Skip to main content
SpringerLink
Log in

The phylogeny and new classification of the genus Onobrychis (Fabaceae-Hedysareae): evidence from molecular data

  • Original Article
  • Published:
Plant Systematics and Evolution Aims and scope Submit manuscript

Abstract

The present study was conducted to analyze the phylogenetic status of the genus Onobrychis and to evaluate the monophyly of its subgenera and sections and relationship among them. We sequenced the nuclear ribosomal DNA internal transcribed spacer (nrDNA ITS) and three chloroplast regions trnL-F, rpl32/rpl32-trnL(UAG) and ndhF-rlp32 for phylogenetic reconstruction of 51 species of Onobrychis. In all of our analyses, Eversmannia subspinosa, Corethrodendron scoparium, Greuteria membranacea and G. argyrea were chosen as outgroups. Phylogenetic analyses were performed by maximum parsimony, maximum likelihood and Bayesian methods. Our molecular data indicate that Onobrychis is monophyletic and composed of two main clades, each corresponding to the redefined subgenus Onobrychis (including sections Onobrychis and Hemicyclobrychis) and subgenus Sisyrosema (including sections Afghanicae, Laxiflorae, Heliobrychis, Hymenobrychis, Insignes, Lipskyanae and Litvinovianae), respectively. Sections Lipskyanae and Litvinovianae are newly established and described, representing distinct lineages within the genus. Onobrychis splendida, a species hitherto without a sectional position, along with some members of sect. Anthyllium were retrieved representatives of section Lipskyanae. Sections Afghanicae, Insignes, Heliobrychis and Hymenobrychis (with the inclusion of two species of section Anthyllium) are monophyletic. Sections Dendrobrychis and Lophobrychis are reduced to synonymy of section Onobrychis and Anthyllium to synonymy of section Hymenobrychis. A taxonomic treatment for the genus is presented.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Abou-El-Enain M (2002) Chromosomal criteria and their phylogenetic implications in the genus Onobrychis Mill. sect. Lophobrychis (Leguminosae), with special reference to Egyptian species. Bot J Linn Soc 139:409–414. doi:10.1046/j.1095-8339.2002.00075.x

    Article  Google Scholar 

  • 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. Iranian J Bot 13:64–74

    Google Scholar 

  • Amirabadizadeh H, Abbassi M, Ranjbar M (2007) A new species of Onobrychis Sect. Heliobrychis (tribe Hedysarae) from Iran. Iranian J Bot 13:53–56

    Google Scholar 

  • Amirabadizadeh H, Ghanavati F, Abbassi M, Ranjbar M (2009) A new species of Onobrychis sect. Afghanicae (Fabaceae) from Iran. Iranian J Bot 15:45–50

    Google Scholar 

  • Amirahmadi A, Kazempour Osaloo S, Moein F, Kaveh A, Maassoumi AA (2014a) Molecular systematics of the tribe Hedysareae (Fabaceae) based on nrDNA ITS and plastid trnL-F and matK sequences. Pl Syst Evol 300:729–747. doi:10.1007/s00606-013-0916-5

    Article  CAS  Google Scholar 

  • Amirahmadi A, Kazempour Osaloo S, Khoshsokhan-Mozaffar M, Charkhchian MM (2014b) A new species of Onobrychis sect. Onobrychis (Fabaceae) from Iran. Turkish J Bot 38:658–664. doi:10.3906/bot-1309-54

    Article  Google Scholar 

  • 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 65:11–17. doi:10.1080/00087114.2012.678079

    Article  Google Scholar 

  • Avci S, Sancak C, Can A, Acar A, Pınar NM (2013) Pollen morphology of the genus Onobrychis (Fabaceae) in Turkey. Turkish J Bot 37:669–681. doi:10.3906/bot-1207-52

    Google Scholar 

  • Baldwin BJ, Sanderson MJ, Porter MJ, Wojciechowski MF, Campbell C, Donoghue JM (1995) The ITS region of nuclear ribosomal DNA: a valuable source of evidence of Angiosperm phylogeny. Ann Missouri Bot Gard 82:247–277. doi:10.2307/2399880

    Article  Google Scholar 

  • Ball PW (1978) Onobrychis. In: Tutin TG, Heywood VH, Burges NA, Moore DM, Valentine DH, Walters SM, Webb DA (eds) Flora Europaea, vol 2. Cambridge University Press, Cambridge, pp 187–191

