Genomic repeat abundances contain phylogenetic signal

Systematic Biology

Volumn 64, Issue 1, 2015, Pages 112-126

  Dodsworth, Steven ^a,b   Chase, Mark W ^b,c   Kelly, Laura J ^a,b   Leitch, Ilia J ^b   Macas, Jiři ^d   Novak, Petr ^d   Piednoel, Mathieu ^e   Weiss Schneeweiss, Hanna ^f   Leitch, Andrew R ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b JODRELL LABORATORY   (United Kingdom)

^c UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^d INSTITUTE OF PLANT MOLECULAR BIOLOGY   (Czech Republic)

^e UNIVERSITY OF MUNICH   (Germany)

^f UNIVERSITY OF VIENNA   (Austria)

Author keywords

Continuous characters; Genomics; Molecular systematics; Next generation sequencing; Phylogenetics; RepetitiveDNA

Indexed keywords

PLANT DNA;

ANGIOSPERM; ANIMAL; CLASSIFICATION; CLUSTER ANALYSIS; DROSOPHILA; GENE; GENETICS; GENOME; NUCLEOTIDE REPEAT; PHYLOGENY;

ANGIOSPERMS; ANIMALS; CLUSTER ANALYSIS; DNA, PLANT; DROSOPHILA; GENES, INSECT; GENOME; PHYLOGENY; REPETITIVE SEQUENCES, NUCLEIC ACID;

EID: 84965165257     PISSN: 10635157     EISSN: 1076836X     Source Type: Journal    
DOI: 10.1093/sysbio/syu080     Document Type: Article

References (87)

