Plant Systematics and Evolution

, Volume 300, Issue 4, pp 729–747 | Cite as

Molecular systematics of the tribe Hedysareae (Fabaceae) based on nrDNA ITS and plastid trnL-F and matK sequences

  • Atefe Amirahmadi
  • Shahrokh Kazempour Osaloo
  • Fatemeh Moein
  • Akram Kaveh
  • Ali Asghar Maassoumi
Original Article


This study represents the molecular phylogeny of the tribe Hedysareae using nrDNA ITS and plastid trnL-F and matK sequence data. The molecular analyses united nine Hedysaroid genera in a well-supported monophyletic group (tribe Hedysareae). The tribe is circumscribed here as comprising Alhagi, Corethrodendron, Ebenus, Eversmannia, Hedysarum, Onobrychis, Sulla, Taverniera, and Greuteria. Our analyses revealed that Caragana and allies form a well-supported clade, the so-called Caraganean clade, which is weakly allied with the Hedysareae. Within the Hedysareae, Alhagi is the first diverging lineage followed by Sulla clade and a large assemblage of the other Hedysaroid genera. Ebenus and Taverniera were monophyletic. All analyses showed that Hedysarum is not monophyletic in the present circumscription. Most members of the genus with the inclusion of Sartoria hedysaroides were gathered in a single clade. The two other Hedysarum species (H. membranaceum and H. argyreum) were sister taxa and placed in a clade with Eversmannia subspinosa and Corethrodendron. Onobrychis was retrieved as a weakly supported clade. On the basis of the present sequence data together with non-molecular characteristics, we transferred H. aculeolatum to Sulla and S. hedysaroides to Hedysarum as well as elevated H. membranaceum and H. argyreum to the new generic rank named as Greuteria Amirahmadi & Kaz. Osaloo. A diagnostic key to the genera of the tribe is provided.


Fabaceae Greuteria Hedysareae Molecular phylogeny nrDNA ITS Plastid matK and trnL-F 



The present study was financially supported in part by Grant-in-Aids for Scientific Research, No. 89002433, to S. K. O (corresponding author) from INSF (Iran National Science Foundation). This work represents partial fulfillment of the requirement for obtaining a PhD degree by the first author from Tarbiat Modares University. We would like to thank the staff of the herbaria of ANK, FUMH, G, GAZI, MSB, TARI, TUH, KNRCH, and WANRCH to allow studying herbarium specimens and providing leaf materials. We would like to thank the anonymous reviewers for their comments on the improving the manuscript.


  1. Ahangarian S, Kazempour Osaloo S, Maassoumi AA (2007) Molecular phylogeny of the tribe Hedysareae with special reference to Onobrychis (Fabaceae) as inferred from nrDNA ITS sequences. Iran Jour Bot 13:64–74Google Scholar
  2. Aksoy H, Unal F, Aytac Z (2001) Karyological study on four endemic Ebenus L. Taxa (Fabaceae) in Turkey. Caryologica 54:307–311CrossRefGoogle Scholar
  3. Ali SI (1977) Papilionaceae. In: Nasir E, Ali SI (eds) Flora of West Pakistan, no. 100. University of Karachi, KarachiGoogle Scholar
  4. Amirahmadi A, Kazempour Osaloo S, Maassoumi AA (2010) Loss of chloroplast trnLUAA intron in two species of Hedysarum (Fabaceae): evolutionary implications. IJB 8:150–155Google Scholar
  5. Archie JW (1989) A randomization test for phylogenetic information in systematic data. Syst Zool 38:239–252CrossRefGoogle Scholar