    Google Scholar 

  • Cunningham CW (1997) Can three incongruence tests predict when data should be combined? Molec Biol Evol 14:733–740

    Article  CAS  PubMed  Google Scholar 

  • Dong W, Liu J, Yu J, Wang L, Zhou S (2012) Highly variable chloroplast markers for evaluating plant phylogeny at low taxonomic levels and for DNA barcoding. PLoS ONE 7:e35071. doi:10.1371/journal.pone.0035071

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 J Bot 86:887–899

    Article  CAS  Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15

    Google Scholar 

  • Duan L, Wen J, Yang X, Liu PL, Arslan E, Ertuğrul K, Chang ZY (2015) Phylogeny of Hedysarum and tribe Hedysareae (Leguminosae: Papilionoideae) inferred from sequence data of ITS, matK, trnL-F and psbA-trnH. Taxon 64:49–64. doi:10.12705/641.26

    Article  Google Scholar 

  • Edgar RC (2004) Muscle: multiple sequence alignment with high accuracy and high throughput. Nucl Acids Res 32:1792–1797. doi:10.1093/nar/gkh340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Farris JS, Kallersjo M, Kluge AG, Bult C (1995) Testing significance of incongruence. Cladistics 10:315–319. doi:10.1111/j.1096-0031.1994.tb00181.x

    Article  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 38:783–791. doi:10.2307/2408678

    Article  Google Scholar 

  • Grossheim AA (1972) Onobrychis Adans. (Leguminosae). In: Komarov VL, Shishkin BK, Bobrov EG (eds) Flora of the USSR, vol 13. Israel Program for Scientific Translations, Jerusalem, pp 244–281

    Google Scholar 

  • Hayot Carbonero C, Carbonero F, Smith LMJ, Brown TA (2012) Phylogenetic characterization of Onobrychis species with special focus on the forage crop Onobrychis viciifolia Scop. Genet Resources Crop Evol 59:1777–1788. doi:10.1007/s10722-012-9800-3

    Article  Google Scholar 

  • Hedge IC (1970) Onobrychis (Leguminosae-Hedysareae). In: Davis PH, Chamberlain DF, Matthews VA (eds) Flora of Turkey and the East Aegean Islands, vol 3. Edinburgh University Press, Edinburgh, pp 560–590

    Google Scholar 

  • Hesamzadeh Hejazi SM, Ziaei Nasab M (2010) Cytotaxonomy of some Onobrychis (Fabaceae) species and populations in Iran. Caryologia 63:18–31. doi:10.1080/00087114.2010.589705

    Article  Google Scholar 

  • Irfan E, Turgut-Balik D, Sahin A, Kursat M (2007) Total electrophoretic band patterns of some Onobrychis species growing in Turkey. Amer Eurasian J Agric Environ Sci 2:123–126

    Google Scholar 

  • Karamian R, Moradi Behjou A, Ranjbar M (2012) Anatomical findings of Onobrychis sect. Heliobrychis (Fabaceae) in Iran and their taxonomic implications. Turkish J Bot 36:27–31. doi:10.3906/bot-1010-2

    Google Scholar 

  • Kazempour Osaloo S, Maassoumi AA, Murakami N (2005) Molecular systematics of the Old World Astragalus (Fabaceae) as inferred from nrDNA ITS sequence data. Brittonia 57:367–381. doi:10.1663/0007-196X(2005)057[0367:MSOTOW]2.0.CO;2

  • Lamarck MM, De Candolle AP (1805) Flore Française. vol. 4, part 2, Paris, pp 401–946

  • Lewke Bandara N, Papini A, Mosti S, Brown T, Smith LMJ (2013) A phylogenetic analysis of genus Onobrychis and its relationships within the tribe Hedysareae (Fabaceae). Turkish J Bot 37:981–992. doi:10.3906/bot-1210-32

    Article  Google Scholar 

  • Lock JM (2005) Tribe Hedysarae. In: Lewis G, Schrire B, Mackinder B, Lock M (eds) Legumes of the world. Royal Botanical Gardens, Kew, pp 489–495

    Google Scholar 

  • Mabberley DJ (2008) The plant-book. A portable dictionary of the higher plants, 3rd edn. Cambridge University Press, Cambridge

