hoot SB, Terrazas T, Sheahan MC, Chase MW (1996) Sapindales: molecular delimitation and infraordinal groups. Amer J Bot 83:802–811
Goldberg A (1986) Classification, evolution and phylogeny of the families of Dicotyledons. Smithsonian Contr Bot 58:1–314
Grubov VI (1963) Introduction. Plants of Central Asia, 1 (In Russian)
Grubov VI (1999) Plants of Central Asia, vol 2. Science Publishers, Enfield
Hall T (2001) BioEdit: Biological sequence alignment editor for Windows 95/98 (version 5.0.9). http://www.mbio.ncsu.edu/BioEdit/bioedit.html
Hillis DM, Bull JJ (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst Biol 42:182–192
Huelsenbeck JP, Rannala B (2004) Frequentist properties of Bayesian posterior probabilities of phylogenetic trees under simple and complex substitution models. Syst Biol 53:904–913
Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755
Hussein SR, Kawashty SA, Tantawy ME, Saleh NAM (2009) Chemosystematic studies of Nitraria retusa and selected taxa of Zygophyllaceae in Egypt. Pl Syst Evol 277:251–264
Hutchinson J (1967) The genera of the flowering plants. Clarendon Press, Oxford
Ilyin MM (1944) Nitraria and origin of desert flora. Nature 5–6:116–118
Kang Y, Zhang ML, Chen ZD (2003) A preliminary phylogenetic study of the subgenus Pogonophace (Astragalus) in China based on ITS sequence data. Acta Bot Sin 45:140–145
Khalkuziev P (1990) About kinship relations of some Desert Plant families. Academic Science Press of Uzbek SSR, Tashkent, pp 53–83 (In Russian)
Komarov VL (1908) IX. On species and distribution of the genus Nitraria. Introduction to floras of China and Mongolia. Acta Horti Petropitani 29:151–176 (In Russian)
Komarov VL (1947) Opera Selecta II. Mosquae, Leninopoli. Academic Science Press, USSR, pp 137–161 (In Russian)
Korovin EP (1935) Essays on the history of the vegetation of Central Asia. I. Desert Betpak Dala (Central Kazakhstan). Bull. Central Asian State University 20(4):183–218
Liu YX, Huang ZH (2000) Management of protection of desert plant and grassland. Gansu Cultural Press, Lanzhou, pp 102–106
Liu YX, Zhou LH (1998) Nitrariaceae. In: Wu ZY, Raven PH, Hong DY (eds) Flora of China, vol 11. Science Press and Missouri Botanical Garden Press, Beijing and St. Louis (In Chinese)
Muellner AN, Vassiliades DD, Renner SS (2007) Placing Biebersteiniaceae, a herbaceous clade of Sapindales, in a temporal and geographic context. Pl Syst Evol 266:233–252
Namzaoglu E, Duran A, Akhani H (2005) A New Genus Record for the Flora of Turkey: Tetradiclis Stev.ex M.Bieb. (Zygophyllaceae). Turkish J Bot 29:403–407
Noble JC, Whalley RDB (1978a) The biology and autecology of Nitraria L. in Australia. I. Distribution, morphology and potential utilization. Austral J Ecol 3:141–163
Noble JC, Whalley RDB (1978b) The biology and autecology of Nitraria L. in Australia. II. Seed germination, seedling establishment and response to salinity. Austral J Ecol 3:165–177
Nylander JAA, Olsson U, Alström P et al (2008) Accounting for phylogenetic uncertainty in biogeography: a Bayesian approach to dispersal-vicariance analysis of the thrushes (Aves: Turdus). Syst Biol 57:257–268
Oxelman B, Liden M, Berglund D (1997) Chloroplast rpS16 intron phylogeny of the tribe Sileneae (Caryophyllaceae). Pl Syst Evol 206:393–410
Pan XL, Shen GM, Chen P (1999) A preliminary research on taxonomy and systematics of genus Nitraria. Acta Bot Yunnan 21:287–295 (In Chinese with English abstract)
Pan XY, Wei XP, Yu QS, Chen JK, Wang GX (2003) Polyploidy: classification, evolution and applied perspective of the genus Nitraria L. Chin Bull Bot 20:632–638 (In Chinese with English abstract)
Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environm Safety 60:324–349
Petrov MP (1964) Economic value of Nitraria. Academic Science Press of Turkmen SSR 2:41–45 (In Russian)
Popov MG (1927) The main features of the history of the flora of Central Asia. Bull. SAGU 15:239–290
Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818
Przewalskii NM (1883) From Zaisan, to Hami, Tibet and upper reaches of Yellow River. Third trip to Central Asia, 1st edn, St Petersburg (In Russia)
Ronse Decraene LP, Smets EF (1991) Morphological studies in Zygophyllaceae. I. The floral development and vascular anatomy of Nitraria retusa. Amer J Bot 78:1438–1448
Ronse Decraene LP, De Laet J, Smets EF (1996) Morphological studies in Zygophyllaceae. II. The floral development and vascular anatomy of Peganum harmala. Amer J Bot 83:201–215