  6. Arslan E, Ertuğrul K (2010) Genetic relationships of the genera Onobrychis, Hedysarum, and Sartoria using seed storage proteins. Turk J Biol 34:1–7Google Scholar
  7. Arslan E, Ertuğrul K, Tugay O, Dural H (2012) Karyological studies of the genus Onobrychis Mill. and the related genera Hedysarum L. and Sartoria Boiss. & Heldr. (Fabaceae, Hedysareae) from Turkey. Caryologia 65:11–17CrossRefGoogle Scholar
  8. Awmack CS, Lock JM (2002) The genus Alhagi (Leguminosae: Papilionoideae) in the Middle East. Kew Bull 57:435–443CrossRefGoogle Scholar
  9. Aytaç Z (2000) The genus Ebenus L. (Leguminosae/Fabaceae) in Turkey. Karaca Arbor Mag 5:145–171Google Scholar
  10. Baldwin BG (1992) Phylogenetic utility of the internal transcribed spacer of nuclear ribosomal DNA in plants: an example from the Compositae. Mol Phylogenet Evol 1:3–16PubMedCrossRefGoogle Scholar
  11. Baldwin BJ, Sanderson MJ, Markprter J, Wojciechowski MF, Campbell C, Donoghue JM (1995) The ITS region of nuclear ribosomal DNA: a valuable source of evidence of Angiosperm phylogeny. Ann Miss Bot Gard 82:247–277CrossRefGoogle Scholar
  12. Basiner TFJ (1845) Enumeratio monographica specierum generis Hedysari. Mém Acad Imp Sci St Pétersbourg 6:45–97Google Scholar
  13. Battandier JA (1888) Dicotylédones–Thalamiflores. In: Battandier JA, Trabut LC (eds) Flore de ľ Algérie, Fascicule 1. Typographie Adolphe Jourdan, AlgerGoogle Scholar
  14. Bentham G (1853) On three new genera connected with the Indian flora. Hooker’s J Bot Kew Gard Misc 5:304–309Google Scholar
  15. Bentham G (1865) Leguminosae. In: Bentham G, Hooker JD (eds) Genera plantarum, vol 1, part 2. L. Reeve & Co., London, pp 434–600Google Scholar
  16. Boissier E (1856) Diagnoses plantarum Orietalium Novarum. Ser. II, vol 5. Herrmann, Lipsiae, p 92Google Scholar
  17. Chamberlain DF (1970) Alhagi. In: Davis PH (ed) Flora of Turkey and the East Aegean Island, vol 3. Edinburgh University Press, Edinburg, pp 596–597Google Scholar
  18. Chase MW, Cowan RS, Hollingsworth PM et al (2007) A proposal for a standardised protocol to barcode all land plants. Taxon 56:295–299Google Scholar
  19. Chennaoui H, Marghali S, Marrakchi M, Trifi- Farah N (2007) Phylogenetic relationships in the North African genus Hedysarum as inferred from ITS sequences of nuclear ribosomal DNA. Genet Resour Crop Evol 54:389–397CrossRefGoogle Scholar
  20. Chennaoui-Kourda H, Marghali M, Marrakchi M, Trifi-Farah N (2007) genetic diversity of Sulla genus (Hedysareae) and related species using inter-simple sequence repeat (ISSR) markers. Biochem Syst Ecol 35:682–688CrossRefGoogle Scholar
  21. Chennaoui-Kourda H, Marghali S, Zitouna N, Trifi-Farah N (2012) Phylogenetic relationships of Mediterranean Hedysarea species assessed by AFLP markers. Plant Syst Evol 298:51–58CrossRefGoogle Scholar
  22. Choi BH, Ohashi H (1996) Pollen morphology and taxonomy Hedysarum and and its related genera of the tribe Hedysareae (Leguminosae—Papilinoideae). J Jap Bot 71:191–213Google Scholar
  23. Choi BH, Ohashi H (1998) Proposal to conserve the name Hedysarum (Leguminosae: Papilionoideae) with a conserved type. Taxon 47:977CrossRefGoogle Scholar
