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Plant Systematics and Evolution

, Volume 288, Issue 1–2, pp 25–42 | Cite as

Phylogeny of Salsoleae s.l. (Chenopodiaceae) based on DNA sequence data from ITS, psbB–psbH, and rbcL, with emphasis on taxa of northwestern China

  • Zhi-Bin Wen
  • Ming-Li Zhang
  • Ge-Lin Zhu
  • Stewart C. Sanderson
Original Article

Abstract

To reconstruct phylogeny and verify the monophyly of major subgroups, a total of 52 species representing almost all species of Salsoleae s.l. in China were sampled, with analysis based on three molecular markers (nrDNA ITS, cpDNA psbB–psbH and rbcL), using maximum parsimony, maximum likelihood, and Bayesian inference methods. Our molecular evidence provides strong support for the following: (1) Camphorosmeae is nested within Salsoleae s.l. instead of the previously suggested sister relationship. (2) Tribe Salsoleae s.l. is monophyletic and is composed of three monophyletic subunits, Caroxyloneae, the Kali clade, and Salsoleae s.str. (3) Climacoptera is separated from Salsola s.l. It does not form a monophyletic group but is split into two monophyletic parts, Climacoptera I and Climacoptera II. (4) Halogeton is clearly polyphyletic, as are Anabasis and the genus Salsola s.l. (5) Caroxylon, Haloxylon, Kali, and Petrosimonia are well-supported monophyletic genera. Additional evidence is needed regarding the monophyly of Halimocnemis, which remains unclear.

Keywords

Salsoleae s.l. Anabasis Climacoptera Halogeton Molecular phylogeny China 

Notes

Acknowledgments

Thanks to Prof. P. Yan for providing Salsoleae s.l. field collections from Xinjiang Province, China, Dr. D. M. Williams (London, UK) for helpful comments on the manuscript, Mrs. Lorraine Williams (London, UK) for improving the English of the manuscript, and two anonymous reviewers for valuable comments on a previous version. This research was funded by the National Basic Research Program of China (2009CB825104), Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences.

