• This record comes from PubMed

Complete chloroplast genomes from apomictic Taraxacum (Asteraceae): Identity and variation between three microspecies

. 2017 ; 12 (2) : e0168008. [epub] 20170209

Language English Country United States Media electronic-ecollection

Document type Journal Article

Chloroplast DNA sequences show substantial variation between higher plant species, and less variation within species, so are typically excellent markers to investigate evolutionary, population and genetic relationships and phylogenies. We sequenced the plastomes of Taraxacum obtusifrons Markl. (O978); T. stridulum Trávniček ined. (S3); and T. amplum Markl. (A978), three apomictic triploid (2n = 3x = 24) dandelions from the T. officinale agg. We aimed to characterize the variation in plastomes, define relationships and correlations with the apomictic microspecies status, and refine placement of the microspecies in the evolutionary or phylogenetic context of the Asteraceae. The chloroplast genomes of accessions O978 and S3 were identical and 151,322 bp long (where the nuclear genes are known to show variation), while A978 was 151,349 bp long. All three genomes contained 135 unique genes, with an additional copy of the trnF-GGA gene in the LSC region and 20 duplicated genes in the IR region, along with short repeats, the typical major Inverted Repeats (IR1 and IR2, 24,431bp long), and Large and Small Single Copy regions (LSC 83,889bp and SSC 18,571bp in O978). Between the two Taraxacum plastomes types, we identified 28 SNPs. The distribution of polymorphisms suggests some parts of the Taraxacum plastome are evolving at a slower rate. There was a hemi-nested inversion in the LSC region that is common to Asteraceae, and an SSC inversion from ndhF to rps15 found only in some Asteraceae lineages. A comparative repeat analysis showed variation between Taraxacum and the phylogenetically close genus Lactuca, with many more direct repeats of 40bp or more in Lactuca (1% larger plastome than Taraxacum). When individual genes and non-coding regions were for Asteraceae phylogeny reconstruction, not all showed the same evolutionary scenario suggesting care is needed for interpretation of relationships if a limited number of markers are used. Studying genotypic diversity in plastomes is important to characterize the nature of evolutionary processes in nuclear and cytoplasmic genomes with the different selection pressures, population structures and breeding systems.

See more in PubMed

Palmer JD and Thompson WF. Chloroplast DNA rearrangements are more frequent when a large inverted repeat sequence is lost. Cell 1982; 29: 537–550. PubMed

Jansen RK, Raubeson LA, Boore JL, Chumley TW, Haberle RC, Wyman SK, et al. Methods for obtaining and analyzing whole chloroplast genome sequences. Methods Enzymol. 2005; 395: 348–384. 10.1016/S0076-6879(05)95020-9 PubMed DOI

Hollingsworth PM, Forrest LL, Spouge JL, Hajibabaei M, Ratnasingham S, van der Bank M, et al. A DNA barcode for land plants. Proc Natl Acad Sci U S A. 2009; 106: 12794–12797. 10.1073/pnas.0905845106 PubMed DOI PMC

Birky CW Jr. The inheritance of genes in mitochondria and chloroplasts: laws, mechanisms, and models. Annu Rev Genet. 2001; 35: 125–148. 10.1146/annurev.genet.35.102401.090231 PubMed DOI

Stegemann S, Keuthe M, Greiner S, Bock R. Horizontal transfer of chloroplast genomes between plant species. Proc Natl Acad Sci USA. 2012; 109:2434–2438. 10.1073/pnas.1114076109 PubMed DOI PMC

Wang Z.H., Peng H., and Kilian N.. Molecular phylogeny of the Lactuca alliance (Cichorieae subtribe Lactucinae, Asteraceae) with focus on their Chinese centre of diversity detects potential events of reticulation and chloroplast capture. PloS One. 2013, 8: e82692 10.1371/journal.pone.0082692 PubMed DOI PMC

Moore MJ, Soltis PS, Bell CD, Burleigh JG, Soltis DE. Phylogenetic analysis of 83 plastid genes further resolves the early diversification of eudicots. Proc Natl Acad Sci U S A. 2010; 107: 4623–4628. 10.1073/pnas.0907801107 PubMed DOI PMC