  24. Choi BH, Ohashi H (2003) Generic criteria and an infrageneric system for Hedysarum and related genera (Papilinoideae–Leguminosae). Taxon 52:567–576CrossRefGoogle Scholar
  25. Choi BH, T Nemato, Ohashi H (1999) Anatomy of nodal regions and leaves in Hedysarum and related genera (Leguminosae). J Jap Bot 74:236–250Google Scholar
  26. Chrtková-Žertová A (1968) Hedysarum L. In: Tutin TG et al (eds) Flora Europaea, vol 2. Cambridge University Press, Cambridge, pp 185–187Google Scholar
  27. Cui H (1998) Flora Reipublicae Popularis Sinicae, vol 42. Science Press, BeijingGoogle Scholar
  28. Cunningham CW (1997) Can three incongruence tests predict when data should be combined? Mol Biol Evol 14:733–740PubMedCrossRefGoogle Scholar
  29. De Candolle AP (1825) Prodromus systematis naturalis regni vegetabilis, vol 2. Treuttel and Wurtz, Paris, p 307Google Scholar
  30. Douzery E, Pridgeon A, Kores P, Linder HP, Kurzweil H, Chase M (1999) Molecular phylogenetics of Diseae (Orchidaceae): a contribution from nuclear ribosomal ITS sequences. Amer Jour Bot 86:887–899CrossRefGoogle Scholar
  31. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15Google Scholar
  32. Edgar RC (2004) Muscle: multiple sequence alignment with high accuracy and high throughput. Nucl Acids Res 32:1792–1797PubMedCentralPubMedCrossRefGoogle Scholar
  33. Ems SC, Morden CW, Dixon CK, Wolfe KH, dePamphilis CW, Palmer JD (1995) Transcription, splicing and editing of plastid RNAs in the non-photosynthetic plant Epifagus virginiana. Plant Mol Biol 29:721–733PubMedCrossRefGoogle Scholar
  34. Farris JS, Kallersjo M, Kluge AG, Bult C (1995) Testing significance of incongruence. Cladistics 10:315–319CrossRefGoogle Scholar
  35. Fedtschenko BA (1902) Generis Hedysari revisio. Acta Horti Petrop 19:183–342Google Scholar
  36. Fedtschenko BA (1972) Hedysarum L. (Leguminosae). In: Komarov VL, Shishkin BK, Bobrov EG (eds) Flora of the USSR, vol 13. Israel Program for Scientific Translation, Jerusalem, pp 199–243Google Scholar
  37. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 38:783–791CrossRefGoogle Scholar
  38. Goldblatt P (1981) Cytology and the phylogeny of Leguminosae. In: Polhill RM, Raven PH (eds) Advances in legume systematics, part 2. Royal Botanic Gardens, Kew, pp 427–463Google Scholar
  39. Gorshkova SG (1972) Eversmannia Bge. (Leguminosae). In: Komarov VL, Shishkin BK, Bobrov EG (eds) Flora of the USSR, vol 13. Israel Program for Scientific Translation, Jerusalem, pp 198–199Google Scholar
  40. Greuter W, Raus T (1986) Med-Checklist Notulae 13. Willdenowia 16:103–116Google Scholar
  41. Grossheim AA (1972) Onobrychis Adans. (Leguminosae). In: Komarov VL, Shishkin BK, Bobrov EG (eds) Flora of the USSR, vol 13. Israel Program for Scientific Translation, Jerusalem, pp 244–281Google Scholar
  42. Hall TA (1999) BioEdit: a user friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98Google Scholar
  43. Hedge IC (1970) Hedysarum, Onobrychis and Sartoria. In: Davis PH (ed) Flora of Turkey and the East Aegean Islands, vol 3. Edinburgh University Press, Edinburgh, pp 549–590Google Scholar
  44. Hilu KW, Liang H (1997) The matK gene: sequence variation and application in plant systematics. Am J Bot 84:830–839PubMedCrossRefGoogle Scholar