References

  1. Akhani H (2004) Halophytic vegetation of Iran: towards a syntaxonomical classification. Ann Bot (Rome) 4:66–82Google Scholar
  2. Akhani H, Trimborn P, Ziegler H (1997) Photosynthetic pathways in Chenopodiaceae from Africa, Asia and Europe with their ecological, phytogeographical and taxonomical importance. Plant Syst Evol 206:187–221CrossRefGoogle Scholar
  3. Akhani H, Ghobadnejhad M, Hashemi SM (2003) Ecology, biogeography and pollen morphology of Bienertia cycloptera Bunge ex Boiss. (Chenopodiaceae), an enigmatic C4 plant without Kranz anatomy. Plant Biol 5:167–178CrossRefGoogle Scholar
  4. Akhani H, Edwards G, Roalson EH (2007) Diversification of the old world Salsoleae s.l. (Chenopodiaceae): molecular phylogenetic analysis of nuclear and chloroplast data sets and a revised classification. Int J Plant Sci 168:931–956CrossRefGoogle Scholar
  5. Assadi M (2001) Chenopodiaceae. In: Assadi M, Khatamsaz M, Maassoumi AA (eds) Flora of Iran, vol 38. Research Institute of Forests and Rangelands, Tehran, pp 27–65Google Scholar
  6. Blackwell WH Jr (1977) The subfamilies of the Chenopodiaceae. Taxon 26:395–397CrossRefGoogle Scholar
  7. Borger CP, Yan GJ, Scott JK, Walsh MJ (2008) Salsola tragus or S. australis (Chenopodiaceae) in Australia—untangling taxonomic confusion through molecular and cytological analyses. Aust J Bot 56:600–608CrossRefGoogle Scholar
  8. Botschantzev VP (1956) Sbornik rabot po geobotanike, lesovedeniju, paleogeografii floristike: dva novykh roda iz semeistva marevykh. In: Akademiku VN, Sukachevu K (eds) Akademia Nauk SSSR. Izdatel’stvo Akademia Nauk SSSR, Moscow, pp 108–118Google Scholar
  9. Botschantzev VP (1969) The genus Salsola: a concise history of its development and dispersal (in Russian). Bot Zhurn 54:989–1001Google Scholar
  10. Botschantzev VP (1974) Species subsections Caroxylon sections Caroxylon (Thunb.) Fenzl generis Salsola L. (in Russian). Nov Sist Vyssh Rast 11:110–174Google Scholar
  11. Botschantzev VP (1976) Conspectus speciorum sections Coccosalsola Fenzl generis Salsola L. (in Russian). Nov Sist Vyssh Rast 13:74–102Google Scholar
  12. Butnik AA (1979) Types of development of seedlings of Chenopodiaceae Vent. (in Russian). Bot Zhurn 64:834–842 (in Russian)Google Scholar
  13. Cabrera JF, Jacobs SWL, Kadereit G (2009) Phylogeny of the Australian Camphorosmeae (Chenopodiaceae) and the taxonomic significance of the fruiting perianth. Int J Plant Sci 170:505–521CrossRefGoogle Scholar
  14. Casati P, Andreo CS, Edwards GE (1999) Characterization of NADP-malic enzyme from two species of Chenopodiaceae: Haloxylon persicum (C4) and Chenopodium album (C3). Phytochemistry 52:985–992CrossRefGoogle Scholar
  15. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15Google Scholar
  16. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  17. Freitag H (1997) Salsola L. (Chenopodiaceae). In: Rechinger KH (ed) Flora Iranica, vol 172. Akademische Druck und Verlagsanstalt, Graz, pp 154–255Google Scholar
  18. Fu LK, Zhang XC, Qin HN, Ma JS (1993) Index herbariorum sinicorum (in Chinese). Chinese Science and Technology Press, Beijing, pp 425–457Google Scholar
  19. Grubov VI (1999) Chenopodiaceae. In: Plants of Central Asia, vol 2. Science Publishers, Enfield, pp 87–133Google Scholar
  20. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704CrossRefPubMedGoogle Scholar
  21. Hillis DM, Bull JJ (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst Biol 42:182–192Google Scholar
  22. Holmgren PK, Holmgren NH (1998) (continuously updated) Index herbariorum. http://sciweb.nybg.org/science2/IndexHerbariorum.asp
  23. Huelsenbeck JP, Rannala B (2004) Frequentist properties of Bayesian posterior probabilities of phylogenetic trees under simple and complex substitution models. Syst Biol 53:904–913CrossRefPubMedGoogle Scholar
  24. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755CrossRefPubMedGoogle Scholar
  25. Iljin MM (1936) Chenopodiaceae. In: Siskin BK (ed) Flora SSSR, vol 6 (in Russian). Izdatel’stvo Akademii Nauk SSSR, Leningrad, pp 2–354Google Scholar
  26. Johnson LA, Soltis DE (1995) Phylogenetic inference in Saxifragaceae sensu stricto and Gilia (Polemoniaceae) using matK sequences. Ann Mo Bot Gard 82:149–175CrossRefGoogle Scholar
  27. Kadereit G, Borsch T, Weising K, Freitag H (2003) Phylogeny of Amaranthaceae and Chenopodiaceae and the evolution of C4 photosynthesis. Int J Plant Sci 164:959–986CrossRefGoogle Scholar
  28. Kadereit G, Gotzek D, Jacobs S, Freitag H (2005) Origin and age of Australian Chenopodiaceae. Org Divers Evol 5:59–80CrossRefGoogle Scholar
  29. 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 45:140–145Google Scholar
  30. Kapralov MV, Akhani H, Voznesenskaya EV, Edwards G, Franceschi V, Roalson EH (2006) Phylogenetic relationships in the Salicornioideae/Suaedoideae/Salsoloideae s.l. (Chenopodiaceae) clade and a clarification of the phylogenetic position of Bienertia and Alexandra using multiple DNA sequence datasets. Syst Bot 31:571–585Google Scholar
  31. Kühn U, Bittrich V, Carolin R, Freitag H, Hedge IC, Uotila P, Wilson PG (1993) Chenopodiaceae. In: Kubitzki K, Rohwer JG, Bittrich V (eds) The families and genera of vascular plants, vol 2. Springer, Berlin, pp 253–281Google Scholar
