Phylogenetic analysis of Zieria (Rutaceae) in Australia and New Caledonia based on nuclear ribosomal DNA shows species polyphyly, divergent paralogues and incongruence with chloroplast DNA
Rosemary A. Barrett A , Michael J. Bayly A E , Marco F. Duretto B , Paul I. Forster C , Pauline Y. Ladiges A and David J. Cantrill DA School of BioSciences, The University of Melbourne, Vic. 3010, Australia.
B National Herbarium of New South Wales, Royal Botanic Gardens and Domain Trust, Mrs Macquaries Road, Sydney, NSW 2000, Australia.
C Queensland Herbarium, Department of Science, Information Technology & Innovation, Brisbane Botanic Gardens, Toowong, Qld 4066, Australia.
D Royal Botanic Gardens Victoria, Birdwood Avenue, South Yarra, Vic. 3141, Australia.
E Corresponding author. Email: mbayly@unimelb.edu.au
Australian Systematic Botany 31(1) 16-47 https://doi.org/10.1071/SB16034
Submitted: 23 August 2017 Accepted: 17 November 2017 Published: 28 February 2018
Abstract
This study presents a phylogeny of Zieria Sm. (Rutaceae) based on sequences of internal transcribed spacer and external transcribed spacer regions of nrDNA, and using Neobyrnesia suberosa J.A.Armstr. as the outgroup. The phylogeny includes 109 samples, representing 58 of the 60 currently recognised species of Zieria, with multiple accessions of most. Ten species were resolved as monophyletic on the basis of two, or in one case four, samples. Monophyly of four species was neither supported nor rejected, and all other species with more than one accession were resolved as polyphyletic or paraphyletic. Results showed that divergent paralogues of nrDNA are present in some individuals, although the underlying evolutionary process that gave rise to those paralogues is uncertain. Divergent paralogues within genomes could predate speciation and be variably retained or variably detected within the species sampled here; alternatively, they could represent novel nrDNA combinations formed through hybridisation after speciation. There was no strong evidence for recombination between paralogues or that paralogues represent pseudogenes. Variation of nrDNA sequences was clearly incongruent with previously published cpDNA variation, with the nrDNA potentially providing a better indication of species relationships in Zieria. Evidence for this comes from the greater level of congruence, in some species at least, between nrDNA and existing species-level taxonomy than between cpDNA and taxonomy. Incomplete lineage sorting is proposed as a plausible cause for much of the conflict between nrDNA and cpDNA in Zieria, although, in most cases, there was insufficient information to identify the underlying causes with confidence. Implications for species-level taxonomy are discussed.
Additional keywords: biogeography, chloroplast lineage sorting, hybrids, molecular phylogeny, nrDNA, taxonomy.
References
Álvarez I, Wendel JF (2003) Ribosomal ITS sequences and plant phylogenetic inference. Molecular Phylogenetics and Evolution 29, 417–434.| Ribosomal ITS sequences and plant phylogenetic inference.Crossref | GoogleScholarGoogle Scholar |
Appelhans MS, Wen J, Wagner WL (2014) A molecular phylogeny of Acronychia, Euodia, Melicope and relatives (Rutaceae) reveals polyphyletic genera and key innovations for species richness. Molecular Phylogenetics and Evolution 79, 54–68.
| A molecular phylogeny of Acronychia, Euodia, Melicope and relatives (Rutaceae) reveals polyphyletic genera and key innovations for species richness.Crossref | GoogleScholarGoogle Scholar |
Armstrong JA (1991) Studies on pollination and systematics in the Australian Rutaceae. PhD thesis, University of New South Wales, Sydney.
