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The evolution of Dianthus polylepis complex (Caryophyllaceae) inferred from morphological and nuclear DNA sequence data: one or two species?

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Abstract

Dianthus polylepis complex consists of two already known endemic species, Dianthus polylepis and D. binaludensis, in Khorassan-Kopetdagh floristic province. The taxonomic position of these species has long been debated. The aim of the present study is to shed light on the evolutionary relationships of the members of the complex using morphological and molecular data. In morphological study, firstly, 56 vegetative and floral characters were measured on 33 specimens of the both species. Multivariate analyses were performed on 25 (out of 56) significantly discriminating morphological traits. In molecular study, we sequenced alleles obtained from a region between 2nd and 6th exons of the gene coding for the enzyme dihydroflavonol 4-reductase copy1 (DFR1). Morphological results show that most of a priori identified accessions were not grouped in a posteriori classification. It is difficult to discriminate D. polylepis from D. binaludensis in morphological continuum among the accessions. Results obtained from the molecular data indicated no monophyly for the members of the D. polylepis complex. Consistency between the morphological and molecular results shows that D. polylepis and D. binaludensis were not morphologically and molecularly well differentiated. Therefore, we propose a new combination as D. polylepis subsp. binaludensis.

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References

  • Akhani H (1998) Plant biodiversity of Golestan National Park. Stapfia 53:1–411

    Google Scholar 

  • Al-Saghir MG (2010) Perspective on Chromosome Numbers in the Genus Pistacia L. (Anacardiaceae). Int J Plant Breed Genet 4:153–157

    Article  Google Scholar 

  • Assadi M (1985) The genus Dianthus L. (Caryophyllaceae) in Iran. Iran J Bot 3:9–54

    Google Scholar 

  • Balao F, Casimiro-Soriguer R, Talavera M, Herrera J, Talavera S (2009) Distribution and diversity of cytotypes in Dianthus broteri as evidenced by genome size variations. Ann Bot 104:965–973

    Article  PubMed  Google Scholar 

  • Balao F, Valente LM, Vargas P, Herrera J, Talavera S (2010) Radiative evolution of polyploid races of the Iberian carnation Dianthus broteri (Caryophyllaceae). New Phytol 187:542–551

    Article  PubMed  CAS  Google Scholar 

  • Baldwin BG, Sanderson MJ, Porter JM, Wojciechowski MF, Campbell CS, Donoghue MJ (1995) The ITS region of nuclear ribosomal DNA: a valuable source of evidence on angiosperm phylogeny. Ann Missouri Bot Gard 82:247–277

    Article  Google Scholar 

  • Baldwin BG, Cawford DJ, Francisco-Ortega J, Kim S, Sang T, Stuessy T (1998) Molecular phylogenetic insights into the origin and evolution of island plants. In: Soltis DE, Soltis PS, Doyle JJ (eds) Molecular systematics of plants II. Kluwer, Boston, pp 410–441

    Chapter  Google Scholar 

  • Bijlsma R, Van der Velde M, Van de Zande L, Boerema AC, Van Zanten BO (2000) Molecular markers reveal cryptic species within Polytrichum commune (common hair-cap moss). Plant Biol 2:408–414

    Article  CAS  Google Scholar 

  • Bittkau C, Comes HP (2009) Molecular inference of a Late Pleistocene diversification shift in Nigella s. lat. (Ranunculaceae) resulting from increased speciation in the Aegean archipelago. J Biogeogr 36:1346–1360

    Article  Google Scholar 

  • Bloch D, Werdenberg N, Erhardt A (2006) Pollination crisis in the butterfly-pollinated wild carnation Dianthus carthusianorum? New Phytol 169:699–706

    Article  PubMed  Google Scholar 

  • Bryant D, Moulton V (2002). NeighborNet: an agglomerative method for the construction of planar phylogenetic networks. Algorithms in bioinformatics. In: Guigo R, Gusfield D (eds) Second international workshop, WABI, Rome, Italy. Lecture Notes in Computer Science, vol 2452, pp 375–391

  • Bryant D, Moulton V (2004) Neighbour-Net: an agglomerative method for the construction of phylogenetic networks. Mol Biol Evol 21:255–265

    Article  PubMed  CAS  Google Scholar 

  • Collin CL, Shykoff JA (2003) Outcrossing rates in the Gynomonoecious-Gynodioecious species Dianthus sylvestris (Caryophyllaceae). Amer J Bot 90:579–585

    Article  Google Scholar 

  • Crespi AL, Bernardos S, Paiva J, Amich F, Fernandes CP, Castro A (2004) An approach to phenotypic analysis and environmental variability. The examples of the genera Dianthus L. and Lotus L. in the north of Portugal. Acta Bot Croat 63:35–48

