Molecular phylogeny of Onobrychis sect. Onobrychis (Fabaceae-Hedysareae) with insights into its taxonomy and character evolution

ANAHITA HADADI; AKRAM KAVEH; HANYIEH NAFISI; SHAHROKH KAZEMPOUR-OSALOO

doi:10.11646/phytotaxa.592.3.2

Issue: Vol. 592 No. 3: 20 April 2023

Type: Article

Published: 2023-04-20

DOI: 10.11646/phytotaxa.592.3.2

Page range: 196-216

Abstract views: 168

PDF downloaded: 6

**Molecular phylogeny of Onobrychis sect. Onobrychis (Fabaceae-Hedysareae) with insights into its taxonomy and character evolution**

ANAHITA HADADI⁺⁻
AKRAM KAVEH⁺⁻
HANYIEH NAFISI⁺⁻
SHAHROKH KAZEMPOUR-OSALOO⁺⁻

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

Phylogenetic analysis character evolution Onobrychis sect. Onobrychis monophyly subsection Eudicots

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Abstract

Onobrychis sect. Onobrychis, as the most species-rich section of the genus Onobrychis, ranges from Central Asia to Europe with a south extension into North Africa. In this study, we concentrated on the systematics of previously poorly represented O.sect. Onobrychis using a substantial taxon sampling. To test the monophyly of the section as well as to clarify interspecific relationships, the nuclear ribosomal DNA internal transcribed spacer(nrDNA ITS) and three chloroplast sequences (ndhF-rlp32, rpl32-trnL_(UAG), and trnG_(UCC)-trnS_(GCU)) were employed. Phylogenetic analyses were performed by maximum likelihood and Bayesian inferences. The results showed that O.sect. Onobrychis is monophyletic and composed of two main well-supported clades which are redefined as two subsections (O.subsect. Onobrychis, O. subsect. Macropterae).Ancestral character reconstruction of morphological traits: life form, wing to standard ratio, chromosome number, and ploidy level, indicated that short-winged petal is a synapomorphy for a group of species in the section while other traits have undergone parallel evolution. Possessing the basic chromosome number x= 7 has arisen twice, independently. It seems that perenniality and polyploidy are probably the key innovations in the diversification of O. sect. Onobrychis.