1. Angiosperm Phylogeny Group. 2009. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot. J. Linn. Soc. 161:105-121.
2. Ambrozova K., Mandakova T., Bures P., Neumann P., Leitch I.J., Koblizkova A., Macas J., Lysak M.A. 2011. Diverse retrotransposon families and an AT-rich satellite DNA revealed in giant genomes of Fritillaria lilies. Ann. Bot. 107:255-268.
3. Bai C., AlversonW.S., Follansbee A.,Waller D.M. 2012. New reports of nuclear DNA content for 407 vascular plant taxa from the United States. Ann. Bot. 110:1623-1629.
4. Barrett C.F., Davis J.I., Leebens-Mack J., Conran, J.G., Stevenson D.W. 2013. Plastid genomes and deep relationships among the commelinid monocot angiosperms. Cladistics 29:65-87.
5. Bock D.G., Kane N.C., Ebert D.P., Rieseberg L.H. 2014. Genome skimming reveals the origin of the Jerusalem Artichoke tuber crop species: neither from Jerusalem nor an artichoke. New Phyt. 201:1021-1030.
6. Brookfield J.F.Y. 2005. The ecology of the genome-mobile DNA elements and their hosts. Nat. Rev. Gen. 6:128-136.
7. Bybee S.M., Bracken-Grissom H., Haynes B.D., Hermansen R.A., Byers R.L., Clement M.J., Udall J.A., Wilcox E.R., Crandall K.A. 2011. Targeted amplicon sequencing (TAS): A scalable next-gen approach to multilocus, multitaxa phylogenetics. Genome Biol. Evol. 3:1312-1323.
8. Carpenter M.L., Buenrostro J.D., Valdiosera C., Schroeder H., Allentoft M.E., Sikora M., Rasmussen M., Gravel S., Guillen S., Nekhrizov G., Leshtakov K., Dimitrova D., Theodossiev N., Pettener D., Luiselli D., Sandoval K., Morena-Estrada A., Li Y., Wang J., Gilbert T.P., Willerslev E., Greenleaf W.J., Bustamante C.D. 2013. Pulling out the 1%: Whole-genome capture for the targeted enrichment of ancient DNA sequencing libraries. Am. J. Hum. Genet. 93: 852-864.
9. CBOL Working Plant Group. 2009. A DNA barcode for land plants. Proc. Natl. Acad. Sci. USA 106:12794-12797.
10. Chase M.W., Knapp S., Cox A.V., Clarkson J.J., Butsko Y., Joseph J., Savolainen V., Parokonny A.S. 2003. Molecular systematics, GISH and the origin of hybrid taxa in Nicotiana (Solanaceae). Ann. Bot. 92:107-127.
11. Clarkson J.J., Knapp S., Garcia V.F., Olmstead R.G., Leitch A.R., Chase M.W. 2004. Phylogenetic relationships in Nicotiana (Solanaceae) inferred from multiple plastid DNA regions. Mol. Phyl. Evol. 33:75-90.
12. Clarkson J.J., Lim K.Y., Kovarik A., Chase M.W., Knapp S., Leitch A.R. 2005. Long-term genome diploidisation in allopolyploid Nicotiana section Repandae (Solanaceae). New Phytol. 168:241-252.
13. Clarkson J.J.,Kelly L.J., LeitchA.R.,KnappS., ChaseM.W. 2010.Nuclear glutamine synthetase evolution in Nicotiana: Phylogenetics and the origins of allotetraploid and homoploid (diploid) hybrids. Mol. Phyl. Evol. 55:99-112.
14. Coleman A.W. 2009. Is there a molecular key to the level of 'biological species' in eukaryotes-ADNAguide. Mol. Phyl. Evol. 50: 197-203.
15. Cronn R., Knaus B.J., Liston A., Maughan P.J., Parks M., Syring J.V., Udall J. 2012. Targeted enrichment strategies for next-generation plant biology. Am. J. Bot. 99:291-311.
16. Day P.D., BergerM., Hill L., FayM.F., Leitch A.R., Leitch I.J., Kelly, L.J. 2014. Evolutionary relationships in the medicinally important genus Fritillaria L. (Liliaceae). Mol. Phyl. Evol. 80:11-19.
17. Ebersberger I., de Matos Simoes R., Kupczok A., Gube M., Kothe E., Voigt K., von Haeseler A. 2011. A consistent phylogenetic backbone for the fungi. Mol. Biol. Evol. 29:1319-1334.
18. Edwards S.V., Fertil B., Giron A., Deschavanne P.J. 2002. A genomic schism in birds revealed by phylogenetic analysis of DNA strings. Syst. Biol. 51:599-613.
19. Fedoroff N.V. 2012. Transposable elements, epigenetics, and genome evolution. Science 338:758-767.
20. Felsenstein J. 1989. PHYLIP-Phylogeny Inference Package (Version 3.2). Cladistics 5:164-166.
21. Felsenstein J. 2005. PHYLIP (Phylogeny Inference Package) version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle.
22. Flavell R.B., Bennett M.D., Smith J.B., Smith D.B. 1974. Genome size and the proportion of repeated nucleotide sequence DNA in plants. Biochem. Genet. 12:257-269.
23. Glenn T.C. 2011. Field guide to next-generation DNA sequencers. Mol. Ecol. Res. doi:10.1111/j.1755-0998.2011.03024.x.
24. Goloboff P.A., Farris J.S., Nixon K. 2003a. Tree analysis using new technology [Internet]. Program and documentation. Distributed by the authors. Available from: http://www.zmuc.dk/ public/phylogeny.