  45. Hilu KW, Borsch T, Muller K, Soltis DE, Soltis PS, Savolainen V, Chase MW et al (2003) Angiosperm phylogeny based on matK sequence information. Am J Bot 90:1758–1776PubMedCrossRefGoogle Scholar
  46. Huber-Morath A (1970) Ebenus L. In: Davis PH (ed) Flora of Turkey and the East Aegean Islands, vol 3. Edinburgh University Press, Edinburgh, pp 590–596Google Scholar
  47. Hutchinson J (1964) The genera of flowering plants, vol 1. Oxford University Press, OxfordGoogle Scholar
  48. Javanmardi F, Kazempour Osaloo S, Maassoumi AA, Nejadsattari T (2012) Molecular phylogeny of Astragalus section Alopecuroidei (Fabaceae) and its allies based on nrDNA ITS and three cpDNAs, matK, trnT-trnYand trnH-psbA sequences. Biochem Syst Ecol 45:171–178CrossRefGoogle Scholar
  49. Johnson LA, Soltis DE (1995) Phylogenetic inference using matK sequences. Ann Mo Bot Gard 82:149–175CrossRefGoogle Scholar
  50. Kazemi M, Kazempour Osaloo S, Maassoumi AA, Rastegar Pouyani E (2009) Molecular phylogeny of selected Old World Astragalus (Fabaceae): incongruence among chloroplast trnL, ndhF and nuclear ribosomal DNA ITS sequences. Nord J Bot 27:425–436CrossRefGoogle Scholar
  51. Kazempour Osaloo S, Kawano S (1999) Molecular systematics of Trilliaceae II. Phylogenetic analyses of Trillium and its allies using sequences of rbcL and matK genes of cpDNA and internal transcribed spacers of 18S-26S nr DNA. Plant Spec Biol 14:75–94CrossRefGoogle Scholar
  52. Kazempour Osaloo S, Utech FH, Ohara M, Kawano S (1999) Molecular systematics of Trilliaceae I. Phylogenetic analyses of Trillium using matK gene sequences. J Plant Res 112:35–49CrossRefGoogle Scholar
  53. Kazempour Osaloo S, Maassoumi AA, Murakami N (2005) Molecular systematics of the Old World Astragalus (Fabaceae) as inferred from nrDNA ITS sequence data. Brittonia 57:367–381CrossRefGoogle Scholar
  54. Kenicer G, Kajita T, Pennington R, Murata J (2005) Systematics and biogeography of Lathyrus (Leguminoseae) based on internal transcribed spacer and cpDNA sequence data. Am J Bot 92:1199–1209PubMedCrossRefGoogle Scholar
  55. Lahaye R, Van der Bank M, Bogarin D, Warner J, Pupulin F, Gigot G, Maurin O, Duthoit Barraclough TG, Savolainen V (2008) DNA barcoding the floras of biodiversity hotspots. PNAS USA 105:2923–2928PubMedCentralPubMedCrossRefGoogle Scholar
  56. Lewis G, Schrire B, Mackinder B, Lock M (2005) Legumes of the world. Royal Botanical Gardens, KewGoogle Scholar
  57. Linnaeus C (1763) Species plantarum, vol 2, 2nd edn. Impensis Laurentii Salvii, Holmiae Google Scholar
  58. Liu Y, Xu LR, Chang Z, Zhu X, Sun H, Yakovlev GP, Choi BH, Larsen K, Bartholomew B (2010) Tribe Hedysareae (Fabaceae) In: Wu ZY, Raven PH, Hong DY (eds) Flora of China, vol 10. Science Press, Beijing, and Missouri Botanical Garden Press, St. Louis, pp 512–545Google Scholar
  59. Lock JM (2005) Tribe Hedysarae. In: Lewis G, Schrire B, Mackinder B, Lock M (eds) Legumes of the world. Royal Botanical Gardens, Kew, pp 489–495Google Scholar
  60. Lock JM, Simpson K (1991) Legume of the West Asia: a check-list. Royal Botanical Gardens, KewGoogle Scholar
  61. Mabberley DJ (2008) The plant-book. A portable dictionary of the higher plants, 3rd edn. Cambridge University Press, CambridgeGoogle Scholar