Shinozaki K, Ohme M, Tanaka M, Wakasugi T, Hayashida N, Matsubayashi T, et al. The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J. 1986; 5: p. 2043 PubMed PMC

Jansen RK, Cai Z, Raubeson LA, Daniell H, Leebens-Mack J, Müller KF, et al. Analysis of 81 genes from 64 plastid genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns. Proc Natl Acad Sci U S A. 2007;104:19369–19374. 10.1073/pnas.0709121104 PubMed DOI PMC

Moore MJ, Bell CD, Soltis PS, Soltis DE. Using plastid genome-scale data to resolve enigmatic relationships among basal angiosperms. Proc Natl Acad Sci U S A. 2007;104: 19363–19368. 10.1073/pnas.0708072104 PubMed DOI PMC

Parks M, Cronn R, Liston A. Increasing phylogenetic resolution at low taxonomic levels using massively parallel sequencing of chloroplast genomes. BMC Biol. 2009;7: 1. PubMed PMC

Wojciechowski MF. IRLC (Inverted Repeat Lacking Clade). Version 11 July 2006: http://tolweb.org/IRLC_%28Inverted_Repeat-lacking_clade%29/60358/2006.07. 11. The tree of life web project, http://tolweb.org. 2006.

Raubeson LA, Jansen RK. A rare chloroplast-DNA structural mutation is shared by all conifers. Biochem Syst Ecol. 1992; 20: 17–24.

Luo J, Hou BW, Niu ZT, Liu W, Xue QY, Ding XY. Comparative chloroplast genomes of photosynthetic orchids: insights into evolution of the Orchidaceae and development of molecular markers for phylogenetic applications. PLoS One. 2014; 9: e99016 10.1371/journal.pone.0099016 PubMed DOI PMC

Bruni I, De Mattia F, Galimberti A, Galasso G, Banfi E, Casiraghi M, Labra M. Identification of poisonous plants by DNA barcoding approach. Int J Legal Med. 2010; 124: 595–603. 10.1007/s00414-010-0447-3 PubMed DOI

Bruni I, Galimberti A, Caridi L, Scaccabarozzi D, De Mattia F, Casiraghi M, Labra M. A DNA barcoding approach to identify plant species in multiflower honey. Food chem. 2015; 170:308–15. 10.1016/j.foodchem.2014.08.060 PubMed DOI

Hollingsworth PM, Li DZ, van der Bank M, Twyford AD. Telling plant species apart with DNA: from barcodes to genomes. Phil. Trans. R. Soc. B. 2016; 371: 20150338 10.1098/rstb.2015.0338 PubMed DOI PMC

Dong W, Liu J, Yu J, Wang L, Zhou S. Highly variable chloroplast markers for evaluating plant phylogeny at low taxonomic levels and for DNA barcoding. PLoS One. 2012; 7: e35071 10.1371/journal.pone.0035071 PubMed DOI PMC

Shaw J, Shafer HL, Leonard OR, Kovach MJ, Schorr M, Morris AB. Chloroplast DNA sequence utility for the lowest phylogenetic and phylogeographic inferences in angiosperms: The tortoise and the hare IV. Am J Bot. 2014; 101: 1987–2004. 10.3732/ajb.1400398 PubMed DOI

Zehdi-Azouzi S, Cherif E, Moussouni S, Gros-Balthazard M, Naqvi SA, Ludeña B, et al.. Genetic structure of the date palm (Phoenix dactylifera) in the Old World reveals a strong differentiation between eastern and western populations. Ann Bot. 2015; 116: 101–12. 10.1093/aob/mcv068 PubMed DOI PMC

Särkinen T, George M. Predicting plastid marker variation: can complete plastid genomes from closely related species help? PLoS One. 2013; 8: e82266 10.1371/journal.pone.0082266 PubMed DOI PMC

Wang M, Cui L, Feng K, Deng P, Du X, Wan F, et al.. Comparative analysis of Asteraceae chloroplast genomes: Structural organization, RNA editing and evolution. Plant Mol Biol Report. 2015; 33: 1526–1538.