    Google Scholar 

  • Dellaporta SL, Wood J, Hicks JB (1983) A plant DNA minipreparation: version 2. Plant Mol Biol Rep 1:19–21

    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 

  • Duarte JM, Wall PK, Edger PP, Landherr LL, Ma H, Pires JC, Leebens-Mack J, dePamphilis CW (2010) Identification of shared single copy nuclear genes in Arabidopsis, Populus, Vitis and Oryza and their phylogenetic utility across various taxonomic levels. BMC Evol Biol 10:61

    Article  PubMed  Google Scholar 

  • Erhardt A (1990) Pollination of Dianthus gratianopolitanus Vill. Plant Syst Evol 170:125–132

    Article  Google Scholar 

  • Erhardt A (1991) Pollination of Dianthus superbus L. Flora 185:99–106

    Google Scholar 

  • Fan C, Purugganan MD, Thomas DT, Wiegmann BM, Xiang QY (2004) Heterogeneous evolution of the Myc-like anthocyanin regulatory gene and its phylogenetic utility in Cornus L. (Cornaceae). Mol Phylog Evol 33:580–594

    Article  CAS  Google Scholar 

  • Fazekas AJ, Kesanakurti PR, Burgess KS, Percy DM, Graham SW, Barrett SCH, Newmaster SG, Hajibabaei M, Husband BC (2009) Are plant species inherently harder to discriminate than animal species using DNA barcoding markers? Mol Ecol Resour 9:130–139

    Article  PubMed  CAS  Google Scholar 

  • Friedman H, Hagiladi A, Resnick N, Barak A, Umiel N (2001) Ethylene-insensitive related phenotypes exist naturally in a genetically variable population of Dianthus barbatus. Theor Appl Genet 103:282–287

    Article  CAS  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) Mrbayes: Bayesian inference of phylogeny. Bioinformatics 17:754–755

    Article  PubMed  CAS  Google Scholar 

  • Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267

    Article  PubMed  CAS  Google Scholar 

  • Inagaki Y, Johzuka-Hisatomi Y, Mori T, Takahashi S, Hayakawa Y, Peyachoknagul S, Ozeki Y, Iida S (1999) Genomic organization of the genes encoding dihydroflavonol 4-reductase for flower pigmentation in the Japanese and common morning glories. Gene 226:181–188

    Article  PubMed  CAS  Google Scholar 

  • Jafari A, Behroozian M (2010) A cytotaxonomic study on Dianthus L. species in north eastern Iran. Asian J Plant Sci 9:58–62

    Article  Google Scholar 

  • Janssens BS, Geuten K, Viaene T, Yuan YM, Song Y, Smets E (2007) Phylogenetic utility of the AP3/DEF K-domain and its molecular evolution in Impatiens (Balsaminaceae). Mol Phylog Evol 43:225–239

    Article  CAS  Google Scholar 

  • Joly S, Starr JR, Lewis WH, Bruneau A (2006) Polyploid and hybrid evolution in roses east of the Rocky Mountains. Am J Bot 93:412–425

    Article  PubMed  Google Scholar 

  • Jullien N (2008). Amplifx. A tool for seeking and designing new primers. Ver. 1.5.4. http://www.softpedia.com/get/Others/Home-Education/AmplifX.shtml

  • Kadereit J, Griebeler E, Comes H (2004) Quaternary diversification in European alpine plants: pattern and process. Proc R Soc Lond B 359:265–274

    Google Scholar 

  • Legendre P, Legendre L (1998) Numerical ecology. Elsevier Press, Amsterdam

    Google Scholar 

  • Linder H (2008) Plant species radiations: where, when, why? Proc R Soc B 363:3097–3105

    Google Scholar 

  • Linder HP, Dlamini T, Henning J, Verboom GA (2006) The evolutionary history of Melianthus (Melianthaceae). Amer J Bot 93:1052–1064

    Article  Google Scholar 

  • Lu Z, Cai YM, Qiang Z, Yu ZH, Ren HM (2002) Sequence of the ITS region of nuclear ribosomal DNA (nrDNA) in Xinjiang wild Dianthus and its phylogenetic relationship [J]. Acta Genet Sinica 29:549–554

    Google Scholar 

  • Mandakova T, Munzbergova Z (2006) Distribution and ecology of cytotypes of the Aster amellus aggregates in the Czech Republic. Ann Bot 98:845–856

