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Species/geographic boundaries and evolutionary interrelationships of cultivated linden-trees (Tilia L.) based on morphological and nrDNA ITS characteristics

Melosik I, Ciupińska M., Winnicka K., Koukoulas G.

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J. Bio. Env. Sci.5(5), 90-118, November 2014


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Nuclear ribosomal transcribed spacers (ITS1-5.8S rRNA-ITS2) is a popular marker that has superior taxa resolution in some groups of organisms. A taxonomic reassessment of 27 Tilia taxa combining a molecular marker (ITS1-5.8S rRNA-ITS2) and morphological characters (40 characteristics of 1,307 leaves and 1,146 fruits) was performed to: (1) evaluate nrDNA ITS as a potential barcode for Tilia species-level identification, (2) detect geographic differentiation pattern of Tilia trees originated from Europe, Asia, and North America and cultivated in common garden conditions, (3) compare Tilia hybrids and their putative parental species. We demonstrate that: (1) intra-individual and intra- morphospecies site polymorphism (2ISP) in ITS sequences occurs; (2) ITS variants in vegetatively propagated hybrids differ from variants in putative parental species; (3) geographical patterns of genetic and morphological differentiation were detected; (4) the majority of hybrids clustered around one of the parental species. The resulting poorly resolved relationship in the phylogenetic analyses (Maximum Parsimony and Maximum Likelihood) can be explained in terms of data quality (low number of parsimony informative sites, high level of homoplasy), the influence of hybridization on the phylogeny, or other issues. The ITS spacers should be excluded as a potential single barcode due to the existence of 2ISPs. We concluded that our ITS survey is not exhaustive because ITS variants in vegetatively propagated hybrids differ from variants in their parental species. A dichotomous key based mainly on qualitative morphological traits is constructed for the cultivated Tilia taxa.


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Species/geographic boundaries and evolutionary interrelationships of cultivated linden-trees (Tilia L.) based on morphological and nrDNA ITS characteristics

Álvarez I, Wendel JF. 2003. Ribosomal ITS sequences and plant phylogenetic inference. Molecular Phylogenetics and Evolution 29, 417-434.

Amheim N, Kristal M, Schmickel R, Wilson G, Ryder O, Zimmer E. 1980. Molecular evidence for genetic exchanges among ribosomal genes on nonhomologous chromosomes in man and apes. Proceedings of the National Academy of Sciences USA 77, 7323-7327.

Banerjee UC. 1976. Trichomes: their application in taxonomy of American species of lindens (Tilia spp.) A scanning electron microscopic study. Scanning electron microscopy. Pt. 7.

Baldwin BG, Sanderson MJ, Porter JM, Wojciechowski MF, Campbell CS, et al. 1995. The ITS region of nuclear ribosomal DNA: a valuable source of evidence on angiosperm phylogeny. Annals of the Missouri Botanical Garden 82, 247-277.

Białobok S. 1991. Lipy: nasze drzewa Leśne (15). Polska Akademia Nauk, Poznań (in Polish).

Boratyńska K, Dolatowski J. 1991. Systematyka i geograficzne rozmieszczenie. In: Białobok S (ed) Lipy – Tilia cordata Mill, Tilia platyphyllos Scop. Nasze drzewa leśne. Polish Academy of Sciences, Institute of Dendrology, Poznań, pp. 54-83 (in Polish).

Borowski J, Solecka M. 1980. Chemotaksonomia wybranych gatunków w rodzaju Tilia. Rocznik Sekcji Dendrologicznej PTB 33, 29-36.

Bryant D, Moulton V. 2004. Neighbor-Net: An agglomerative method for the construction of phylogenetic networks. Molecular Biology and Evolution 21, 255-265.

Buckler IV ES, Ippolito A, Holtsford TP. 1997. The evolution of Ribosomal DNA: Divergent Paralogues and Phylogenetic implications. Genetics 145, 821-832.

Chen S, Kim D-K, Chase MW, Kim J-H. 2013. Networks In a Large-scale Phylogenetic Analysis: Reconstructing Evolutionary History of Asparagales (lilianae) Based on Four Plastid Genes. PLoS One 8, 3, e59472, doi: 10.1371/journal.pone 0059472.

China Plant BOL Group. 2011. Comparative analysis of a large dataset indicates that internal transcribed spacer (ITS) should be incorporated into the core barcode for seed plants. Proceedings of the National Academy of Sciences USA 108, 19641-19646. doi: 10.1073/pnas.1104551108.