  32. Liu YX (1995) Observations on the formation of Chinese desert floras (in Chinese with English abstract). Acta Phytotax Sin 33:131–143Google Scholar
  33. Meyer CA (1829) Generae Chenopodearum. In: Ledebour CF (ed) Flora Altaica, vol 2. Reimer, Berlin, pp 370–371Google Scholar
  34. Moquin-Tandon A (1840) Chenopodearum monographica enumeratio. Loss, Paris, p 182Google Scholar
  35. Moquin-Tandon A (1849) Salsolaceae. In: de Candolle AP (ed) Prodromus systematis naturalis regni vegetabilis, vol 13. Masson, Paris, pp 41–219Google Scholar
  36. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818CrossRefPubMedGoogle Scholar
  37. Pyankov VI, Voznesenskaya EV, Kuz’min AN, Ku MSB, Ganko E, Franceschi VR, Black CC, Edwards GE (2000) Occurrence of C3 and C4 photosynthesis in cotyledons and leaves of Salsola species (Chenopodiaceae). Photosynth Res 63:69–84CrossRefPubMedGoogle Scholar
  38. Pyankov VI, Artyusheva EG, Edwards GE, Black CC, Soltis PS (2001a) Phylogenetic analysis of tribe Salsoleae (Chenopodiaceae) based on ribosomal ITS sequences: implications for the evolution of photosynthesis types. Am J Bot 88:1189–1198CrossRefPubMedGoogle Scholar
  39. Pyankov VI, Ziegler H, Kuz’min A, Edwards G (2001b) Origin and evolution of C4 photosynthesis in the tribe Salsoleae (Chenopodiaceae) based on anatomical and biochemical types in leaves and cotyledons. Plant Syst Evol 230:43–74CrossRefGoogle Scholar
  40. Rilke S (1999) Species diversity and polymorphism in Salsola sect. Salsola sensu lato (Chenopodiacaeae). Syst Geogr Pl 68:305–314CrossRefGoogle Scholar
  41. Schütze P, Freitag H, Weising K (2003) An integrated molecular and morphological study of the subfamily Suaedoideae Ulbr. (Chenopodiaceae). Plant Syst Evol 239:257–286CrossRefGoogle Scholar
  42. Sukhorukov AP (2008) Fruit anatomy of the genus Anabasis (Salsoloideae, Chenopodiaceae). Aust Syst Bot 21:431–442CrossRefGoogle Scholar
  43. Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (* and other methods), version 4.0. Sinauer, SunderlandGoogle Scholar
  44. Takhtajan A (2009) Flowering plants, vol 1, 2nd edn. Springer, BerlinGoogle Scholar
  45. 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 24:4876–4882CrossRefGoogle Scholar
  46. Tzvelev NN (1993) Notes on Chenopodiaceae of Eastern Europe. Ukr Bot Zhurn 50:78–85Google Scholar
  47. Ulbrich E (1934) Chenopodiaceae. In: Engler A, Prantl K (eds) Die natürlichen Pflanzenfamilien, 2nd edn. Duncker & Humblot, Leipzig, pp 379–584Google Scholar
  48. Voznesenskaya EV (1976) The ultrastructure of assimilating organs of some species of the family Chenopodiaceae, II (in Russian). Bot Zhurn 61:1546–1557Google Scholar
  49. Voznesenskaya EV, Artyusheva EG, Franceschi VR, Pyankov VI, Kiirats O, Ku MSB, Edwards GE (2001) Salsola arbusculiformis, a C3–C4 intermediate in Salsoleae (Chenopodiaceae). Ann Bot 88:337–348CrossRefGoogle Scholar
  50. Wang RZ (2007) C4 plants in the deserts of China: occurrence of C4 photosynthesis and its morphological functional types. Photosynthetica 45:167–171CrossRefGoogle Scholar
  51. Wei Y, Dong M, Huang ZY, Tan DY (2008) Factors influencing seed germination of Salsola affinis (Chenopodiaceae), a dominant annual halophyte inhabiting the deserts of Xinjiang, China. Flora 203:134–140Google Scholar
  52. 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, San Diego, pp 315–322Google Scholar
  53. Williams JT, Ford-Lloyd BV (1974) The systematics of the Chenopodiaceae. Taxon 23:353–354CrossRefGoogle Scholar
  54. Wilson PG (1984) Chenopodiaceae. In: George AS (ed) Flora of Australia, vol 4. Australian Government Publishing Service, Canberra, pp 313–317Google Scholar
  55. 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. Theor Appl Genet 101:724–732CrossRefGoogle Scholar
  56. Zhao KF, Fan H, Ungar IA (2002) Survey of halophyte species in China. Plant Sci 163:491–498CrossRefGoogle Scholar
  57. Zhu GL (1996) Origin, differentiation, and geographic distribution of the Chenopodiaceae (in Chinese with English abstract). Acta Phytotax Sin 34:486–504Google Scholar
  58. Zhu GL, Mosyankin SL, Clemants SE (2003) Chenopodiaceae. In: Wu ZY, Raven PH (eds) Flora of China, vol 5. Science Press, Beijing, pp 354–414Google Scholar
  59. Zurawski G, Perrot B, Bottomley W, Whitfeld PR (1981) The structure of the gene for the large subunit of ribulose 1, 5-bisphosphate carboxylase from spinach chloroplast DNA. Nucleic Acids Res 9:3251–3270CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Zhi-Bin Wen
    • 1
    • 2
  • Ming-Li Zhang
    • 1
    • 3
  • Ge-Lin Zhu
    • 4
  • Stewart C. Sanderson
    • 5
  1. 1.Key Laboratory of Biogeography and Bioresource in Arid LandXinjiang Institute of Ecology and Geography, Chinese Academy of SciencesUrumqiChina
  2. 2.Graduate University, Chinese Academy of SciencesBeijingChina
  3. 3.Institute of Botany, Chinese Academy of SciencesBeijingChina
  4. 4.Northwest Normal UniversityLanzhouChina
  5. 5.Shrub Sciences Laboratory, Intermountain Research Station, Forest ServiceU. S. Department of AgricultureOgdenUSA

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