Phylogenetic analysis of the plastid inverted repeat for 244 species: Insights into deeper-level Angiosperm relationships from a long, slowly evolving sequence region

International Journal of Plant Sciences

Volumn 172, Issue 4, 2011, Pages 541-558

  Moore, Michael J ^a   Hassan, Nasr ^b   Gitzendanner, Matthew A ^c   Bruenn, Riva A ^a   Croley, Matthew ^a   Vandeventer, Alexia ^c   Horn, James W ^d   Dhingra, Amit ^e   Brockington, Samuel F ^f   Latvis, Maribeth ^b   Ramdial, Jeremy ^b   Alexandre, Roolse ^b   Piedrahita, Ana ^b   Xi, Zhenxiang ^g   Davis, Charles C ^g   Soltis, Pamela S ^h   Soltis, Douglas E ^b  

^a OBERLIN COLLEGE   (United States)

^b Assiut University   (Egypt)

^c UNIVERSITY OF FLORIDA   (United States)

^d DEPARTMENT OF PALEOBIOLOGY   (United States)

^e WASHINGTON STATE UNIVERSITY   (United States)

^f UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^g HARVARD UNIVERSITY   (United States)

^h UNIVERSITY OF FLORIDA   (United States)

Author keywords

Angiosperm Tree of Life; Large data sets; Phylogenetics; Plastid inverted repeat

Indexed keywords

ANGIOSPERM; CLADISTICS; DATA SET; GENOMICS; MATRIX; PHYLOGENY; PLASTID; RESOLUTION; SAMPLING; SPECIES DIVERSITY; TAXONOMY; TOPOLOGY;

ASTERIDS; CARYOPHYLLALES; DILLENIACEAE; MAGNOLIOPHYTA; ROSIDAE; SANTALALES; SAXIFRAGALES; VITACEAE;

EID: 79955535683     PISSN: 10585893     EISSN: None     Source Type: Journal    
DOI: 10.1086/658923     Document Type: Article

References (75)