    Article  PubMed  Google Scholar 

  • Martens S, Knott J, Seitz CA, Janvari L, Yu SN (2003) Impact of biochemical pre-studies on specific metabolic engineering strategies of flavonoid biosynthesis in plant tissues. Biochem Eng J 14:227–235

    Article  CAS  Google Scholar 

  • Müler K (2005) SeqState: primer design and sequence statistics for phylogenetic DNA data sets. Appl Bioinformatics 4:65–69

    Article  Google Scholar 

  • Naumann J, Symmank L, Samain MS, Müller KF, Neinhuis C, dePamphilis CW, Wanke S (2011) Chasing the hare—evaluating the phylogenetic utility of a nuclear single copy gene region at and below species level within the species rich group Peperomia (Piperaceae). BMC Evol Biol 11:357

    Article  PubMed  CAS  Google Scholar 

  • Nlander JAA (2004). MrModeltest v2. Program distributed by the author, Evolutionary Biology Centre, Uppsala University. http://www.abc.se/~nylander/

  • Nowrouzi G, Priestley KF, Ghafory-Ashtiany M, Javan Doloei G, Rham DJ (2007) Crustal velocity structure in Iranian Kopeh-Dagh, from analysis of P-waveform receiver functions. J Sustain Energy Environ 8:187–194

    Google Scholar 

  • Olsen KO, Schaal BA (1999) Evidence on the origin of cassava: phylogeography of Manihot esculenta. Proc Natl Acad Sci USA 96:5586–5591

    Article  PubMed  CAS  Google Scholar 

  • Otieno DF, Balkwill K, Paton AJ (2006) A multivariate analysis of morphological variation in the Hemizygia bracteosa complex (Lamiaceae, Ocimeae). Plant Syst Evol 26:19–38

    Article  Google Scholar 

  • Otto SP (2007) The evolutionary consequences of polyploidy. Cell 131:452–462

    Article  PubMed  CAS  Google Scholar 

  • Owen E, Semple JC, Baum BR (2006) A multivariate morphometric analysis of the Symphyotrichum boreale—S. nahanniense—S. welshii complex (Asteraceae: Astereae). Canad J Bot 84:1282–1297

    Article  Google Scholar 

  • Oxelman B, Liden M, Berglund D (1997) Chloroplast rps16 intron phylogeny of the tribe Sileneae (Caryophyllaceae). Plant Syst Evol 206:393–410

    Article  Google Scholar 

  • Page DM (2001) TreeView (Win32) Version 1.6.6. http://taxonomy.zoology.gla.ac.uk/rod/rod.html

  • Page DM, Charleston MA (1997) From gene to organismal phylogeny: reconciled trees and the gene tree/species tree problem. Mol Phyl Evol 7:231–240

    Article  CAS  Google Scholar 

  • Paun O, Forest F, Fay MF, Chase MW (2009) Hybrid speciation in angiosperms: parental divergence drives ploidy. New Phytol 182:507–518

    Article  PubMed  Google Scholar 

  • Pillon Y, Fay MF, Hedrén M, Batean RM, Devey DS, Shipunov AB, Bank MVD, Chase MW (2007) Evolution and temporal diversification of western European polyploid species complexes in Dactylorhiza (Orchidaceae). Taxon 56:1185–1208

    Article  Google Scholar 

  • Posada D (2004) Collapse: describing haplotypes from sequence alignments, Ver.1.2. http://darwin.uvigo.es/software/collapse.htm

  • Rambaut A, Drummond AJ (2003) Tracer v 1.3. http://evolve.zoo.ox.ac.uk

  • Ramsey J, Schemske DW (1998) Pathways, mechanisms, and rates of polyploidy formation in flowering plants. Annu Rev Ecol Syst 29:467–501

    Article  Google Scholar 

  • Rechinger KH (1983) Acht neue Arten der Gattung Dianthus (Caryophyllaceae) aus dem Gebiet der Flora Iranica. Plant Syst Evol 142:239–246

    Article  Google Scholar 

  • Rechinger KH (1988) Flora Iranica, No. 163. Caryophyllaceae II. Akademische Druck– u. Verlagsanstalt, Graz

  • Rieseberg LH, Ellstrand NC (1993) What can morphological and molecular markers tell us about plant hybridization? Crit Rev Plant Sci 12:213–241

    CAS  Google Scholar 

  • Rieseberg LH, Wood TE, Baack EJ (2006) The nature of plant species. Nature 440:524–527

    Article  PubMed  CAS  Google Scholar 

  • Sang T (2002) Utility of low-copy nuclear gene sequences in plant phylogenetics. Crit Rev Biochem Mol Biol 37:121–147