Sang T, Crawford DJ, Stuessy TF (1997) Chloroplast DNA phylogeny, reticulate evolution and biogeography of Paeonia (Paeoniaceae). Amer J Bot 84:1120–1136
Savolianen V, Fay MF, Albach DC et al (2000) Phylogeny of the eudicots: a nearly complete familial analysis based on rbcL gene sequences. Kew Bull 55:257–309
Shaw J, Lickey EB, Schilling EE, Small RA (2007) Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III. Amer J Bot 94:275–288
Sheahan MC (2011a) Nitrariaceae. Flowering Plants. Eudicots. The Families and Genera of Vascular Plants. Vol 10:272–275
Sheahan MC (2011b) Tetradiclidaceae. Flowering Plants. Eudicots. The Families and Genera of Vascular Plants. Vol 10:424–427
Sheahan MC, Chase MW (1996) A phylogenetic analysis of Zygophyllaceae R.Br. based on morphological, anatomical and rbcL DNA sequence data. Bot J Linn Soc 113:279–300
Sheahan MC, Cutler DF (1993) Contribution of vegetative anatomy to the systematic of the Zygophyllaceae R.Br. Bot J Linn Soc 113:227–262
Stevens PF (2001) Angiosperm Phylogeny Website. Version 12. http://www.mobot.org/MOBOT/research/APweb/. Accessed July 2012
Su ZH, Zhang ML (2013) Evolutionary response to Quaternary climate aridification and occillations in north-western China revealed by chloroplast phylogeography of the desert shrub Nitraria sphaerocarpa (Nitrariaceae). Biol J Linn Soc 109:757–770
Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (* and other methods), version 4.0. Sunderland: Sinauer Associates
Taberlet P, Gielly L, Pantou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Pl Mol Biol 17:1105–1109
Takhtajan A (1969) Flowering plants: origin and dispersal. Oliver and Boyd, Edinburgh
Takhtajan A (1980) Outline of the classification of the flowering plants (Magnoliophyta). Bot Rev 46:225–359 (In Russian)
Takhtajan A (1983) The systematic arrangement of dicotyledonous families. In: Metcalfe CR, Chalk L (eds) Anatomy of the dicotyledons, vol 2, 2nd edn. Clarendon Press, Oxford, pp 180–201
Takhtajan A (1986) Floristic regions of the world. University of California Press, Berkeley
Takhtajan A (1987) Systema magnoliophytorum. Nauka, Leningrad (In Russian)
Tate JA, Simpson BB (2003) Paraphyly of Tarasa (Malvaceae) and diverse origins of the polyploid species. Syst Bot 28:723–737
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. Nucleic Acids Res 24:4876–4882
Vassilchenko IT (1982) On the origin of the flora of Middle Asia. Bot Zhurn (Moscow & Leningrad) 67:722–728 (In Russian with English abstract)
Vysochina GI, Banaev EV, Kukushkina TA, Schaldaeva TM, Yamtirov MB (2011) Phytochemical description of the Siberian species Nitraria (Nitrariaceae) genus. Rastit mir Aziat Ross 2:108–113 (In Russian with English abstract)
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: a guide to methods and applications. Academic Press, San Diego, pp 315–322
Xu DH, Abe J, Sakai M, Kanazawa A, Shimamoto Y (2000) Sequence variation of non-coding regions of chloroplast DNA of soybean and related wild species and its implications for the evolution of different chloroplast haplotypes. Theo App Genetics 101:724–732
Yu Y, Harris AJ, He X (2010) S-DIVA (Statistical Dispersal-Vicariance Analysis): a tool for inferring biogeographic histories. Mol Phylogenet Evol 56:848–850
Zhang Y (2006) Studies on molecular systematics and genetic diversity of genus Nitraria L. Ph D Thesis, Lanzhou University (In Chinese with English abstract)
Zhang Y, An L, Gao H, Li M, Jing L, Gao T (2005) Phylogenetic relationship and taxonomy of genera Nitraria based on two molecular data. Lanzhou University, School of Life Sciences
Zhao T, Wang ZT, Branford-White CJ, Xu H, Wang CH (2011) Classification and differentiation of the genus Peganum indigenous to China based on chloroplast trnL-F and psbA-trnH sequences and seed coat morphology. Pl Biol 13:940–947
Acknowledgments
We thank Dr. Stewart C. Sanderson (Shrub Sciences Laboratory, USDA, Utah, USA) for his careful English improvement to the manuscript. This research was financially supported by the National Key Basic Research Program of China (2012FY111500, 2014CB954201), and Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences.
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Temirbayeva, K., Zhang, ML. Molecular phylogenetic and biogeographical analysis of Nitraria based on nuclear and chloroplast DNA sequences. Plant Syst Evol 301, 1897–1906 (2015). https://doi.org/10.1007/s00606-015-1202-5
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DOI: https://doi.org/10.1007/s00606-015-1202-5