References

Abou-El-Enain, M.M. (2002) Chromosomal criteria and their phylogenetic implications in the genus Onobrychis Mill. sect. Lophobrychis (Leguminosae), with special reference to Egyptian species.Botanical Journal of the Linnean Society 139: 409–414. https://doi.org/10.1046/j.1095-8339.2002.00075.x
Akçelik,E.S., Avci, S., Uzun, S. & Sancak, C. (2012) Karyotype. Analysis of some Onobrychis (Sainfoin) species in Turkey. Archives of Biological Sciences, Belgrade 64 (2): 567–571. https://doi.org/10.2298/ABS1202567A
Amirahmadi, A., Kazempour-Osaloo, S., Khoshsokhan Mozaffar, M. & Charkhchian, M.M. (2014a) A new species of Onobrychis sect. Onobrychis (Fabaceae) from Iran. Turkish Journal of Botany 38: 658–664. https://doi.org/10.3906/bot-1309-54
Amirahmadi, A., Kazempour-Osaloo, S., Moein, F., Kaveh, A. &Maassoumi, AA. (2014b) Molecular systematic of the tribe Hedysareae(Fabaceae) based on nrDNA ITS and plastid trnL-F and matKsequences. Plant Systematics and Evolution 300: 729–747. https://doi.org/10.1007/s00606-013-0916-5
Amirahmadi, A., Kazempour-Osaloo, S., Kaveh, A. & Maassoumi, A.A. (2016) The phylogeny and new classification of the genus Onobrychis(Fabaceae-Hedysareae): evidence from molecular data.Plant Systematics and Evolution 302: 1445–1456. https://doi.org/10.1007/s0060 6-016-1343-1
Amirahmadi, A.&Khoshsokhan-Mozaffar, M. (2021) Molecular and morphological evidence of Onobrychisavanakensis, a new species from Iran. Phytotaxa 487 (1): 75–82. https://doi.org/10.11646/phytotaxa.487.1.6
Arnott, G.A.W. (1836) Pugillus Plantarum Indiae Orientalis. nova Acta Physico-medica Academiae CaesareaeLeopoldino-Carolinae naturae Curiosorum Exhibentia Ephemerides sive Observationes Historias et Experimenta 18 (1): 321–356.
Astanova, S.B. &Abdusaljamova, L.N. (1981) Chisla khromosom nekotorych vidov rodov Oxytropis DC., Onobrychis Mill. (semejstvo Leguminosae Juss.) flory Tadzhikistana. Izvestiia Akademii Nauk Tadzhikskoi SSR: Otdelenie Biologicheskikh Nauk 4 (85): 38–41.
Avci, S., Ilhan, E., Erayman, M. &Sancak, C. (2014) Analysis of Onobrychis genetic diversity using SSR marker from related legume species. Journal of Animal and Plant Sciences 24: 556–566.
Avci, S., Tekin, N., Sancak, C., Özcan, S. &Marangi, A.O. (2016) Phylogenetic relationship of some Onobrychis taxa naturally grown in Turkey based on morphology and nuclear ribosomal DNA.Legume Research 39: 665–673. https://doi.org/10.18805/lr.v0iOF.11184
Avci, S., Tuna, M. & Kaya, M.D. (2019) Autotetraploid plant production in endemic Onobrychis elata with colchicine treatments. Journal of Applied Botany and Food Quality 92: 88–93.
Ball, P.W. (1968)Onobrychis(Leguminosae). In: Tutin, T.G., Heywood, V.H., Burges, N.A., Moore, D.M., Valentine, D.H., Walters, S.M. & Webb, D.A. (Eds.)Flora EuropaeaVol. 2. Cambridge, UK: Cambridge University Press, pp. 187–191.
Baltisberger, M. (1991) IOPB chromosome data 3. IOPB Newsletter 17: 5–7.
Basiner, T. (1845) Enumeratio monographica specierum generis Hedysari. Bulletin de la Classe Physico-Mathématique de l’AcadémieImpériale des Sciences de Saint-Pétersbourg 4: 305–315.
Besser, V.S. (1822) Enumeratio Plantarum per Volhyniam et Podoliam, HuscusqueObservatarum, Pars Prima ContinensPlantasClassium XIII. PriorumSystematisSexualis. Vilnae. pp. 1–111.
Boissier, E. (1843) Leguminosae. In: Diagnoses Plantarum Orientalium Novarum. Vol. 2. Genevae Typographia Ferd. Ramboz. pp. 6–107.