25. Goloboff P.A., Farris J.S., Kallersjo M., Oxelman B., Ramirez M.J., Szumik C.A. 2003b.Improvements to resampling measures of group support. Cladistics 19:324-332.
26. Goloboff P.A., Mattoni C.I., QuinterosA.S. 2006. Continuous characters analyzed as such. Cladistics 22:589-601.
27. Goloboff P.A., Farris J.S., Nixon K.C. 2008. TNT, a free program for phylogenetic analysis. Cladistics 24:774-786.
28. Goloboff P.A., Catalano S.A., Mirande J.M., Szumik C.A., Arias J.S., Kallersjo M., Farris J.S. 2009. Phylogenetic analysis of 73060 taxa corroborates major eukaryotic groups. Cladistics 25: 211-230.
29. Guschanski K., Krause J., Sawyer S., Valente L.M., Bailey S., Finstermeier K., Sabin R., Gilissen E., Sonet G., Nagy Z.T., Lenglet G., Mayer F., Savolainen V. 2013. Next-generation museomics disentangles one of the largest primate radiations. Syst. Biol. 62(4):539-554.
30. Hansen C.N., Heslop-Harrison J.S. 2004. Sequences and phylogenies of plant pararetroviruses, viruses and transposable elements. Adv. Bot. Res. 41:165-193.
31. Hebert P.D.N., Cywinska A., Ball S.L., deWaard J.R. 2003. Biological identifications through DNA barcodes. Proc. R. Soc. Biol. Sci. SerB. 270:313-321.
32. Huson D.H., Bryant D. 2006. Application of phylogenetic networks in evolutionary studies. Mol. Biol. Evol. 23:254-267.
33. Jurka J., Bao W., Kojima K.K. 2011. Families of transposable elements, population structure and the origin of species. Biol. Direct 6:44.
34. Jurka J., Bao W., Kojima K.K., Kohany O., Yurka M.G. 2012. Distinct groups of repetitive families preserved in mammals correspond to different periods of regulatory innovations in vertebrates. Biol. Direct 7:36.
35. Kayal E., Roure B., Philippe H., Collins A.G., Lavrov D.V. 2013. Cnidarian phylogenetic relationships as revealed by mitogenomics. BMC Evol. Biol. 13:5.
36. Kejnovsky E., Leitch I.J., Leitch A.R. 2009. Contrasting evolutionary dynamics between angiosperm and mammalian genomes. TREE 24:572-582.
37. Kelly L.J., Leitch A.R., Clarkson J.J., Hunter R.B., Knapp S., Chase M.W. 2010. Intragenic recombination events and evidence for hybrid speciation in Nicotiana (Solanaceae). Mol. Biol. Evo. 27: 781-799.
38. Kelly L.J., Leitch, I.J. 2011. Why size really matters when sequencing plant genomes. Plant Ecol. Div. 5:415-425.
39. Kelly L.J., Leitch A.R., Fay M.F., Renny-Byfield S., Pellicer J., Macas J., Leitch I.J. 2012. Why size really matters when sequencing plant genomes. Plant Ecol. Div. 5:415-425.
40. Kelly L.J., Leitch A.R., Clarkson J.J., Knapp S., Chase M.W. 2013. Reconstructing the complex evolutionary origin of wild allopolyploid tobaccos (Nicotiana section Suaveolentes). Evolution 67:80-94.
41. Kovarik A., Renny-Byfield S., Grandbastien M-A., Leitch A.R. 2012. Evolutionary implications of genome and karyotype restructuring in Nicotiana tabacum L. In: Soltis P.S., Soltis D.E., editors. Polyploidy and Genome Evolution. London: Springer.
42. Leitch A.R., Leitch I.J. 2008. Perspective - genomic plasticity and the diversity of polyploid plants. Science 320:481-483.
43. Leitch A.R., Leitch I.J. 2012. Ecological and genetic factors linked to contrasting genome dynamics in seed plants. New Phytol. 194: 629-646.
44. Lim K.Y., Matyasek R., Lichtenstein C.P., Leitch A.R. 2000. Molecular cytogenetic analyses and phylogenetic studies in Nicotiana section Tomentosae. Chromosoma 109:245-258.
45. Lim K.Y.,KovarikA., Matyasek R., ChaseM.W., Knapp S., McCarthy E., Clarkson J.J., LeitchA.R. 2006.Comparative genomics and repetitive sequence divergence in the species of diploid Nicotiana section Alatae. Plant J. 48:907-919.
46. Macas J., Neumann P., Navratilova A. 2007. Repetitive DNA in the pea (Pisum sativum L.) genome: comprehensive characterisation using 454 sequencing and comparison to soybean and Medicago trunculata. BMC Genomics 8:427.
47. Mallatt J.,Waggoner Craig C., Yoder M.J. 2010. Nearly complete rRNA genes assembled from across themetazoan animals: effects of more taxa, a structure-based alignment, and paired-sites evolutionary models on phylogeny reconstruction. Mol. Phyl. Evol. 55:1-17.
48. Meyer M., Stenzel U., Myles S., Prufer K., Hofreiter M. 2007. Targeted high-throughput sequencing of tagged nucleic acid samples. Nucleic Acids Res. 35:e97.