Kim KJ, Choi KS, Jansen RK. Two chloroplast DNA inversions originated simultaneously during the early evolution of the sunflower family (Asteraceae). Mol Biol Evol. 2005; 22: 1783–1792. 10.1093/molbev/msi174 PubMed DOI

Asker S, Jerling L. Apomixis in plants. CRC press; 1992.

Mendel G, Versuche über Pflanzenhybriden. Verhandlungen des naturforschenden Vereines in Brunn. 1866; 4: 44.

Richards AJ, The origin of Taraxacum agamospecies. Bot J Linn Soc. 1973; 66: 189–211. PubMed PMC

Mogie M, Ford H. Sexual and asexual Taraxacum species. Bot J Linn Soc. 1988; 35: 155–168.

King LM, Schaal BA. Genotypic variation within asexual lineages of Taraxacum officinale. Proc Natl Acad Sci U S A. 1990; 87: 998–1002. PubMed PMC

Nogler G.A., Gametophytic apomixis. Springer; 1984.

Kirschner J, Drábková LZ, Štěpánek J, Uhlemann I. Towards a better understanding of the Taraxacum evolution (Compositae—Cichorieae) on the basis of nrDNA of sexually reproducing species. Plant Syst Evol. 2015; 301: 1135–56.

Van der Hulst RG, Mes TH, Den Nijs JC, Bachmann K. Amplified fragment length polymorphism (AFLP) markers reveal that population structure of triploid dandelions (Taraxacum officinale) exhibits both clonality and recombination. Mol Ecol. 2000; 9: 1–8. PubMed

Majeský Ľ, Vašut RJ, Kitner M, Trávníček B. The pattern of genetic variability in apomictic clones of Taraxacum officinale indicates the alternation of asexual and sexual histories of apomicts. PLoS One. 2012; 7: e41868 10.1371/journal.pone.0041868 PubMed DOI PMC

Mes TH, Kuperus P, Kirschner J, Štepánek J, Štorchová H, Oosterveld P, et al., Detection of genetically divergent clone mates in apomictic dandelions. Mol Ecol. 2002; 11: 253–265. PubMed

Majeský Ľ, Vašut RJ, Kitner M. Genotypic diversity of apomictic microspecies of the Taraxacum scanicum group (Taraxacum sect. Erythrosperma). Plant Syst Evol. 2015; 301: 2105–24.

Wittzell H. Chloroplast DNA variation and reticulate evolution in sexual and apomictic sections of dandelions. Mol Ecol. 1999; 8: 2023–2035. PubMed

Kirschner J, Štěpánek J, Mes TH, Den Nijs JC, Oosterveld P, Štorchová H, et al. Principal features of the cpDNA evolution in Taraxacum (Asteraceae, Lactuceae): a conflict with taxonomy. Plant Syst Evol. 2003; 239: 231–255.

Mes TH, Kuperus P, Kirschner J, Stepanek J, Oosterveld P, Storchova H, et al. Hairpins involving both inverted and direct repeats are associated with homoplasious indels in non-coding chloroplast DNA of Taraxacum (Lactuceae: Asteraceae). Genome. 2000; 43: 634–641. PubMed

Doyle JJ. Isolation of plant DNA from fresh tissue. Focus. 1990; 12: 13–15.

Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012; 28: 1647–1649. 10.1093/bioinformatics/bts199 PubMed DOI PMC

Timme RE, Kuehl JV, Boore JL, Jansen RK. A comparative analysis of the Lactuca and Helianthus (Asteraceae) plastid genomes: identification of divergent regions and categorization of shared repeats. Am J Bot. 2007; 94: 302–312. 10.3732/ajb.94.3.302 PubMed DOI

Wyman SK, Jansen RK, Boore JL, Automatic annotation of organellar genomes with DOGMA. Bioinformatics. 2004; 20: 3252–3255. 10.1093/bioinformatics/bth352 PubMed DOI

Lowe TM, Eddy SR. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 1997; 25: 955–964. PubMed PMC

Conant GC, Wolfe KH. GenomeVx: simple web-based creation of editable circular chromosome maps. Bioinformatics. 2008; 24: 861–862. 10.1093/bioinformatics/btm598 PubMed DOI