Boissier, E. (1872) Flora Orientalis:sive, Enumeratio plantarum in Oriente a Graecia et Aegypto ad Indiae fines hucusque observatarum, vol.2. Genevae & Basilease pp. 1–1159.
Boissier, E. (1856) Diagnoses plantarum Orientalium. ser. 2, vol. 2. B. Hermann, Lipsiae [Leipzig].
Candolle, A.P. de (1825) Prodromus Systematis Naturalis Regni Vegetabilis 2. Paris, 281 pp.
Choi, BH. & Ohashi, H. (2003) Generic criteria and an infrageneric system for Hedysarum and related genera (Papilinoideae— Leguminosae). Taxon 52: 567–576. https://doi.org/10.2307/3647455
Desvaux, N.A. (1814) Memoire et Observations sur la Famille des PlantesLegumineuses. Journal de Botanique, Appliquée à l’Agriculture, à la Pharmacie, à la Médecine et aux Arts, Paris 3 (1–2): 65–84. 
Doyle, J.J. & Doyle, J.L. (1987) A rapid DNA isolation of fresh leaf tissue. Phytochemical bulletin 19: 11–15.
Duan, L.J., Wen, J.N., Yang, X., Liu, P.L., Arslan, E., Ertuðrul, K. & Chang, Z.Y. (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. https://doi.org/10.12705/641.26
d’Urville, J.S.C.D. (1822) Mémoires de la Société Linnéenne de Paris. Vol. 1. Pzris, pp. 1–741.
Falistocco, E. (1991) Chromosome study and genome relationships in perennial species of Onobrychis. Genetics and Breeding 45: 25–31.
Favarger, C. (1997) Notes de caryologiealpienneVI. Bulletin de la Société Neuchâteloise des Sciences Naturelles 120: 19–33.
Fedchenko, B.A. (1905) Flora of Western Tien-Shan: XXXI. Leguminosae.Trudy Imperatorskago S.-Peterburgskago Botaničeskago Sada. 24: 155– 260.
Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 38: 783–791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x
Fischer, F.E.L. von (1812) Catalogue du Jardin des Plants de S. E. Monsieur le Comte Alexis Razoumoffsky a Gorenkipres de Moscou, ed. 2. pp. 1–116.
Freyn, J.F. (1890) Plantae novae Orientales. Oesterreichische Botanische Zeitschrift. 40: 441–447. https://doi.org/10.1007/BF01790573
Freyn, J.F. (1892) Plantae novae Orientales II. Oesterreichische Botanische Zeitschrift 42: 80–84. https://doi.org/10.1007/BF01790941
Garnatje, T.& Cardona, A. (1988) Fitodermologia I cariologia d’ Onobrychis viciifolia Scop., O. supina (Chaix) DC.i O. saxatilis Lam. De Catalunya. Orsis 3: 55–65.
Ghanavati., F. &Nematpajooh, N. (2012) Study of ploidy level of annual species of Onobrychis in Iran. Caryologia 65: 328–334. https://doi.org/10.1080/00087114.2012.760880
Ghanavati, F. &Amirabadizadeh, H. (2018) A new species of Onobrychis (Papilionaceae) form Iran. Iranian Journal of Botany 24 (2): 114–118.
Goldbatt, P. (1981) Index to plant chromosome numbers, 1975-1978. Monographs in Systematic Botany, V5. Saint Louis: Missouri Botanical Garden.
Gomurgen, A.N. (1996) Meiotic analysis of selected material of sainfoin and its progeny with branched and unbranched peduncles. Turkish Journal of Botany 20: 399–411. https://doi.org/10.55730/1300-008X.2613
Grossheim, A.A. (1972) Onobrychis Adans. (Leguminosae). In: Komarov, V.L., Shishkin, B.K. & Bobrov, E.G. (Eds.) Flora of the USSR, vol. 13. Israel Program for Scientific Translations, Jerusalem, pp. 244–281. [English translation]
Haddadi, A. (2008) Cytotaxonomic study on the genu Onobrychis sect. Onobrychis in Iran. MSc. thesis. Bu-Ali Sina University. 
Handel-Mazzetti, H.R.E. (1909a) Revision der balkanischen und vorderasiatischen Onobrychis Artenaus der section Eubrychis. Österreichische Botanische Zeitschrift 59: 369–378. https://doi.org/10.1007/BF01642076