  62. Maire R (1939) Contribution á ľétude de la Flore de ľAfrique du Nord. Bull Soc Hist Nat Afrique N 30:327–370Google Scholar
  63. Meikle RD (1977) Flora of Cyprus, vol 1. Bentham–Moxon Trust, Royal Botanic GardensGoogle Scholar
  64. Mozaffarian V (1988) New species and new plant records from Iran. Iran J Bot 4:61–70Google Scholar
  65. Neuhaus H, Link G (1987) The chloroplast tRNALYS(UUU) gene from mustard (Sinapis alba) contains a class II intron potentially coding for a matures related polypeptide. Curr Genet 11:251–257PubMedCrossRefGoogle Scholar
  66. Newmaster SG, Fazekas AJ, Steeves RAD, Janovec J (2008) Testing candidate plant barcode regions in the Myristicaceae. Mol Ecol Res 8:480–490CrossRefGoogle Scholar
  67. Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University, UppsalaGoogle Scholar
  68. Oskoueiyan R, Kazempour Osaloo S, Maassoumi AA, Nejadsattari T, Mozaffarian V (2010) Phylogenetic status of Vavilovia formosa (Fabaceae–Fabeae) based on nrDNA ITS and cpDNA sequences. Biochem Syst Ecol 38:313–319CrossRefGoogle Scholar
  69. Page DM (2001) Treeview (Win32) version 1.6.6. Available at.
  70. Plunkett GM, Downie SR (1999) Major lineages within Apiaceae subfamily Apioideae: a comparison of chloroplast restriction site and DNA sequence data. Am J Bot 86:1014–1026PubMedCrossRefGoogle Scholar
  71. Polhill RM (1981) Hedysareae. In: Polhil RM, Rave PH (eds) Advances in legume systematics, part 1. Royal Botanic Gardens, Kew, pp 367–370Google Scholar
  72. Polhill RM, Raven PH (eds) (1981) Advances in legume systematics, part 1. Royal Botanic Gardens, Kew, pp 1–425Google Scholar
  73. Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: advantages of akaike information criterion and Bayesian approaches over likelihood ratio tests. Sys Biol 53:793–808CrossRefGoogle Scholar
  74. Qiu YL, Lee J, Bernasconi-Quadroni F, Soltis DE, Soltis PS, Zanis M, Zimmer EA, Chen Z, Savolainen V, Chase MW (1999) The earliest angiosperms: evidence from mitochondrial, plastid and nuclear genomes. Nature 402:404–407PubMedCrossRefGoogle Scholar
  75. Ragupathy S, Newmaster SG, Murugesan M, Balasubramaniam V (2009) DNA barcoding discriminates a new cryptic grass species revealed in an ethnobotany study by the hill tribes of the Western Ghats in southern India. Mol Ecol Resour 9:164–171PubMedCrossRefGoogle Scholar
  76. Ranjbar M, Karamian R (2003) Caraganeae, a newtribe with notes on the genus Chesneya Lindel. (Fabaceae) from flora of the Iran. Thaiszia J Bot 13:67–75Google Scholar
  77. Rechinger KH (1984) Tribus Hedysareae (Papilionaceae II). In: Rechinger KH (ed) Flora Iranica, no. 157. Akademische Druck, Graz, pp 365–475Google Scholar
  78. Riahi M, Zarre S, Maassoumi AA, Kazempour Osaloo S, Wojciechowski MF (2011) Towards a phylogeny for Astragalus section Caprini (Fabaceae) and its allies based on nuclear and plastid DNA sequences. Plant Syst Evol 293:119–133CrossRefGoogle Scholar
  79. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1–210CrossRefGoogle Scholar
  80. Safaei Chaei Kar S, Ghanavati F, Mozafari J, Naghavi MR, Amirabadizadeh H, Darvish F (2012) Phylogenetic relationships of Onobrychis Mill. (Fabaceae: Papilionoideae) based on ITS sequences of nuclear ribosomal DNA and morphological traits. Crop Breed J 2:91–99Google Scholar