Chŷtry M, Sădlo J. 1997. Tilia-dominated calcicolous forests in the Czech Republic from a Central European perspective. Annali di Botanica 55, 105-118.

Darriba D, Taboada GL, Doallo R, Posada D. 2012. “jModelTest2: more models, new heuristics and parallel computing”. Nature Methods 9, 8, 722.

Dover GA. 1982. Molecular Drive: a cohesive mode of species evolution. Nature 299, 111-116.

Doyle J, Doyle JL. 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical bulletin 19, 11-15.

Fineschi S, Salvini D, Taurchini D, Carnevale S, Vendramin GG. 2003. Chloroplast DNA variation of Tilia cordata (Tiliaceae). Canadian Journal of Forest Research 33, 2503-2508.

Fromm M, Hattemer HH. 2003. Inheritance of allozymes and hybridization in two European Tilia species. Heredity 91, 337-344.

Goloboff PA, Farris JS, Nixon KC. 2003. T.N.T.: Tree Analysis Using New Technology Program and documentation available from the authors, and at www.zmwc.dk/public/phylogeny.

Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. 2010. PhyML 3.0: new algorithms, methods and utilities. Systematic Biology 59, 3, 307-321.

Harris DJ, Crandall KA. 2000. Intragenomic variation within ITS1 and ITS2 of freshwater crayfishes (Decapoda: Cambaridae): implications for phylogenetic and microsatellite studies. Molecular Biology and Evolution 17, 284-291.

Howell DC. 2007. Statistical methods for psychology (6th ed.). Thomson Wadsworth, Belmont.

Hřibová E, Čižkovà J, Christelovà P, Taudien S, de Langhe E, Doležel J. 2011. The ITS1-5.8S-ITS2 Sequence Region in the Musaceae: Structure, Diversity and Use in Molecular Phylogeny. PLoS ONE 6, 3, e17863 doi: 10.1371/journal.pone.0017863.

Huson DH, Bryant D. 2006. Application of Phylogenetic Networks in Evolutionary Studies. Molecular Biology and Evolution 23, 2, 254-267.

King MG, Roalson EH. 2008. Exploring evolutionary dynamics of nrDNA in Carex subgenus Vignea (Cyperaceae). Systematic Botany 33, 514-524.

Koch M, Al-Shehbaz A. 2000. Molecular systematics of the Chinense Yinshania (Brassicaceae) evidence from plastid trnL intron and nuclear ITS DNA sequence data. Annals of the Missouri Botanical Garden 87, 246-272.

Koch M, Dobeš Ch, Mitchell-Olds T. 2003. Multiple Hybrid Formation in Natural Populations: Concerted Evolution of the Internal Transcribed Spacer of Nuclear Ribosomal DNA (ITS) in North American Arabis divaricarpa (Brassicaceae). Molecular Biology and Evolution 20, 3, 338-350.

Lanfear R, Calcott B, Ho SYW, Guindon S. 2012. PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29, 6, 1695-1701. doi: 10.1093/molbev/mss020.

Liesebach H, Sinkó Z. 2008. A contribution to the systematics of the genus Tilia with respect to some hybrids by RAPD analysis. Dendrobiology 59, 13-22.

Lindner DI, Banik MT. 2011. Intragenomic variation in the ITS rDNA region obscures phylogenetic relationships and inflates estimates of operational taxonomic units in genus Laetiporus. Mycologia 103, 4, 731-740. doi: 10.3852/10-331.

Morrison DA. 2010. Using Data-Display Networks for Exploratory Data Analysis in Phylogenetic Studies. Molecular Biology and Evolution 27, 1044-1057.

Nei M. 1987. Molecular evolutionary genetics. Columbia university Press, New York.

Nei M, Rooney AP. 2005. Concerted and birth-and-death evolution of multigene families. Annual Review of Genetics 39, 121-152.

Phuekvilai P, Wolff K. 2013. Characterization of microsatellite loci in Tilia platyphyllos (Malvaceae) and cross-amplification in related species. Applications in Plant Sciences 1, 4, 1200386.

Pigott CD. 1997. Tilia. In: Cullen J. et al. (eds) The European Garden Flora 5. Cambridge University Press, Cambridge, UK.

Pigott CD. 2002. A review of chromosome numbers in the genus Tilia (Tiliaceae). Edinburgh Journal of Botany 02, 239-246.