Kurtz S, Choudhuri JV, Ohlebusch E, Schleiermacher C, Stoye J, Giegerich R. REPuter: the manifold applications of repeat analysis on a genomic scale. Nucleic Acids Res. 2001; 29: 4633–4642. PubMed PMC

Benson G. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 1999; 27: 573 PubMed PMC

Frazer KA, Pachter L, Poliakov A, Rubin EM, Dubchak I. VISTA: computational tools for comparative genomics. Nucleic Acids Res. 2004; 32: W273–279. 10.1093/nar/gkh458 PubMed DOI PMC

Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013; 30: 2725–2729. 10.1093/molbev/mst197 PubMed DOI PMC

Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution, 1985; 783–791. PubMed

Van der Hulst RG, Mes TH, Falque M, Stam P, Den Nijs JC, Bachmann K. Genetic structure of a population sample of apomictic dandelions. Heredity. 2003; 90: 326–335. 10.1038/sj.hdy.6800248 PubMed DOI

Ford H. Life history strategies in two coexisting agamospecies of dandelion. Biol J Linn Soc. 1985; 25: 169–186.

Richards AJ. Plant breeding systems. George Allen & Unwin; 1986.

Kirschner J, Oplaat C, Verhoeven KJ, Zeisek V, Uhlemann I, Trávníček B, Räsänen J. Identification of oligoclonal agamospermous microspecies: taxonomic specialists versus microsatellites. Preslia. 2016; 88: 1–7.

Wolfe KH, Li WH, Sharp PM. Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc Natl Acad Sci U S A. 1987; 84: 9054–9058. PubMed PMC

Richards AJ. A comparison of within-plant karyological heterogeneity between agamospermous and sexual Taraxacum (Compositae) as assessed by the nucleolar organiser chromosome. Plant Syst Evol. 1989; 163: 177–185.

Heslop-Harrison JP, Brandes A, Taketa S, Schmidt T, Vershinin AV, Alkhimova EG, et al., The chromosomal distributions of Ty1-copia group retrotransposable elements in higher plants and their implications for genome evolution. Genetica. 1997; 100: 197–204. PubMed

Liu Y, Huo N, Dong L, Wang Y, Zhang S, Young HA, et al., Complete chloroplast genome sequences of Mongolia medicine Artemisia frigida and phylogenetic relationships with other plants. PLoS One. 2013; 8: e57533 10.1371/journal.pone.0057533 PubMed DOI PMC

Lu C, Shen Q, Yang J, Wang B, Song C. The complete chloroplast genome sequence of Safflower (Carthamus tinctorius L.). Mitochondrial DNA A DNA MappSeqAnal. 2015; March 5: 1–3. PubMed

Ahmed I, Biggs PJ, Matthews PJ, Collins LJ, Hendy MD, Lockhart PJ. Mutational dynamics of aroid chloroplast genomes. Genome Biol Evol. 2012; 4: 1316–1323. 10.1093/gbe/evs110 PubMed DOI PMC

Kanamoto H, Yamashita A, Okumura S, Hattori M, Tomizawa KI. The complete genome sequence of the Lactuca sativa (lettuce) chloroplast. Plant Cell Physiol. 2004; 45:. S39–S39.

Holmquist GP. Chromosome bands, their chromatin flavors, and their functional features. Am J Hum Genet. 1992; 51: 17 PubMed PMC

Walker JF, Zanis MJ, Emery NC. Comparative analysis of complete chloroplast genome sequence and inversion variation in Lasthenia burkei (Madieae, Asteraceae). Am J Bot. 2014; 101: 722–729. 10.3732/ajb.1400049 PubMed DOI

Kilian N, Gemeinholzer B, and Lack H. Cichorieae. Systematics, evolution, and biogeography of Compositae, 2009: 343–383.

Tremetsberger K, Gemeinholzer B, Zetzsche H, Blackmore S, Kilian N, Talavera S. Divergence time estimation in Cichorieae (Asteraceae) using a fossil-calibrated relaxed molecular clock. Org Divers Evol. 2013; 13: 1–3.