  81. Sanderson MJ, Wojciechowski MF (1996) Diversification rates in a temperate legume clade: “are there so many species” of Astragalus (Fabaceae). Am J Bot 83:1488–1502CrossRefGoogle Scholar
  82. Sang T, Crawford DJ, Stuessy T (1995) Documentation of reticulate evolution in peonies (Paeonia) using internal transcribed spacer sequences of nuclear ribosomal DNA: implication for biogeography and concerted evolution. Proc Natl Acad Sci USA 92:6813–6817PubMedCentralPubMedCrossRefGoogle Scholar
  83. Selvaraj D, Sarma RK, Sathishkuman R (2008) Phylogenetic analysis of chloroplast matK gene from Zingiberaceae for plant DNA barcoding. Bioinformation 3:24–27PubMedCentralPubMedCrossRefGoogle Scholar
  84. Shaperenko KK (1972) Alhagi Adans. (Leguminosae). In: Komarov VL, Shishkin BK, Bobrov EG (eds) Flora of the USSR, vol 13. Israel Program for Scientific Translation, Jerusalem, pp 281–285Google Scholar
  85. Shaw J, Lickey E, Beck JT, Farmer SB, Liu W, Miller J, Siripun KC, Winder CT, Schilling EE, Small RL (2005) The Tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. Am J Bot 92:42–166Google Scholar
  86. Silvestro D, Michalak I (2011) raxmlGUI: a graphical front-end for RAxML. Org Divers Evol 12:335–337CrossRefGoogle Scholar
  87. Širjaev G (1925) Onobrychis generis revisio critica. Pars prima. Publications Faculte des Sciences de l’ Université Masaryk 56:1–197Google Scholar
  88. Soltis DE, Kuzoff RK, Conti E, Gornall R, Ferguson K (1996) matK and rbcL gene sequence data indicate that Saxifraga (Saxifragaceae) is polyphyletic. Am J Bot 83:371–382CrossRefGoogle Scholar
  89. Starr JR, Naczi RFC, Chouinard BN (2009) Plant DNA barcodes and species resolution in sedges (Carex, Cyperaceae). Mol Ecol Resour 9:151–163PubMedCrossRefGoogle Scholar
  90. Steele KP, Vilgalys R (1994) Phylogenetic analyses of Polemoniaceae using nucleotide sequences of the Plastid gene matK. Syst Bot 19:126–142CrossRefGoogle Scholar
  91. Steele KP, Wojciechowski MF (2003) Phylogenetic analyses of tribes Trifolieae and Vicieae based on sequences of the plastid gene matK (Papilionoideae: Leguminosae). In: Klitgaard BB, Bruneau A (eds) Advances in legume systematics, part 10. Higher level systematics. Royal Botanic Gardens, Kew, pp 355–370Google Scholar
  92. Stirton CH (2005) Tribe Psoraleeae. In: Lewis G, Schrire B, Mackinder B, Lock M (eds) Legumes of the world. Royal Botanical Gardens, Kew, pp 447–451Google Scholar
  93. Sugita M, Shinozaki K, Sugiura M (1985) Tobacco chloroplast tRNALys(UUU) gene contains a 2.5-kilobase-pair intron: an open reading frame and a conserved boundary sequence in the intron. P N A S USA 82:3557–3561CrossRefGoogle Scholar
  94. Sun H, Bartholomew B (2010) Eversmannia (Fabaceae–Hedysareae). In: Wu ZY, Raven PH, Hong DY (eds) Flora of China, vol 10. Science Press, Beijing, and Missouri Botanical Garden Press, St. Louis, pp 526Google Scholar
  95. Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (*and other methods), Version 4.0b10. Sinauer Associates, SunderlandGoogle Scholar
  96. Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal Primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol Biol 17:1105–1109PubMedCrossRefGoogle Scholar