    Google Scholar 

  • Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University, Uppsala

    Google Scholar 

  • Page DM (2001) Treeview (Win32) version 1.6.6. Available at: http://taxonomy.zoology.gla.ac.uk/rod/treeview.html

  • Pavlova DK, Manova VI (2000) Pollen morphology of the genera Onobrychis and Hedysarum (Hedysareae, Fabaceae) in Bulgaria. Ann Bot Fenn 37:207–217

    Google Scholar 

  • Podlech D (1967) Neue und bemerkenswerte Fabaceae aus Nordost-Afghanistan (beiträge zur Flora von Afghanistan II). Mitt Bot Staatssamml München 6:547–591

    Google Scholar 

  • Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: advantages of akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst Biol 53:793–808. doi:10.1080/10635150490522304

    Article  PubMed  Google Scholar 

  • Ranjbar M, Amirabadizadeh H, Karamian R, Ghahremani MA (2004) Notes on Onobrychis sect. Heliobrychis (Fabaceae) in Iran. Willdenowia 34:187–190. doi:10.3372/wi.34.34116

    Article  Google Scholar 

  • Ranjbar M, Karamian R, Hajmoradi F (2009) Taxonomic notes on Onobrychis sect. Hymenobrychis (Fabaceae, Hedysareae) in Iran. Novon 19:215–218. doi:10.3417/2007119

    Article  Google Scholar 

  • Ranjbar M, Karamian R, Hadadi A (2010) Cytosystematics of three Onobrychis species (Fabaceae) in Iran. Caryologia 63:237–249. doi:10.1080/00087114.2010.10589733

    Article  Google Scholar 

  • Ranjbar M, Hajmoradi F, Karamian R (2012) An overview on cytogenetics of the genus Onobrychis (Fabaceae) with special reference to O. sect. Hymenobrychis from Iran. Caryologia 65:187–198. doi:10.1080/00087114.2012.735887

    Article  Google Scholar 

  • Rechinger KH (1984) Hedysareae. In: Rechinger KH (ed) Flora Iranica, vol 157. Akademische Druck, Graz, pp 365–475

    Google Scholar 

  • Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. doi:10.1093/sysbio/sys029

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 2:91–99

    Google Scholar 

  • Safaei Chaei Kar S, Ghanavati F, Naghavi MR, Amirabadi-zade H, Rabiee R (2014) Molecular phylogenetics of the Onobrychis genus (Fabaceae: Papilionoideae) using ITS and trnL–trnF DNA sequence data. Austral J Bot 62:235–250. doi:10.1071/BT13279

    Article  CAS  Google Scholar 

  • 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 92:6813–6817

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shaw J, Lickey EB, Schilling EE, Small RL (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. doi:10.3732/ajb.94.3.275

    Article  CAS  Google Scholar 

  • Silvestro D, Michalak I (2012) raxmlGUI: a graphical front-end for RAxML. Organisms Divers Evol 12:335–337. doi:10.1007/s13127-011-0056-0

    Article  Google Scholar 

  • Širjaev G (1925) Onobrychis generis revisio critica, pars prima. Spisy Přír Fak Masarykovy Univ 56:1–197

    Google Scholar 

  • Širjaev G (1926) Onobrychis generis revisio critica, partes secunda et tertia. Spisy Přír Fak Masarykovy Univ 76:1–165

    Google Scholar 

  • Swofford DL (2002) PAUP*: Phylogenetic analysis using parsimony (*and other methods), Version 4.0b10. Sinauer Associates, Sunderland

    Google Scholar 

  • 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. doi:10.1007/BF00037152

    Article  CAS  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molec Biol Evol 30:2725–2729. doi:10.1093/molbev/mst197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Townsend CC (1974) Papilionaceae. In: Townsend CC, Guest ER (eds) Flora of Iraq, vol 3. Ministry of Agriculture and Agrarian Reform of the Republic of Iraq, Baghdad, pp 54-601

    Google Scholar 

  • 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 315–322

    Google Scholar 

  • 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 24:409–437. doi:10.2307/2419698

    Article  Google Scholar 

  • Yildiz B, Ciplak B, Aktoklu E (1999) Fruit morphology of sections of the genus Onobrychis Miller (Fabaceae) and its phylogenetic implications. Israel J Pl Sci 47:269–282. doi:10.1080/07929978.1999.10676784