Nie X, Lv S, Zhang Y, Du X, Wang L, Biradar SS, Tan X, Wan F, Weining S. Complete chloroplast genome sequence of a major invasive species, crofton weed (Ageratina adenophora). PLoS One. 2012; 7: e36869 10.1371/journal.pone.0036869 PubMed DOI PMC

McCauley DE, Sundby AK, Bailey MF, Welch ME. Inheritance of chloroplast DNA is not strictly maternal in Silene vulgaris (Caryophyllaceae): evidence from experimental crosses and natural populations. Am. J. Bot.. 2007; 94:1333–1337. 10.3732/ajb.94.8.1333 PubMed DOI

Ellis JR, Bentley KE, McCauley DE. Detection of rare paternal chloroplast inheritance in controlled crosses of the endangered sunflower Helianthus verticillatus. Heredity. 2008; 100:574–80. 10.1038/hdy.2008.11 PubMed DOI

Saeidi H, Rahiminejad MR, Vallian S, Heslop-Harrison JS. Biodiversity of diploid D-genome Aegilops tauschii Coss. in Iran measured using microsatellites. Genet Resour Crop Evol. 2006; 53: 1477–1484.

Sterk AA, Hommels CH, Jenniskens MJPJ, Neuteboom JH, den Nijs JCM, Oosterveld P et al. Paardebloemen: planten zonder vader. Variatie, evolutie en toepassingen van het geslacht paardebloem (Taraxacum). Utrecht: KNNV; 1987: 184–189.

Richards AJ. The origin of Taraxacum agamospecies. J. Linn. Soc. Bot. 1973; 66: 189–211. PubMed PMC

Dempewolf H, Kane NC, Ostevik KL, Geleta M, Barker MS, Lai Z, Stewart ML, Bekele E, Engels JM, Cronk QC, Rieseberg LH. Establishing genomic tools and resources for Guizotia abyssinica (Lf) Cass.—the development of a library of expressed sequence tags, microsatellite loci, and the sequencing of its chloroplast genome. Mol Ecol Resour. 2010; 10:1048–58. 10.1111/j.1755-0998.2010.02859.x PubMed DOI

Kumar S, Hahn FM, McMahan CM, Cornish K, Whalen MC. Comparative analysis of the complete sequence of the plastid genome of Parthenium argentatum and identification of DNA barcodes to differentiate Parthenium species and lines. BMC plant biology. 2009; 17:1. PubMed PMC

Liu PL, Wan Q, Guo YP, Yang J, Rao GY. Phylogeny of the genus Chrysanthemum L.: evidence from single-copy nuclear gene and chloroplast DNA sequences. PLoS One. 2012; 7: e48970 10.1371/journal.pone.0048970 PubMed DOI PMC

Choi KS, Park S. The complete chloroplast genome sequence of Aster spathulifolius (Asteraceae); genomic features and relationship with Asteraceae. Gene. 2015; 572: 214–221. 10.1016/j.gene.2015.07.020 PubMed DOI

Doorduin L, Gravendeel B, Lammers Y, Ariyurek Y, Chin-A-Woeng T, Vrieling K. The complete chloroplast genome of 17 individuals of pest species Jacobaea vulgaris: SNPs, microsatellites and barcoding markers for population and phylogenetic studies. DNA research. 2011; 28: dsr002. PubMed PMC

Zhang Y, Li L, Yan TL, Liu Q. Complete chloroplast genome sequences of Praxelis (Eupatorium catarium Veldkamp), an important invasive species. Gene. 2014; 549: 58–69. 10.1016/j.gene.2014.07.041 PubMed DOI

Turner KG, Grassa CJ. Complete plastid genome assembly of invasive plant, Centaurea diffusa. bioRxivorg. 2014; 1: 005900.

Curci PL, De Paola D, Danzi D, Vendramin GG, Sonnante G. Complete chloroplast genome of the multifunctional crop globe artichoke and comparison with other Asteraceae. PLoS One. 2015; 10: e0120589 10.1371/journal.pone.0120589 PubMed DOI PMC

Find record

Citation metrics

Loading data ...

Archiving options

Loading data ...