Armstrong JA (2002) Zieria (Rutaceae): a systematic and evolutionary study. Australian Systematic Botany 15, 277–463.
| Zieria (Rutaceae): a systematic and evolutionary study.Crossref | GoogleScholarGoogle Scholar |
Armstrong JA, Harden G (2002) Zieria. In ‘Flora of New South Wales. Vol. 2’, 2nd edn. (Ed. G Harden) pp. 277–288. (UNSW Press: Sydney, NSW, Australia)
Armstrong JA, Powell JM (1980) Neobyrnesia (Rutaceae): a new genus endemic to Northern Australia. Telopea 1, 399–408.
| Neobyrnesia (Rutaceae): a new genus endemic to Northern Australia.Crossref | GoogleScholarGoogle Scholar |
Arnheim N (1983) Concerted evolution in multigene families. In ‘Evolution of Genes and Proteins’. (Eds M Nei, R Koehn) pp. 38–61 (Sinauer Associates: Sunderland, MA, USA)
Bailey CD, Carr TG, Harris SA, Hughes CE (2003) Characterization of angiosperm nrDNA polymorphism, paralogy, and pseudogenes. Molecular Phylogenetics and Evolution 29, 435–455.
| Characterization of angiosperm nrDNA polymorphism, paralogy, and pseudogenes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXovVWntbY%3D&md5=750f83329320a467f5cb4be23c41e3a8CAS |
Baldwin BG (1992) Phylogenetic utility of the internal transcribed spacers of nuclear ribosomal DNA in plants: an example from the Compositae. Molecular Phylogenetics and Evolution 1, 3–16.
| Phylogenetic utility of the internal transcribed spacers of nuclear ribosomal DNA in plants: an example from the Compositae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXms1eksLo%3D&md5=bd34b66c04b4e023f3981038b7e25d7eCAS |
Baldwin BG, Markos S (1998) Phylogenetic utility of the external transcribed spacer (ETS) of 18S–26S rDNA: congruence of ETS and ITS trees of Calycadenia (Compositae). Molecular Phylogenetics and Evolution 10, 449–463.
| Phylogenetic utility of the external transcribed spacer (ETS) of 18S–26S rDNA: congruence of ETS and ITS trees of Calycadenia (Compositae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhtlKmtb4%3D&md5=f392482c8a3164850f1c14c134dab112CAS |
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. Annals of the Missouri Botanical Garden 82, 247–277.
| The ITS region of nuclear ribosomal DNA: a valuable source of evidence on angiosperm phylogeny.Crossref | GoogleScholarGoogle Scholar |
Barrett RA, Bayly MJ, Duretto MF, Forster PI, Ladiges PY, Cantrill DJ (2014) A chloroplast phylogeny of Zieria (Rutaceae) in Australia and New Caledonia shows widespread incongruence with species-level taxonomy. Australian Systematic Botany 27, 427–449.
| A chloroplast phylogeny of Zieria (Rutaceae) in Australia and New Caledonia shows widespread incongruence with species-level taxonomy.Crossref | GoogleScholarGoogle Scholar |
Bayly MJ, Ladiges PY (2007) Divergent paralogues of ribosomal DNA in eucalypts (Myrtaceae). Molecular Phylogenetics and Evolution 44, 346–356.
| Divergent paralogues of ribosomal DNA in eucalypts (Myrtaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmtVOltbo%3D&md5=01541ffcc7998428c4b35e144a37630dCAS |
Bayly MJ, Udovicic F, Gibbs AK, Parra-O C, Ladiges PY (2008) Ribosomal DNA pseudogenes are widespread in the eucalypt group (Myrtaceae): implications for phylogenetic analysis. Cladistics 24, 131–146.
| Ribosomal DNA pseudogenes are widespread in the eucalypt group (Myrtaceae): implications for phylogenetic analysis.Crossref | GoogleScholarGoogle Scholar |
Bayly MJ, Holmes GD, Forster PI, Cantrill DJ, Ladiges PY (2013) Major clades of Australasian Rutoideae (Rutaceae) based on rbcL and atpB sequences. PLoS One 8, e72493
| Major clades of Australasian Rutoideae (Rutaceae) based on rbcL and atpB sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlaqsbrF&md5=0211e3ab46691f2d95da275e38106b67CAS |
Bayly MJ, Duretto MF, Holmes GD, Forster PI, Cantrill DJ, Ladiges PY (2015) Transfer of the New Caledonian genus Boronella to Boronia (Rutaceae) based on analyses of cpDNA and nrDNA. Australian Systematic Botany 28, 111–123.