    Article  Google Scholar 

  • Zarrabian M, Majidi MM (2015) Genetic diversity and relationships within and among Onobrychis species using molecular markers. Turkish J Bot 39:681–692. doi:10.3906/bot-1406-47

    Article  CAS  Google Scholar 

  • 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, Austin

Download references

Acknowledgments

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). We would like to thank the staff of the herbaria of, FUMH, HKNRRC, HQNRRC, MSB, TARI and TUH to allow studying herbarium specimens and providing leaf materials. We also thank H. Zare for editing and improving linguistic of the text. The trees resulting from Parsimony, Likelihood and Bayesian analyses of nrDNA ITS and plastid datasets, trnL–F, rpl32/rpl32-trnL(UAG) and ndhF-rpl32 are presented as Electronic Supplementary Material in Online resource 1, 2, 3, 4. The aligned data matrix used in this study is presented as Online Resource 5.

Author information

Authors and Affiliations

  1. School of Biology and Institute of Biological Sciences, Damghan University, Damghan, 36716-41167, Iran

    Atefe Amirahmadi & Reza Naderi

  2. Department of Plant Biology, Faculty of Biological Sciences, Tarbiat Modares University, Tehran, 14115-154, Iran

    Shahrokh Kazempour-Osaloo & Akram Kaveh

  3. Department of Botany, Research Institute of Forests and Rangelands, Tehran, 13185-116, Iran

    Ali A. Maassoumi

Authors
  1. Atefe Amirahmadi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shahrokh Kazempour-Osaloo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Akram Kaveh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ali A. Maassoumi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Reza Naderi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shahrokh Kazempour-Osaloo.

Additional information

Handling editor: Christoph Oberprieler.

Electronic supplementary material

Below is the link to the electronic supplementary material.

606_2016_1343_MOESM1_ESM.pdf

Online Resource 1 Fifty percent majority rule consensus tree resulting from Bayesian inference of the nrDNA ITS dataset. Numbers above branches are posterior probability and likelihood as well as parsimony bootstrap values, respectively. Values<50 % were not shown (PDF 132 kb)

606_2016_1343_MOESM2_ESM.pdf

Online Resource 2 Fifty percent majority rule consensus tree resulting from Bayesian inference of the plastid trnL-F dataset. Numbers above branches are posterior probability and likelihood as well as parsimony bootstrap values, respectively. Values<50 % were not shown (PDF 129 kb)

606_2016_1343_MOESM3_ESM.pdf

Online Resource 3 Fifty percent majority rule consensus tree resulting from Bayesian inference of the plastid rpl32/rpl32- trnLUAG dataset. Numbers above branches are posterior probability and likelihood as well as parsimony bootstrap values, respectively. Values<50 % were not shown (PDF 129 kb)

606_2016_1343_MOESM4_ESM.pdf

Online Resource 4 Fifty percent majority rule consensus tree resulting from Bayesian inference of the plastid ndhF-rpl32 dataset. Numbers above branches are posterior probability and likelihood as well as parsimony bootstrap values, respectively. Values<50 % were not shown (PDF 132 kb)

Online Resource 5 The aligned data matrix used in this study (NEX 171 kb)

Information on Electronic Supplementary Material

Information on Electronic Supplementary Material

Online Resource 1. Fifty percent majority rule consensus tree resulting from Bayesian inference of the nrDNA ITS dataset.

Online Resource 2. Fifty percent majority rule consensus tree resulting from Bayesian inference of the plastid trnL-F dataset.

Online Resource 3. Fifty percent majority rule consensus tree resulting from Bayesian inference of the plastid rpl32/rpl32- trnLUAG dataset.

Online Resource 4. Fifty percent majority rule consensus tree resulting from Bayesian inference of the plastid ndhF-rpl32 dataset.

Online Resource 5. The aligned data matrix used in this study.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Amirahmadi, A., Kazempour-Osaloo, S., Kaveh, A. et al. The phylogeny and new classification of the genus Onobrychis (Fabaceae-Hedysareae): evidence from molecular data. Plant Syst Evol 302, 1445–1456 (2016). https://doi.org/10.1007/s00606-016-1343-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00606-016-1343-1

Keywords

Search

Navigation