Pigott CD. 2008. The identity of limes labeled Tilia insularis. The Plantsman (new series) 7, 194-195.

Pigott CD. 2012. Lime-Trees and Basswoods. A Biological Monograph of the genus Tilia. Cambridge University Press, Cambridge, UK.

Potts A, Hedderson TA, Grimm GW. 2014. Constructing Phylogenies in the Presence of Intra-Individual Site Polymorphisms (2ISPs) with a Focus on the Nuclear Ribosomal Cistron. Systematic Biology 63, 1-16, doi:10.1093/sysbio/syt052.

Rozas J, Sanchez-Delbarrio JC, Messeguer X, Rozas R. 2003. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19, 24-96-2497.

Sani A, Reddy SK, Jawali N. 2008. Intra-individual and intra-specific heterogenity in nuclear rDNA ITS region of Vigna species from subgenus Ceratotropis. Genetics Research 90, 4, 299-316. doi: 10.1017/s001667230800983.

Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, Chen W, Fungal Barcoding Consortium. 2012. Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proceedings of the National Academy of Sciences USA. doi: 10.1073/pnas.1117018109.

Seneta  W,   Dolatowski   J. 2008. Dendrologia. Wydawnictwo Naukowe PWN, Warszawa (in Polish).

Shaw AJ, Cox C, Boles S. 2003. Polarity of peatmoss (Sphagnum) evolution: who says mosses have no roots. American Journal of Botany 90, 1777-1787.

Song J, Shi L, Li D, Sun Y, Niu Y. et al. 2012. Extensive Pyrosequencing Reveals Frequent Intra-Genomic Variations of Internal Transcribed Spacer Regions of Nuclear Ribosomal DNA. PLoS ONE 7, 8, e43971. doi: 10.1371/journal.pone.0043971.

Stamatakis A. 2006.  RAxML-VI-HPC:  maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 21, 2688-2690. doi: 10.1093/bioinformatics/btl4.

Stanisz A. 2007. Przystępny kurs statystyki z zastosowaniem STATISTICA PL na przykładach z medycyny 3: Analizy wielowymiarowe. StatSoft Polska Sp. z o. o., Kraków (in Polish).

Stern RF, Andersen RA, Jameson I, Küpper FC, Coffroth M-A, et al. 2012. Evaluating the Ribosomal Internal Transcribed Spacer (ITS) as a Candidate Dinoflagellate Barcode Marker. PLoS ONE 7(8), e42780. doi:10.1371/journal.pone.0042780.

Szymanowski T. 1970. Tilia insularis. Rocznik Sekcji Dendrologicznej Polskiego Towarzystwa Botanicznego. 24, 99-106 (in Polish).

Tabachnick BG, Fidell LS. 2007. Using multivariate statistics (5th ed.) Allyn & Bacon, Boston.

Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA 4: Molecular Evolutionary Genetic Analysis (MEGA) Software version 4.0. Molecular Biology and Evolution 24, 1596-1599.

Thornhill DJ, Lajeunesse TC, Santos SR. 2007. Measuring rDNA diversity in eukaryotic microbial systems: how intragenomic variation, pseudogenes and PCR artifacts confound biodiversity estimates. Molecular Ecology 16, 5326-5340. doi: 10.1111/j.1365-294X.2007.03576.x.

Wendel JF, Schnabel A, Seelanan T. 1995. Bidirectional interlocus concerted evolution following allopolyploid speciation in cotton (Gossypium). Proceedings of the National Academy of Sciences USA 92, 280-284.

Wicksell V, Christensen K. 1999. Hybridization among Tilia cordata and T. platyphyllos (Tiliaceae) in Denmark. Nordic Journal of Botany 19, 6, 673-684. Wissemann V. 1999. Genetic constitution of Rosa sect. Caninae (R. canina, R. jundzillii) and sect. Gallicanae (R. gallica). Angewandte Botanik 73, 191-196.

Volkov RA, Komarova NY, Hemleben V. 2007. Ribosomal DNA in plant hybrids: inheritance, rearrangement, expression. Systematics and Biodiversity 5, 261-276. doi:10.1017/s1477200007002447.

Yousefzadeh H, Colagar AH, Tabari M, Sattarian A, Assadi M. 2012. Utility of ITS region sequence and structure for molecular identification of Tilia species from Hyrcanian forests, Iran. Plant Systematics and Evolution 298, 947-961. doi: 10.1007/s00606-012-0604-x.


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