| Transfer of the New Caledonian genus Boronella to Boronia (Rutaceae) based on analyses of cpDNA and nrDNA.Crossref | GoogleScholarGoogle Scholar |
Bayly MJ, Holmes GD, Forster PI, Cantrill DJ, Munzinger J, Ladiges PY (2016) Phylogeny, classification and biogeography of Halfordia (Rutaceae) in Australia and New Caledonia. Plant Systematics and Evolution 302, 1457–1470.
| Phylogeny, classification and biogeography of Halfordia (Rutaceae) in Australia and New Caledonia.Crossref | GoogleScholarGoogle Scholar |
Bena G, Jubier M-F, Olivieri I, Lejeune B (1998) Ribosomal external and internal transcribed spacers: combined use in the phylogenetic analysis of Medicago (Leguminosae). Journal of Molecular Evolution 46, 299–306.
| Ribosomal external and internal transcribed spacers: combined use in the phylogenetic analysis of Medicago (Leguminosae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXht1Sksrw%3D&md5=21051e6181847ac5ea89d8b5df945618CAS |
Bentham G (1863) ‘Flora Australiensis: a Description of the Plants of the Australian Territory. Vol. 1.’ (Lovell Reeve and Co.: London, UK)
Bergsten J (2005) A review of long-branch attraction. Cladistics 21, 163–193.
| A review of long-branch attraction.Crossref | GoogleScholarGoogle Scholar |
Boni MF, Posada D, Feldman MW (2007) An exact nonparametric method for inferring mosaic structure in sequence triplets. Genetics 176, 1035–1047.
| An exact nonparametric method for inferring mosaic structure in sequence triplets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXovVOqsrw%3D&md5=d7f5803f8e24bd08b6d68b70d5142c89CAS |
Buckler ES, Ippolito A, Holtsford TP (1997) The evolution of ribosomal DNA: divergent paralogues and phylogenetic implications. Genetics 145, 821–832.
Childs G, Maxson R, Cohn RH, Kedes L (1981) Orphons: dispersed genetic elements derived from tandem repetitive genes of eucaryotes. Cell 23, 651–663.
| Orphons: dispersed genetic elements derived from tandem repetitive genes of eucaryotes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXhs12ltLY%3D&md5=de09d18f59a3739d5b13f2a658d31861CAS |
Clevinger JA, Panero JL (2000) Phylogenetic analysis of Silphium and subtribe Engelmanniinae (Asteraceae: Heliantheae) based on ITS and ETS sequence data. American Journal of Botany 87, 565–572.
| Phylogenetic analysis of Silphium and subtribe Engelmanniinae (Asteraceae: Heliantheae) based on ITS and ETS sequence data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjsVektrc%3D&md5=3b795d86b0c1267834719db308280123CAS |
Duretto MF (1999) Rutaceae. In ‘Flora of Victoria. Vol. 4’. (Eds N Walsh, T Entwisle) pp. 153–197. (Inkata Press: Melbourne, Vic., Australia)
Duretto MF (2009) 87 Rutaceae, version 2009 : 1. In ‘Flora of Tasmania Online’. (Ed. MF Duretto) (Tasmanian Herbarium, Tasmanian Museum & Art Gallery: Hobart, Tas., Australia) Available at www.tmag.tas.gov.au/floratasmania [Verified 21 December 2017]
Duretto MF, Forster PI (2007) A taxonomic revision of the genus Zieria Sm. (Rutaceae) in Queensland. Austrobaileya 7, 473–544.
Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, Mitchell SE (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One 6, e19379
| A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmtVKru7Y%3D&md5=d29a55917cb8fe6ba4d72f6e3eb4fcdcCAS |
Engler A (1931) Rutaceae. In ‘Die natürlichen Pflanzenfamilien Teil 19a’, 2nd edn. (Eds HGA Engler, K Prantl) pp. 187–359. (Wilhelm Engelmann: Leipzig, Germany)
Farris JS, Källersjö M, Kluge AG, Bult C (1994) Testing significance of incongruence. Cladistics 10, 315–319.
| Testing significance of incongruence.Crossref | GoogleScholarGoogle Scholar |
Farris JS, Källersjö M, Kluge AG, Bult C (1995) Constructing a significance test for incongruence. Systematic Biology 44, 570–572.