49. Murray M.G., Peters D.L., Thompson W.F. 1981. Ancient repeated sequences in the pea and mung bean genomes and implications for genome evolution. J. Mol. Evol. 17:31-42.
50. Nichols R. 2001. Gene trees and species trees are not the same. Trends Ecol. Evol. 16:364.
51. Neumann P., Navratilova A., Schroeder-Reiter E., Koblizkova A., Steinbauerova V., Chocholova E., Novak P., Wanner G., Macas J. 2012. Stretching the rules: Monocentric chromosomes with multiple centromere domains. PLoS Genetics 8:e1002777.
52. Novak P., Neumann P., Macas J. 2010. Graph-based clustering and characterisation of repetitive sequences in next-generation sequencing data. BMC Bioinformatics 11:378.
53. Novak P., Neumann P., Pech J., Steinhaisl J., Macas J. 2013. RepeatExplorer: a Galaxy-based web server for genome-wide characterisation of eukaryotic repetitive elements from nextgeneration sequence reads. Bioinformatics. 29(6):792-793.
54. Obbard D.J., Maclennan J., Kim K.W., Rambaut A., O'Grady P.M., Jiggins F.M. 2012. Estimating divergence dates and substitution rates in the Drosophila phylogeny. Mol. Biol. Evol. 29:3459-3473.
55. Pellicer J., Fay M.F., Leitch I.J. 2010. The largest eukaryotic genome of them all? Bot J. Linn. Soc. 164:10-15.
56. Philippe H., Derelle R., Lopez P., Pick K., Borchiellini C., Boury-Esnault N., Vacelet J., Renard E., Houliston E., Queinnec E., Da Silva C., Wincker P., Le Guyader H., Leys S., Jackson D.J., Schreiber F., Erpenbeck D., Morgenstern B., Worheide G., Manuel M. 2009. Phylogenomics revives traditional views on deep animal relationships. Curr. Biol. 19:706-712.
57. Pagan H.J.T., Macas J.,Novak P., McCulloch E.S., Stevens R.D., RayD.A. 2012. Survey sequencing reveals elevated DNA transposon activity, novel elements, and variation in repetitive landscapes among bats. Genome Biol. Evol. 4:575-585.
58. Parisod C., Mhiri C., Lim K.Y., Clarkson J.J., Chase M.W., Leitch A.R., Grandbastien M-A. 2012. Differential dynamics of transposable elements during long-termdiploidisation of Nicotiana section Repandae (Solanaceae) allopolyploid genomes. PLoS One 7:e50352.s
59. Park J.M., Manen J.F., Colwell A.E., Schneeweiss G.M. 2008. A plastid gene phylogeny of the non-photosynthetic parasitic Orobanche (Orobanchaceae) and related genera. J. Plant Res. 121: 365-376.
60. Piednoel M., Aberer A.J., Schneeweiss G.M., Macas J., Novak P., Gundlach H., Temsch E.M., Renner S.S. 2012. Next-generation sequencing reveals the impact of repetitive DNA across phylogenetically closely-related genomes of Orobanchaceae. Mol. Biol. Evol. 29:3601-3611.
61. Piednoel M., Carrete-Vega G., Renner S.S. 2013. Characterization of the LTR retrotransposon repertoire of a plant clade of six diploid and one tetraploid species. Plant J. 75(4):699-709.
62. Pillon Y., Johansen J., Sakishima T., Chamala S., Brad Barbazuk W., Roalson E.H., Price D.K., Stacy E.A. 2013. Potential use of low-copy nuclear genes in DNA barcoding: a comparison with plastid genes in two Hawaiian plant radiations. BMC Evol. Biol.13:35.
63. Pride D.T., Meinersmann R.J., Wassenaar T.M., Blaser M.J. 2003. Evolutionary implications of microbial genome tetranucleotide frequency biases. Genome Res. 13:145-158.
64. Renny-Byfield S., Chester M., Kovarik A., LeComber S.C., Grandbastien M-A., Deloger M., Nichols R.A., Macas J., Novak P., Chase M.W., Leitch A.R. 2011. Next generation sequencing reveals genome downsizing in allotetraploid Nicotiana tabacum, predominantly through the elimination of paternally derived repetitive DNAs. Mol. Biol. Evol. 28:2843-2854.
65. Renny-Byfield S.,KovarikA., ChesterM., Nichols R.A., Macas J.,Novak P., Leitch A.R. 2012. Independent, rapid and targeted loss of highly repetitive DNA in natural and synthetic allopolyploids of Nicotiana tabacum. PLoS One 7:e36963.
66. Renny-Byfield S., Kovarik A., Kelly L.J., Macas J., Novak P., Chase M.W., Nichols R.A., Pancholi M.R., Grandbastien M-A., Leitch A.R. 2013. Diploidisation and genome size change in allopolyploids is associated with differential dynamics of low and high copy sequences. Plant J. 74(5):829-839.
67. RonstedN., LawS., Thornton H., FayM.F., ChaseM.W. 2005. Molecular phylogenetic evidence for the monophyly of Fritillaria and Lilium (Liliaceae; Liliales) and the infrageneric classification of Fritillaria. Mol. Phyl. Evol. 35:509-527.