Handel-Mazzetti, H.R.E. (1909b) Revision der balkanischen und vorderasiatischen Onobrychis Artenaus der section Eubrychis. Österreichische Botanische Zeitschrift 59: 424–430. https://doi.org/10.1007/BF01637499
Handel-Mazzetti, H.R.E. (1933) Anthophyta. Symbolae Sinicae 7: 1–730. https://doi.org/10.1007/978-3-662-29370-6_1
Hanelt P (ed.) (2001) Mansfeld’s Encyclopedia of Agricultural and Horticultural Crops (Except Ornamentals). Vol. 2. Springer Verlag, Germany, pp. 541–1132. https://doi.org/10.1007/978-3-540-30442-5
Hayot Carbonero, C., Carbonero, F., Smith, L.M.J. & Brown, T.A. (2012) Phylogenetic characterization of Onobrychis species with a special focus on the forage crop Onobrychis viciifolia Scop. Genetic Resources and Crop Evolution 59: 1777–1788. https://doi.org/10.1007/s10722-012-9800-3
Hedge, I.C. (1969) Materials for a flora of Turkey, XVII: Onobrychis and Hedysarum. Notes from the Royal Botanic Garden, Edinburgh 29: 33–37.
Hedge, I.C. (1970) Onobrychis. In: Davis, P.H. (Ed.) Flora of Turkey and the East Aegean Islands. Vol. 3. Edinburgh: University Press, pp. 560–589.
Hejazi, H., Mohsen, S. & Ziaei Nasab, M. (2010) Cytotaxonomy of some Onobrychis (Fabaceae) species and populations in Iran. Caryologia 63 (1): 18–31. https://doi.org/10.1080/00087114.2010.589705
İleri, O. & Avci, S. (2018) Karyological characteristics of some endemic Onobrychis taxa belonging to Onobrychis section naturally grown in Turkey. Turkish Journal of Agriculture—Food Science and Technology 6 (11): 1530–1536. https://doi.org/10.24925/turjaf.v6i11.1530-1536.1781
Jafri, S.M. (1980) Hedysareae. In: Jafri, S.M.H., Gadi, A. El (ed.) Flora of Libya. Al Faateh University, Lybia. pp. 136–145.
Karamian, R., Ranjbar, M. & Hadadi, A. (2011) Chromosome number reports in five Onobrychis species (O. sect. Onobrychis, Fabaceae) in Iran. Journal of Cell and Molecular Research 3 (2): 81–92. https://doi.org/10.22067/jcmr.v3i2.14616
Katoh, K. Rozewicki, J. & Yamada, K.D. (2019) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics 20: 1160–1166. https://doi.org/10.1093/bib/bbx108 
Kliphuis, E. (1977) In: Love, A. (ed.) IOPB chromosome number reports LVI. Taxon 26: 257–274. https://doi.org/10.24925/turjaf.v6i11.1530-1536.1781
Lamarck, J.B.P. (1779) Flore Françoise, ou Descriptions Succinctes de Toutes les Plantes qui Croissent Naturellementen France, vol. 2. Paris, pp. 1–684. https://doi.org/10.5962/bhl.title.9461
Lewis, P.O. (2001) A likelihood approach to estimating phylogeny from discrete morphological character data. Systematic Biology 50: 913–925. https://doi.org/10.1080/106351501753462876
Lewke Bandara, N., Papini, A., Mosti, S., Brown, T. & Smith, L.M.J. (2013) A phylogenetic analysis of genus Onobrychis and its relationships within the tribe Hedysareae (Fabaceae). Turkish Journal of Botany 37: 981–992. https://doi.org/10.3906/bot-1210-32
Lifante, Z.D., Luque, T. & Bárbara, C.S. (1992) Chromosome numbers of plants collected during Iter Mediterraneum II in Israel.Bocconea 3: 229–250.
Linnæus,C. (1753) Species Plantarum. Stockholm.
Lock, J.M. (2005) Tribe Hedysareae.In:Lewis, G., Schrire, B., Mackinder, B. & Lock, M. (Eds.) Legumes of the World. Royal Botanical Gardens, pp. 489–495.
López González, G. (1986) Some novelties concerning the Spanish plants of Linnaeus. II. Analesdel Jardin Botánico de Madrid 42 (2): 319–324. [in Spanish]
Mabberley, D.J. (2008)The plant-book. A portable dictionary of the higher plants, 3rd edn. Cambridge University Press, Cambridge.