| Constructing a significance test for incongruence.Crossref | GoogleScholarGoogle Scholar |
Fehrer J, Krak K, Chrtek J (2009) Intra-individual polymorphism in diploid and apomictic polyploid hawkweeds (Hieracium, Lactuceae, Asteraceae): disentangling phylogenetic signal, reticulation, and noise. BMC Evolutionary Biology 9, 239
| Intra-individual polymorphism in diploid and apomictic polyploid hawkweeds (Hieracium, Lactuceae, Asteraceae): disentangling phylogenetic signal, reticulation, and noise.Crossref | GoogleScholarGoogle Scholar |
Feliner GN, Rosselló JA (2007) Better the devil you know? Guidelines for insightful utilization of nrDNA ITS in species-level evolutionary studies in plants. Molecular Phylogenetics and Evolution 44, 911–919.
| Better the devil you know? Guidelines for insightful utilization of nrDNA ITS in species-level evolutionary studies in plants.Crossref | GoogleScholarGoogle Scholar |
Fitch WM (1970) Distinguishing homologous from analogous proteins. Systematic Zoology 19, 99–113.
| Distinguishing homologous from analogous proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3MXkvFyisw%3D%3D&md5=355fe8418505602b68ff2a07ddbbeab0CAS |
French PA, Brown GK, Bayly MJ (2016) Incongruent patterns of nuclear and chloroplast variation in Correa (Rutaceae): introgression and biogeography in south-eastern Australia. Plant Systematics and Evolution 302, 447–468.
| Incongruent patterns of nuclear and chloroplast variation in Correa (Rutaceae): introgression and biogeography in south-eastern Australia.Crossref | GoogleScholarGoogle Scholar |
Garcia-Jacas N, Soltis PS, Font M, Soltis DE, Vilatersana R, Susanna A (2009) The polyploid series of Centaurea toletana: glacial migrations and introgression revealed by nrDNA and cpDNA sequence analyzes. Molecular Phylogenetics and Evolution 52, 377–394.
| The polyploid series of Centaurea toletana: glacial migrations and introgression revealed by nrDNA and cpDNA sequence analyzes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXms12hsb4%3D&md5=fc7159531dfb3795e8eff33db641503dCAS |
George AS, Duretto MF, Forster PI (2013) Zieria. In ‘Flora of Australia. Vol. 26: Meliaceae, Rutaceae and Zygophyllaceae’. (Ed. A Wilson) pp. 282–336. (Australian Biological Resources Study: Canberra, ACT, Australia; and CSIRO Publishing: Melbourne, Vic. Australia)
Gibbs MJ, Armstrong JS, Gibbs AJ (2000) Sister-scanning: a Monte Carlo procedure for assessing signals in recombinant sequences. Bioinformatics 16, 573–582.
| Sister-scanning: a Monte Carlo procedure for assessing signals in recombinant sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXosFSqs7g%3D&md5=d3e2e2131b983749609b61ae1eba6d00CAS |
Gibbs AK, Udovicic FB, Drinnan AN, Ladiges P (2009) Phylogeny and classification of Eucalyptus subgenus Eudesmia (Myrtaceae) based on nuclear ribosomal DNA, chloroplast DNA and morphology. Australian Systematic Botany 22, 158–179.
| Phylogeny and classification of Eucalyptus subgenus Eudesmia (Myrtaceae) based on nuclear ribosomal DNA, chloroplast DNA and morphology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmvFygtrs%3D&md5=eb0d8224d0ef7997b8d187a23f406378CAS |
Harpke D, Peterson A (2008) 5.8 S motifs for the identification of pseudogenic ITS regions. Botany 86, 300–305.
| 5.8 S motifs for the identification of pseudogenic ITS regions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXltVKhs7k%3D&md5=c92e18f06fa65535f7d081eebb42cdbcCAS |
Heath L, van der Walt E, Varsani A, Martin DP (2006) Recombination patterns in aphthoviruses mirror those found in other picornaviruses. Journal of Virology 80, 11827–11832.
| Recombination patterns in aphthoviruses mirror those found in other picornaviruses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht12hu7bK&md5=4ffeffa2f824b76b8cc7732cb6c8c901CAS |
Hogbin P, Crisp M (2003) Evolution of the coastal neospecies Zieria prostrata (Rutaceae) and its relationship to the Zieria smithii species complex. Australian Systematic Botany 16, 515–525.