    Article  PubMed  CAS  Google Scholar 

  • Seppä P, Helanterä H, Trontti K, Punttila P, Chernenko A, Martin SJ, Sundström L (2011) The many ways to delimit species: hairs, genes and surface chemistry. Myrmecol News 15:31–41

    Google Scholar 

  • Shaw AJ, Gutkin MS, Bernstein BR (1994) Systematics of the tree mosses (Climacium, Musci); genetic and morphological evidence. Syst Bot 19:263–272

    Article  Google Scholar 

  • Sheikholeslami MR, Kouhpeyma M (2012) Structural analysis and tectonic evolution of the eastern Binalud Mountains, NE Iran. J Geodyn 61:23–46

    Article  Google Scholar 

  • Simmons MP, Ochoterena H (2000) Gaps as characters in sequence-based phylogenetic analyses. Syst Biol 49:369–381

    Article  PubMed  CAS  Google Scholar 

  • Small RL, Cronn RC, Wendel JF (2004) Use of nuclear genes for phylogeny reconstruction in plants. Aust Syst Bot 17:145–170

    Article  CAS  Google Scholar 

  • Soltis PS, Soltis DE (2009) The role of hybridization in plant speciation. Annu Rev Plant Biol 60:561–588

    Article  PubMed  CAS  Google Scholar 

  • Sultan SE (1987) Evolutionary implications of phenotypic plasticity in plants. Evol Biol 21:127–178

    Article  Google Scholar 

  • Swofford DL (2002). PAUP*: phylogenetic analysis using parsimony (*and other methods), version 4.0b10. Sinauer Press, Sunderland, MA

  • Syring J, Willyard A, Cronn R, Liston A (2005) Evolutionary relationships among Pinus (Pinaceae) subsections inferred from multiple low-copy nuclear loci. Amer J Bot 92:2086–2100

    Article  Google Scholar 

  • Ter Braak CJF, Smilauer P (2002) CANOCO Reference manual and user’s guide to Canoco for Windows: Software for Canonical Community Ordination (version 4). Microcomputer Power, Ithaca

    Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) ClustalW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  • Tu T, Dillon MO, Sun H, Wen J (2008) Phylogeny of Nolana (Solanaceae) of the Atacama and Peruvian deserts inferred from sequences of four plastid markers and the nuclear LEAFY second intron. Mol Phylog Evol 49:561–573

    Article  CAS  Google Scholar 

  • Valente LM, Savolainen V, Vargas P (2010) Unparalleled rates of species diversification in Europe. Proc R Soc B 277:1489–1497

    Article  PubMed  Google Scholar 

  • Volkov RA, Komarova NY, Hemleben V (2007) Ribosomal DNA in plant hybrids: inheritance, rearrangement, expression. Syst Biodiv 5:261–276

    Article  Google Scholar 

  • West-Eberhard MJ (1989) Phenotypic plasticity and the origins of diversity. Ann Rev Ecol Syst 20:249–278

    Article  Google Scholar 

  • Whittall JB, Medina-Marino A, Zimmer EA, Hodges SA (2006) Generating single copy nuclear gene data for a recent adaptive radiation. Mol Phylog Evol 39:124–134

    Article  CAS  Google Scholar 

  • Wood TE, Takebayashi N, Barker MS, Mayrose I, Greenspoon PB, Rieseberg LH (2009) The frequency of polyploid speciation in vascular plants. Proc Natl Acad Sci USA 106:13875–13879

    Article  PubMed  CAS  Google Scholar 

  • Xie DY, Jackson LA, Cooper JD, Ferreira D, Paiva NL (2004) Molecular and biochemical analysis of two cDNA clones encoding dihydroflavonol 4-reductase from Medicago truncatula. Plant Physiol 134:979–994

    Article  PubMed  CAS  Google Scholar 

  • Yan HF, Hao G, Hu CM, Ge XJ (2011) DNA barcoding in closely related species: A case study of Primula L. sect. Proliferae Pax (Primulaceae) in China. J Syst Evol 49:225–236

    Article  Google Scholar 

  • Zmasek CM, Eddy SR (2001) ATV: display and manipulation of annotated phylogenetic trees. Bioinformatics 17:383–384

    Article  PubMed  CAS  Google Scholar 

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The authors wish to thank vice president for Research and Technology of Ferdowsi University of Mashhad for financial support.

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Farsi, M., Behroozian, M., Vaezi, J. et al. The evolution of Dianthus polylepis complex (Caryophyllaceae) inferred from morphological and nuclear DNA sequence data: one or two species?. Plant Syst Evol 299, 1419–1431 (2013). https://doi.org/10.1007/s00606-013-0804-z

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