Maddison, W.P. & Maddison, D.R. (2011) Mesquite: a modular system for evolutionary analysis. Version 2.75. Available from: http://mesquiteproject.org (accessed 19 April 2023)
Medikus, F.K. (1787) Versuch einer neuen Lehrart, die Pflanzen nach zwei mtethoden zugleich, nehmlich nach der kunstlichen und naturlichen, zu ordnen, durch ein Beispiel einer naturlichen Familie erdrtert. Vorlesungen der Churpfälzischen physicalisch-ökonomischen Gesellschaft. Vol. 2. Heidelberg. pp. 327–460.
Magulaev, A.J. (1989) Cytotaxonomic study of the Northern Caucasica Onobrychis. In: Tesizy II Symposium Plant Karyology. pp. 73–76. [in Russian]
Miller, P. (1754) The Gardeners Dictionary. Abridged. ed. 4, vol. 2. [The volume has no page numbers]. John & James Rivington, London. https://doi.org/10.5962/bhl.title.79061
Miller, M.A., Pfeiffer, W. & Schwartz, T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE). 14 November 2010. New Orleans, LA, pp. 1–8. https://doi.org/10.1109/GCE.2010.5676129
Montmollin, B. (1984) Cytotaxonomic study of the flora of Crete II, Chromosomes Numbers. Botanica Helvetica 94: 261–267. [in French]
Nafisi, H., Kazempour‑Osaloo, S., Mozaffarian, V. &Schneeweiss, G.M. (2019) Molecular phylogeny and divergence times of the genus Hedysarum (Fabaceae) with special reference to section Multicaulia in Southwest Asia. Plant Systematics and Evolution 305: 1001–1017. https://doi.org/10.1007/s00606-019-01620-3
Nylander, J.A.A. (2004) Mr Modeltest v2. Program distributed by the author. Evolutionary Biology Center, Uppsala University, Uppsala.
Nylander, J.A.A., Wilgenbusch, J.C., Warren, D.L. & Swofford, D.L. (2008) AWTY (are we there yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics 24: 581–583. https://doi.org/10.1093/bioinformatics/btm388
Page, D.M. (2001) Treeview (Win32) version 1.6.6. [Available at: http://taxonomy.zoology.gla.ac.uk/rod/treeview.html]
Posada, D. & Buckley, T.R. (2004) Model selection and model averaging in phylogenetics: advantages of akaike information criterion and Bayesian approaches over likelihood ratio tests. Systematic Biology 53: 793–808. https://doi.org/10.1080/10635150490522304
POWO (2023) Plants of the World Online. Facilitated by the Royal Botanic Gardens, Kew. Published on the Internet: http://www.plantsoftheworldonline.org/ (Retrieved 20 January 2023).
Rambaut, A. & Drummond, AJ. (2007) Tracer, version 1.4. Computer program and documentation distributed by the author. [http://tree.bio.ed.ac.uk/software/tracer/]
Ranjbar, M., Karamian, R., Tolui, Z. &Amirabadizadeh, H. (2007) Onobrychis assadii (Fabaceae), a new species from Iran. Annales Botanici Fennici 44: 481–484.
Ranjbar M, Karamian R & Hadadi, A. (2010) Cytosystematics of three Onobrychis species (Fabaceae) in Iran. Caryologia 63 (3): 237–249.
Ranjbar, M., Hadadi, A. & Karamian, R. (2011) Systematic study of Onobrychis shahpurensis (Fabaceae) in Iran, with the description of O. neychalanensis sp. nov. Nordic Journal of Botany 29: 163–174. https://doi.org/10.1111/j.1756-1051.2011.01099.x
Ranjbar, M., Karamian, R., Hadadi, A. &Johartchi, M.R. (2012) Taxonomic notes on Onobrychis sect. Onobrychis subsect.Macropterae (Fabaceae) from Iran. Phytotaxa 39: 51–60. https://doi.org/10.11646/phytotaxa.39.1.5
Rechinger, K.H. (1940) Plantae novae iranicae. I. Repertorium Novarum Specierum Regni Vegetabilis 48 (S1): 33–48. https://doi.org/10.1002/fedr.4870482102
Rechinger, K.H. (1984) Onobrychis. In: Rechinger, K.H. (ed.) Flora Iranica 157. Akademische Druck- und Verlags-Anstalt, Graz & Wien, pp. 389–459.