| Evolution of the coastal neospecies Zieria prostrata (Rutaceae) and its relationship to the Zieria smithii species complex.Crossref | GoogleScholarGoogle Scholar |
Holmes GD, Downing TL, James L, Blacket MJ, Hoffman AA, Bayly MJ (2014) Phylogeny of the holly grevilleas (Proteaceae) based on nuclear ribosomal and chloroplast DNA. Australian Systematic Botany 27, 56–77.
| Phylogeny of the holly grevilleas (Proteaceae) based on nuclear ribosomal and chloroplast DNA.Crossref | GoogleScholarGoogle Scholar |
Hong-Wa C, Besnard G (2013) Intricate patterns of phylogenetic relationships in the olive family as inferred from multi-locus plastid and nuclear DNA sequence analyses: a close-up on Chionanthus and Noronhia (Oleaceae). Molecular Phylogenetics and Evolution 67, 367–378.
| Intricate patterns of phylogenetic relationships in the olive family as inferred from multi-locus plastid and nuclear DNA sequence analyses: a close-up on Chionanthus and Noronhia (Oleaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjsFOrurw%3D&md5=09ed9dbda9a402096d397cd390cbe11eCAS |
Jobes DV, Thien LB (1997) A conserved motif in the 5.8 S ribosomal RNA (rRNA) gene is a useful diagnostic marker for plant internal transcribed spacer (ITS) sequences. Plant Molecular Biology Reporter 15, 326–334.
| A conserved motif in the 5.8 S ribosomal RNA (rRNA) gene is a useful diagnostic marker for plant internal transcribed spacer (ITS) sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjs1arurY%3D&md5=235caedb66d275833cf2296c6f344279CAS |
Käss E, Wink M (1997) Molecular phylogeny and phylogeography of Lupinus (Leguminosae) inferred from nucleotide sequences of the rbcL gene and ITS 1 + 2 regions of rDNA. Plant Systematics and Evolution 208, 139–167.
| Molecular phylogeny and phylogeography of Lupinus (Leguminosae) inferred from nucleotide sequences of the rbcL gene and ITS 1 + 2 regions of rDNA.Crossref | GoogleScholarGoogle Scholar |
King MG, Roalson EH (2008) Exploring evolutionary dynamics of nrDNA in Carex subgenus Vignea (Cyperaceae). Systematic Botany 33, 514–524.
| Exploring evolutionary dynamics of nrDNA in Carex subgenus Vignea (Cyperaceae).Crossref | GoogleScholarGoogle Scholar |
Ladiges PY, Bayly MJ, Nelson GJ (2010) East–west continental vicariance in Eucalyptus subgenus Eucalyptus (Myrtaceae). In ‘Beyond Cladistics: the Branching of a Paradigm’. (Eds DM Williams, S Knapp) pp. 267–302. (University of California Press: Berkeley, CA, USA)
Li F, Fan Q, Li Q, Chen S, Guo W, Cui D, Liao W (2014) Molecular phylogeny of Cotoneaster (Rosaceae) inferred from nuclear ITS and multiple chloroplast sequences. Plant Systematics and Evolution 300, 1533–1546.
| Molecular phylogeny of Cotoneaster (Rosaceae) inferred from nuclear ITS and multiple chloroplast sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsFCqu7c%3D&md5=7df6d66beb740357356f9dcffd5d1400CAS |
Liston A, Robinson WA, Oliphant JM, Alvarez-Buylla ER (1996) Length variation in the nuclear ribosomal DNA internal transcribed spacer region of non-flowering seed plants. Systematic Botany 21, 109–120.
| Length variation in the nuclear ribosomal DNA internal transcribed spacer region of non-flowering seed plants.Crossref | GoogleScholarGoogle Scholar |
Liu J-S, Schardl CL (1994) A conserved sequence in internal transcribed spacer 1 of plant nuclear rRNA genes. Plant Molecular Biology 26, 775–778.
| A conserved sequence in internal transcribed spacer 1 of plant nuclear rRNA genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXitVeisLs%3D&md5=887de17b2f3a1ebffb4be6b75cbdbd3bCAS |
Martin D, Rybicki E (2000) RDP: detection of recombination amongst aligned sequences. Bioinformatics 16, 562–563.