68. Rubin B.E.R., Ree R.H., Moreau C.S. 2012. Inferring phylogenies from RAD sequence data. PLoS One 7:e33394.
69. Sarkiinen T., Staats M., Richardson J.E., Cowan R.S., Bakker F.T. 2012. How to open the treasure chest? Optimising DNA extraction from herbarium specimens. PloS One 7:e43808.
70. Schaefer H., Hechenleitner P., Santos-Guerra A., Menezes de Sequeira M., Pennington R.T., Kenicer G., Carine M.A. 2012. Systematics, biogeography, and character evolution of the legume tribe Fabeae with special focus on themiddle-Atlantic island lineages.BMCEvol. Biol. 12:250.
71. Schneeweiss G.M., Colwell A.E., Park J.M., Jang C.G., Stuessy T.F. 2004. Phylogeny of holoparasitic Orobanche (Orobanchaceae) inferred from nuclear ITS-sequences. Mol. Phyl. Evol. 30: 465-478.
72. Schoch C.L., Seifert K.A., Huhndorf S., Robert V., Spouge J.L., Levesque C.A., Chen W., Fungal Barcoding Consortium. 2012. Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for fungi. Proc. Natl. Acad. Sci. 109: 6241-6246.
73. Seetharam A.S., Stuart G.W. 2013. Whole genome phylogeny for 21 Drosophila species using predicted 2b-RAD fragments. PeerJ. 1:e226.
74. Smith U.E., Hendricks, J.R. 2013. Geometric morphometric character suites as phylogenetic data: Extracting phylogenetic signal from gastropod shells. Syst. Biol. 62(3):366-385.
75. Soltis D.E., Smith S.A., Cellinese N., Wurdack K.J., Tank D.C., Brockington S.F., Refulio-Rodriguez N.F., Walker J.B., Moore M.J., Carlsward B.S., Bell C.D., Latvis M., Crawley S., Black C., Diouf D., Xi Z., Rushworth C.A., Gitzendanner M.A., Sytsma K.J., Qiu Y-L., Hilu K.W., Davis C.C., Sanderson M.J., Beaman R.S., Olmstead R.G., JuddW.S., Donoghue M.J., Soltis P.S. 2011. Angiosperm phylogeny: 17 genes, 640 taxa. Am. J. Bot. 98:704-730.
76. Straub S.C.K., ParksM.,Weitemier K., Fishbein M., Cronn R.C., Liston A. 2012. Navigating the tip of the genomic iceberg: Next generation sequencing for plant systematics. Am. J. Bot. 99:349-364.
77. Tautz D., Arctander P., Minelli A., Thomas R.H., Vogler A.P. 2003. A plea for DNA taxonomy. Trends Ecol. Evol. 18:70-74.
78. Telford M.J., Copley R.R. 2011. Improving animal phylogenies with genomic data. Trends Gen. 27:186-195.
79. Timmermans M.J.T.N., Dodsworth S., Culverwell C.L., Bocak L., Ahrens D., Littlewood D.T.J., Pons J.,VoglerA.P. 2010.Why barcode? High-throughput multiplex sequencing of mitochondrial genomes for molecular systematics. Nucleic Acids Res. 38:e197.
80. Turner B., Munzinger J., Duangjai S., Temsch E.M., Stockenhuber R., Barfuss M.H.J., Chase M.W., Samuel R. 2013. Molecular phylogenetics of New Caledonian Diospyros (Ebenaceae) using plastid and nuclear markers. Mol. Phyl. Evol. 69:740-763.
81. Wagner C.E., Keller I., Wittwer S., Selz O.M., Mwaiko S., Greuter L., Sivasundar A., Seehausen O. 2012. Genome-wide RAD sequence data provide unprecedented resolution of species boundaries and relationships in the Lake Victoria cichlid adaptive radiation. Mol. Ecol. 22(3):787-798.
82. Wicker T., Sabot F., Hua-Van A., Bennetzen J.L., Capy P., Chalhoub B., Flavell A., Leroy P.,MorganteM., Panaud O., Paux E., SanMiguel P., Schulman A.H. 2007. A unified classification system for eukaryotic transposable elements. Nat. Rev. Genet. 8:973-982.
83. Will K.W., Rubinoff D. 2004. Myth of the molecule: DNA barcodes for species cannot replace morphology for identification and classification. Cladistics 20:47-55.
84. Yang Y., Hou Z.C., Qian Y.H., Kang H., Zeng Q.T. 2012. Increasing the data size to accurately reconstruct the phylogenetic relationships between nine subgroups of the Drosophila melanogaster species group (Drosophilidae, Diptera). Mol. Phyl. Evol. 62:214-223.
85. Zhou X., Xu S., Xu J., Chen B., Zhou K., Yang G. 2012. Phylogenomic analysis resolves the interordinal relationships and rapid diversification of the Laurasiatherian mammals. Syst. Biol. 61:150-164.
86. Yoder J.B., Briskine R.,Mudge J., FarmerA., Paape T., Steele K.,Weiblen G.D., Bharti A.K., Zhou P., May G.D., Young N.D., Tiffin P. 2013. Phylogenetic signal variation in the genomes of Medicago (Fabaceae). Syst. Biol. 62(3):424-438.
87. Zhang N., Zeng L., Shan H., Ma H. 2012. Highly conserved lowcopy nuclear genes as effective markers for phylogenetic analyses in angiosperms. New Phytol. 195:923-937.