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Hohna, S., Larget, B., Liu, L., Suchard, M.A. &Huelsenbeck, J.P. (2012) MrBayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61: 539–542. https://doi.org/10.1093/sysbio/sys029
Safaei-Chaeikar, S., Ghanavati, F., Naghavi, M.R., Amirabadi-Zadeh, H. &Rabiee, R. (2014) Molecular phylogenetics of the Onobrychis genus (Fabaceae: Papilionoideae) using ITS and trnL–trnF DNA sequence data. Australian Journal of Botany 62 (3): 235–250. https://doi.org/10.1071/BT13279
Sang, T., Crawford, D.J. & Stuessy, T.F. (1995) Documentation of reticulate evolution in peonies (Paeonia) using internal transcribed spacer sequences of nuclear ribosomal DNA: implications for biogeography and concerted evolution. Proceedings of the National Academy of Sciences of the United States of America 92: 6813–6817. https://doi.org/10.1073/pnas.92.15.6813
Schrenk, H. (1841) Euumeratio generum, specierum et varietatum novarum, in Songaria, Praeprimis in itinere versus lacus Balchasch et Alakul, nec non in altis montibusa latauatque Tarbagatai collectarum. In: Fischer, F.E.L. & Meyer, C.A. (eds.) Enumatio Plantarum Novarum, vol. 1. Petropoli, pp. 1–113.
Scopoli, J.A. (1772) Flora Carniolica, Exhibens Plantas Carniolae Indigenas et Distributas. Tomus II: 1–496. Editio Secunda Aucta et Reformata, Viennae.
Sepet, S., Emre, I., Kiran, Y., Kursat, M. &Sahin, A. (2011) Karyological studies on eight species of Onobrychis genus in Turkey. Biologia 66: 996–1002. https://doi.org/10.2478/s11756-011-0112-4
Shaw, J., Lickey, E.B., Beck, J.T., Farmer, S.B., Liu, W., Miller, J., Siripun, K.C., Winder, C.T., Schilling, E.E. & Small, R.L. (2005) Thetortoise and the hare II: relative utility of 21 noncoding chloroplastDNA sequences for phylogenetic analysis. American Journal of Botany 92: 142–166. https://doi.org/10.3732/ajb.92.1.142
Shaw, J., Lickey, E.B., Schilling, E.E. & Small, R.L. (2007) Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in Angiosperms: the tortoise and the hare III. American Journal of Botany 94: 275–288. https://doi.org/10.3732/ajb.94.3.275
Širjaev, G. (1925) Onobrychis generis revisio criteria. Publications of the Faculty of Science, University of Masaryk 56: 96–97.
Širjaev, G. (1926) Onobrychis generis revisio critica. Pars prima. Publications Faculte des Sciences de l’ Universite´ Masaryk 76: 1–165
Swofford, D.L. (2002) PAUP*, Phylogenetic analysis using parsimony (*and other methods). Version 4. Sunderland Massachusetts Sinauer Associates. https://doi.org/10.1111/j.0014-3820.2002.tb00191.x
Townsend, C.C. (1974) Onobrychis. In: Townsend, C.C. & Guest, E. (eds.) Flora of Iraq, Vol. 3. Published by the Ministry of Agriculture of the Republic of Iraq, Baghdad, pp. 471–493.
Trifinopoulos, J., Nguyen, L., Haeseler, A. & Quang Minh, B. (2016) W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis.Nucleic Acids Research 44: 232–235. https://doi.org/10.1093/nar/gkw256
White, T.J., Bruns, T., Lee, S. & Taylor, J. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis, M.A., Gelfand, D.H., Sninsky, J.J. & White, T.J. (Eds.) PCR Protocols: a guide to methods and applications.Academic Press Inc., New York, pp. 315–322. https://doi.org/10.1016/B978-0-12-372180-8.50042-1
Zarrabian, M. & Majidi, M.M. (2015) Genetic diversity and relationships within and among Onobrychis species using molecular markers.Turkish Journal of Botany 39: 681–692. https://doi.org/10.3906/bot-1406-47