| RDP: detection of recombination amongst aligned sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnsVelsbc%3D&md5=b3f2cc03cea34041ad8a0851f2b3adf6CAS |
Martin DP, Posada D, Crandall KA, Williamson C (2005) A modified BOOTSCAN algorithm for automated identification of recombinant sequences and recombination breakpoints. AIDS Research and Human Retroviruses 21, 98–102.
| A modified BOOTSCAN algorithm for automated identification of recombinant sequences and recombination breakpoints.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmtlOntA%3D%3D&md5=9e7c581e01ece58766d87b341f294f96CAS |
Maynard Smith J (1992) Analyzing the mosaic structure of genes. Journal of Molecular Evolution 34, 126–129.
Mayol M, Rosselló JA (2001) Why nuclear ribosomal DNA spacers (ITS) tell different stories in Quercus. Molecular Phylogenetics and Evolution 19, 167–176.
| Why nuclear ribosomal DNA spacers (ITS) tell different stories in Quercus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjt1Gmsb8%3D&md5=aa564124771fe564550d7fc6e1865a35CAS |
Morton CM (2015) Phylogenetic relationships of Zieria (Rutaceae) inferred from chloroplast, nuclear, and morphological data. PhytoKeys 44, 15–38.
| Phylogenetic relationships of Zieria (Rutaceae) inferred from chloroplast, nuclear, and morphological data.Crossref | GoogleScholarGoogle Scholar |
Nei M, Rooney AP (2005) Concerted and birth-and-death evolution of multigene families. Annual Review of Genetics 39, 121–152.
| Concerted and birth-and-death evolution of multigene families.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xlt1Wktw%3D%3D&md5=d0dd7bfe676d5000042eb5136d42d8b1CAS |
Ochieng JW, Henry RJ, Baverstock PR, Steane DA, Shepherd M (2007) Nuclear ribosomal pseudogenes resolve a corroborated monophyly of the eucalypt genus Corymbia despite misleading hypotheses at functional ITS paralogs. Molecular Phylogenetics and Evolution 44, 752–764.
| Nuclear ribosomal pseudogenes resolve a corroborated monophyly of the eucalypt genus Corymbia despite misleading hypotheses at functional ITS paralogs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnslGgsLw%3D&md5=d4fe20f1055fe8b1266f31ff1c55b472CAS |
Padidam M, Sawyer S, Fauquet CM (1999) Possible emergence of new geminiviruses by frequent recombination. Virology 265, 218–225.
| Possible emergence of new geminiviruses by frequent recombination.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXnvFertbs%3D&md5=567dbb71d4f5e2c9587158cea6533abbCAS |
Parra-O C, Bayly MJ, Drinnan A, Udovicic F, Ladiges P (2009) Phylogeny, major clades and infrageneric classification of Corymbia (Myrtaceae), based on nuclear ribosomal DNA and morphology. Australian Systematic Botany 22, 384–399.
| Phylogeny, major clades and infrageneric classification of Corymbia (Myrtaceae), based on nuclear ribosomal DNA and morphology.Crossref | GoogleScholarGoogle Scholar |
Poczai P, Hyvönen J (2010) Nuclear ribosomal spacer regions in plant phylogenetics: problems and prospects. Molecular Biology Reports 37, 1897–1912.
| Nuclear ribosomal spacer regions in plant phylogenetics: problems and prospects.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXis1Wmu7c%3D&md5=08994c7d45488f84b0dc6c2cbc2ea628CAS |
Posada D, Crandall KA (2001) Evaluation of methods for detecting recombination from DNA sequences: Computer simulations. Proceedings of the National Academy of Sciences of the United States of America 98, 13757–13762.
| Evaluation of methods for detecting recombination from DNA sequences: Computer simulations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXovVyntrc%3D&md5=3bb08336582d71e5312d21e75e7797feCAS |
Potts AJ, 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.
| Constructing phylogenies in the presence of intra-individual site polymorphisms (2ISPs) with a focus on the nuclear ribosomal cistron.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhs1OqsA%3D%3D&md5=41cc2911afbe1d93244baa711df05b7eCAS |
Rauscher JT, Doyle JJ, Brown AHD (2002) Internal transcribed spacer repeat-specific primers and the analysis of hybridization in the Glycine tomentella (Leguminosae) polyploid complex. Molecular Ecology 11, 2691–2702.