  97. Thulin M (1985) Revision of Taverniera (Leguminosae: Papilionoideae). Symb Bot Ups 25:44–94Google Scholar
  98. Townsend CC (1974) Leguminales. In: Townsend CC, Guest ER (eds) Flora of Iraq, vol 3. Ministry of Agriculture and Agrarian Reform of the Republic of Iraq, Republic of IraqGoogle Scholar
  99. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis DH (ed) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322Google Scholar
  100. Wojciechowski MF (2003) Reconstructing the phylogeny of legumes (Leguminosae): an early 21st century perspective. In: Klitgaard B, Bruneau A (eds) Advances in legume systematics, part 10. Royal Botanic Gardens, Kew, pp 5–35Google Scholar
  101. Wojciechowski MF (2005) Astragalus (Fabaceae): a molecular phylogenetic perspective. Brittonia 57:382–399CrossRefGoogle Scholar
  102. Wojciechowski MF, Sanderson MJ, Hu JM (1999) Evidence on the monophyly of Astragalus (Fabaceae) and its major subgroups based on nuclear ribosomal DNA ITS and chloroplast DNA trnL intron data. Syst Bot 24:409–437CrossRefGoogle Scholar
  103. Wojciechowski MF, Sanderson MJ, Steele KP, Liston A (2000) Molecular phylogeny of the “temperate herbaceous tribes” of papilionoid legumes: a super tree approach. In: Herendeen P, Bruneau A (eds) Advances in legume systematics, part 9. Royal Botanic Garden, Kew, pp 277–298Google Scholar
  104. Wojciechowski MF, Lavin M, Sanderson MJ (2004) A phylogeny of Legumes (Leguminosae) based on analysis of the plastid matK gene resolves many well-supported subclades within the family. Am J Bot 91:1846–1862PubMedCrossRefGoogle Scholar
  105. Xu LR, Choi BH (2010a) Corethrodendron (Fabaceae–Hedysareae) In: Wu ZY, Raven PH, Hong DY (eds) Flora of China, vol 10. Science Press, Beijing, and Missouri Botanical Garden Press, St. Louis, pp 512–514Google Scholar
  106. Xu LR, Choi BH (2010b) Hedysarum (Fabaceae–Hedysareae). In: Wu ZY, Raven PH, Hong DY (eds) Flora of China, vol 10. Science Press, Beijing, and Missouri Botanical Garden Press, St. Louis, pp 514–525Google Scholar
  107. Yakolev GP, Sytin AK, Roskov YR (1996) Legumes of Northern Eurasia: a check-list. Royal Botanic Gardens, KewGoogle Scholar
  108. Yakovelov GP (1979) Notes on the taxonomy of the genus Alhagi Gagneb (Fabaceae). Bot Zhurn (Mosc Leningr) 64:1794–1799Google Scholar
  109. Yildiz B, Ciplak B, Aktoklu E (1999) Fruit morphology of sections of the genus Onobrychis Miller (Fabaceae) and its phylogenetic implications. Isr J Plant Sci 47:269–282CrossRefGoogle Scholar
  110. Yu WB, Huang PH, Ree RH, Liu ML, Li DZ, Wang H (2011) DNA barcoding of Pedicularis L. (Orobanchaceae): evaluating four universal barcode loci in a large and hemiparasitic genus. J Syst Evol 49:425–437CrossRefGoogle Scholar
  111. Zwickl D (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. PhD thesis, University of Texas at Austin, USAGoogle Scholar

Copyright information

© Springer-Verlag Wien 2013

Authors and Affiliations

  • Atefe Amirahmadi
    • 1
  • Shahrokh Kazempour Osaloo
    • 1
  • Fatemeh Moein
    • 1
  • Akram Kaveh
    • 1
  • Ali Asghar Maassoumi
    • 2
  1. 1.Tarbiat Modares UniversityTehranIran
  2. 2.Research Institute of Forests and RangelandsTehranIran

Personalised recommendations