| Internal transcribed spacer repeat-specific primers and the analysis of hybridization in the Glycine tomentella (Leguminosae) polyploid complex.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xpsl2msbo%3D&md5=56b3d2903d8de22c549a5b34ab522201CAS |
Rauscher JT, Doyle JJ, Brown AHD (2004) Multiple origins and nrDNA internal transcribed spacer homeologue evolution in the Glycine tomentella (Leguminosae) allopolyploid complex. Genetics 166, 987–998.
| Multiple origins and nrDNA internal transcribed spacer homeologue evolution in the Glycine tomentella (Leguminosae) allopolyploid complex.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjtlyntbY%3D&md5=0921ee5805b7ea49eb0fe47efb4d95fcCAS |
Razafimandimbison SG, Kellogg EA, Bremer B (2004) Recent origin and phylogenetic utility of divergent ITS putative pseudogenes: a case study from Naucleeae (Rubiaceae). Systematic Biology 53, 177–192.
| Recent origin and phylogenetic utility of divergent ITS putative pseudogenes: a case study from Naucleeae (Rubiaceae).Crossref | GoogleScholarGoogle Scholar |
Rieseberg LH, Wendel JF (1993) Introgression and its consequences in plants. In ‘Hybrid Zones and the Evolutionary Process.’ (Ed. RG Harrison) pp. 70–114. (Oxford University Press: New York, NY, USA)
Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.
| MRBAYES 3: Bayesian phylogenetic inference under mixed models.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntlKms7k%3D&md5=6664bded48a2cfc2057fa199d4219cadCAS |
Rowe HC, Renaut S, Guggisberg A (2011) RAD in the realm of next generation sequencing technologies. Molecular Ecology 20, 3499–3502.
Samuel R, Bachmair A, Jobst J, Ehrendorfer F (1998) ITS sequences from nuclear rDNA suggest unexpected phylogenetic relationships between Euro-Mediterranean, East Asiatic and North American taxa of Quercus (Fagaceae). Plant Systematics and Evolution 211, 129–139.
| ITS sequences from nuclear rDNA suggest unexpected phylogenetic relationships between Euro-Mediterranean, East Asiatic and North American taxa of Quercus (Fagaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjslWltbs%3D&md5=72f6e774ce0efb03612a4f58e940244fCAS |
Sanderson MJ, Doyle JJ (1992) Reconstruction of organismal and gene phylogenies from data on multigene families: concerted evolution, homoplasy, and confidence. Systematic Biology 41, 4–17.
| Reconstruction of organismal and gene phylogenies from data on multigene families: concerted evolution, homoplasy, and confidence.Crossref | GoogleScholarGoogle Scholar |
Smith JE (1798) The characters of twenty new genera of plants. Transactions of the Linnean Society of London 4, 213–223.
| The characters of twenty new genera of plants.Crossref | GoogleScholarGoogle Scholar |
Soltis PS, Soltis DE (2009) The role of hybridization in plant speciation. Annual Review of Plant Biology 60, 561–588.
| The role of hybridization in plant speciation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXntFGlsLc%3D&md5=737d6a9c354e727a5c872154113bdbbfCAS |
Soltis DE, Johnson LA, Looney C (1996) Discordance between ITS and chloroplast topologies in the Boykinia group (Saxifragaceae). Systematic Botany 21, 169–185.
| Discordance between ITS and chloroplast topologies in the Boykinia group (Saxifragaceae).Crossref | GoogleScholarGoogle Scholar |
Straub SCK, Parks M, Weitemier K, Fishbein M, Cronn RC, Liston A (2012) Navigating the tip of the genomic iceberg: next-generation sequencing for plant systematics. American Journal of Botany 99, 349–364.
| Navigating the tip of the genomic iceberg: next-generation sequencing for plant systematics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XksValtbo%3D&md5=81794225f5caac2a87545a884107598bCAS |
Suárez-Santiago VN, Salinas MJ, Garcia-Jacas N, Soltis PS, Soltis DE, Blanca G (2007) Reticulate evolution in the Acrolophus subgroup (Centaurea L., Compositae) from the western Mediterranean: origin and diversification of section Willkommia Blanca. Molecular Phylogenetics and Evolution 43, 156–172.
| Reticulate evolution in the Acrolophus subgroup (Centaurea L., Compositae) from the western Mediterranean: origin and diversification of section Willkommia Blanca.Crossref | GoogleScholarGoogle Scholar |
Swofford D (2001) ‘PAUP*. Phylogenetic analysis using parsimony, version 4.0b10.’ (Illinois Natural History Survey, Smithsonian Institution: Champaign, IL, USA)
Wagner WH (1983) Reticulistics: the recognition of hybrids and their role in cladistics and classification. In ‘Advances in Cladistics, Vol. 2’. (Eds NI Platnick, VA Funk) pp. 63–79 (Columbia University Press: New York, NY, USA)
Wagner A, Blackstone N, Cartwright P, Dick M, Misof B, Snow P, Wagner GP, Bartels J, Murtha M, Pendleton J (1994) Surveys of gene families using polymerase chain reaction: PCR selection and PCR drift. Systematic Biology 43, 250–261.
| Surveys of gene families using polymerase chain reaction: PCR selection and PCR drift.Crossref | GoogleScholarGoogle Scholar |
Weitemier K, Straub SCK, Cronn RC, Fishbein M, Schmickl R, McDonnell A, Liston A (2014) Hyb-Seq: combining target enrichment and genome skimming for plant phylogenomics. Applications in Plant Sciences 2, 1400042
| Hyb-Seq: combining target enrichment and genome skimming for plant phylogenomics.Crossref | GoogleScholarGoogle Scholar |
Wendel JF, Doyle JJ (1998) Phylogenetic incongruence: window into genome history and molecular evolution. In ‘Molecular Systematics of Plants II: DNA Sequencing’. (Eds DE Soltis, PS Soltis, JJ Doyle) pp. 265–296. (Springer Science+Business Media: New York, NY, USA)
White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In ‘PCR Protocols: a Guide to Methods and Applications’. (Eds MA Innis, DH Gelfand, JJ Sninsky, TJ White) pp. 315–322. (Academic Press, Inc.: New York, NY, USA)
Wright SD, Yong CG, Wichman SR, Dawson JW, Gardner RC (2001) Stepping stones to Hawaii: a trans-equatorial dispersal pathway for Metrosideros (Myrtaceae) inferred from nrDNA (ITS+ETS). Journal of Biogeography 28, 769–774.
| Stepping stones to Hawaii: a trans-equatorial dispersal pathway for Metrosideros (Myrtaceae) inferred from nrDNA (ITS+ETS).Crossref | GoogleScholarGoogle Scholar |
Xu B, Wu N, Gao X-F, Zhang L-B (2012) Analysis of DNA sequences of six chloroplast and nuclear genes suggests incongruence, introgression, and incomplete lineage sorting in the evolution of Lespedeza (Fabaceae). Molecular Phylogenetics and Evolution 62, 346–358.
| Analysis of DNA sequences of six chloroplast and nuclear genes suggests incongruence, introgression, and incomplete lineage sorting in the evolution of Lespedeza (Fabaceae).Crossref | GoogleScholarGoogle Scholar |
Yu W-B, Huang P-H, Li D-Z, Wang H (2013) Incongruence between nuclear and chloroplast DNA phylogenies in Pedicularis section Cyathophora (Orobanchaceae). PLoS One 8, e74828
| Incongruence between nuclear and chloroplast DNA phylogenies in Pedicularis section Cyathophora (Orobanchaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFeiurnJ&md5=32dd94ef37b8bce33b13ffa5e6ebc6c4CAS |
Zimmer EA, Martin SL, Beverley SM, Kan YW, Wilson AC (1980) Rapid duplication and loss of genes coding for the alpha chains of hemoglobin. Proceedings of the National Academy of Sciences of the United States of America 77, 2158–2162.
| Rapid duplication and loss of genes coding for the alpha chains of hemoglobin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXktVCktLc%3D&md5=a113e9eb3a5a234b8cf67e85a4a6fa57CAS |