1. APG (Angiosperm Phylogeny Group) III 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. Barkman TJ, G Chenery, JR McNeal, J Lyons-Weiler, WJ Ellisens, G Moore, AD Wolfe, CW dePamphilis 2000 Independent and combined analyses of sequences from all three genomic compartments converge on the root of flowering plant phylogeny. Proc Natl Acad Sci USA 97:13166-13171.
3. Barkman TJ, JR McNeal, SH Lim, G Coat, HB Croom, ND Young, CW DePamphilis 2007 Mitochondrial DNA suggests at least 11 origins of parasitism in angiosperms and reveals genomic chimerism in parasitic plants. BMC Evol Biol 7:248.
4. Borsch T, D Quandt 2009 Mutational dynamics and phylogenetic utility of noncoding chloroplast DNA. Plant Syst Evol 282:169-199.
5. Braukmann TW, M Kuzmina, S Stefanović 2009 Loss of all plastid ndh genes in Gnetales and conifers: extent and evolutionary significance for the seed plant phylogeny. Curr Genet 55:323-337.
6. Bremer B, K Bremer, N Heidari, P Erixon, RG Olmstead, AA Anderberg, M Källersjö, E Barkhordarian 2002 Phylogenetics of asterids based on 3 coding and 3 non-coding chloroplast DNA markers and the utility of non-coding DNA at higher taxonomic levels. Mol Phylogenet Evol 24:274-301.
7. Brockington SF, R Alexandre, J Ramdial, MJ Moore, S Crawley, A Dhingra, K Hilu, DE Soltis, PS Soltis 2009 Phylogeny of the Caryophyllales sensu lato: revisiting hypotheses on pollination biology and perianth differentiation in the core Caryophyllales. Int J Plant Sci 170:627-643.
8. Bull JJ, JP Huelsenbeck, CW Cunningham, DL Swofford, PJ Waddell 1993 Partitioning and combining data in phylogenetic analysis. Syst Biol 42:384-397.
9. Burleigh JG, KW Hilu, DE Soltis 2009 Inferring phylogenies with incomplete data sets: a 5-gene, 567-taxon analysis of angiosperms. BMC Evol Biol 9:61.
10. Cai Z, M Guisinger, HG Kim, E Ruck, JC Blazier, V McMurtry, JV Kuehl, J Boore, RK Jansen 2008 Extensive reorganization of the plastid genome of Trifolium subterraneum (Fabaceae) is associated with numerous repeated sequences and novel DNA insertions. J Mol Evol 67:696-704.
11. Cai Z, C Penaflor, JV Kuehl, J Leebens-Mack, JE Carlson, CW dePamphilis, JL Boore, RK Jansen 2006 Complete plastid genome sequences of Drimys, Liriodendron, and Piper: implications for the phylogenetic relationships of magnoliids. BMC Evol Biol 6:77.
12. Cantino PD, JA Doyle, SW Graham, WS Judd, RG Olmstead, DE Soltis, PS Soltis,MJ Donoghue 2007 Towards a phylogenetic nomenclature of Tracheophyta. Taxon 56:822-846.
13. Chase MW, MF Fay, DS Devey, O Maurin, N Ronsted, TJ Davies, Y Pillon, et al 2006 Multigene analyses of monocot relationships: a summary. Aliso 22:63-75.
14. Chumley TW, JD Palmer, JP Mower, HM Fourcade, PJ Calie, JL Boore, RK Jansen 2006 The complete chloroplast genome sequence of Pelargonium × hortorum: organization and evolution of the largest and most highly rearranged chloroplast genome of land plants. Mol Biol Evol 23:2175-2190.
15. Cronn R, A Liston, M Parks, DS Gernandt, R Shen, T Mockler 2008 Multiplex sequencing of plant chloroplast genomes using Solexa sequencing-by-synthesis technology. Nucleic Acids Res 36: e122, doi:10.1093/nar/gkn502.
16. dePamphilis CW, JD Palmer 1990 Loss of photosynthetic and chlororespiratory genes from the plastid genome of a parasitic flowering plant. Nature 348:337-339.
17. Dhingra A, KM Folta 2005 ASAP: amplification, sequencing and annotation of plastomes. BMC Genomics 6:176.
18. Downie SR, JD Palmer 1992 Restriction site mapping of the chloroplast DNA inverted repeat: a molecular phylogeny of the Asteridae. Ann Mo Bot Gard 79:266-283.
19. Doyle JJ, JL Doyle 1987 A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11-15.
20. Felsenstein J 1978 Cases in which parsimony or compatibility methods will be positively misleading. Syst Zool 27:401-410.
21. Felsenstein J 1985 Confidence limits on phylogeny: an approach using the bootstrap. Evolution 39:783-791.
22. Givnish TJ, JC Pires, SW Graham, MA McPherson, LM Prince, TB Patterson, HS Rai, et al 2006 Phylogenetic relationships of monocots based on the highly informative plastid gene ndhF: evidence for widespread concerted convergence. Aliso 22:28-51.
23. Graham SW, WJD Iles 2009 Different gymnosperm outgroups have (mostly) congruent signal regarding the root of flowering plant phylogeny. Am J Bot 96:216-227.
24. Graham SW, RG Olmstead 2000 Utility of 17 chloroplast genes for inferring the phylogeny of the basal angiosperms. Am J Bot 87: 1712-1730.
25. Graham SW, PA Reeves, ACE Burns, RG Olmstead 2000 Microstructural changes in noncoding chloroplast DNA: interpretation, evolution, and utility of indels and inversions in basal angiosperm phylogenetic inference. Int J Plant Sci 161(suppl):S83-S96.
26. Graham SW, JM Zgurski, MA McPherson, DM Cherniawsky, JM Saarela, ESC Horne, SY Smith, et al 2006 Robust inference of monocot deep phylogeny using an expanded multigene plastid data set. Aliso 22:3-20.
27. Guisinger MM, JV Kuehl, JL Boore, RK Jansen 2008 Genome-wide analyses of Geraniaceae plastid DNA reveal unprecedented patterns of increased nucleotide substitutions. Proc Natl Acad Sci USA 105: 18424-18429.
28. Haberle RC, HM Fourcade, JL Boore, RK Jansen 2008 Extensive rearrangements in the chloroplast genome of Trachelium caeruleum are associated with repeats and tRNA genes. J Mol Evol 66:350-361.
29. Heath TA, SM Hedtke, DM Hillis 2008 Taxon sampling and the accuracy of phylogenetic analyses. J Syst Evol 46:239-257.
30. Hilu KW, T Borsch, K Müller, DE Soltis, PS Soltis, V Savolainen, MW Chase, et al 2003 Inference of angiosperm phylogeny based on matK sequence information. Am J Bot 90:1758-1776.
31. Jansen RK, Z Cai, LA Raubeson, H Daniell, CW DePamphilis, J Leebens-Mack, KF Müller, et al 2007 Analysis of 81 genes from 64 plastid genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns. Proc Natl Acad Sci USA 104: 19369-19374.
32. Jansen RK, MF Wojciechowski, E Sanniyasi, S-B Lee, H Daniell 2008 Complete plastid genome sequence of the chickpea (Cicer arietinum) and the phylogenetic distribution of rps12 and clpP intron losses among legumes (Leguminosae). Mol Phylogenet Evol 48:1204-1217.
33. Jeanmougin F, JD Thompson, M Gouy, DG Higgins, TJ Gibson 1998 Multiple sequence alignment with Clustal X. Trends Biochem Sci 23:403-405.
34. Jian S, PS Soltis, MA Gitzendanner, MJ Moore, R Li, TA Hendry, YL Qiu, A Dhingra, CD Bell, DE Soltis 2008 Resolving an ancient, rapid radiation in Saxifragales. Syst Biol 57:38-57.
35. Judd WS, RG Olmstead 2004 A survey of tricolpate (eudicot) phylogenetic relationships. Am J Bot 91:1627-1644.
36. Judd WS, DE Soltis, PS Soltis, PD Cantino Forthcoming Malvidae. In K de Queiroz, J Gauthier, PD Cantino, eds. Phylonyms: a companion to the PhyloCode. University of California Press, Berkeley.
37. Kelchner SA 2000 The evolution of non-coding chloroplast DNA and its application in plant systematics. Ann Mo Bot Gard 87:482-498.
38. Klopfstein S, C Kropf, DL Quicke 2010 An evaluation of phylogenetic informativeness profiles and the molecular phylogeny of Diplazontinae (Hymenoptera, Ichneumonidae). Syst Biol 59:226-241.
39. Leebens-Mack J, LA Raubeson, L Cui, JV Kuehl, MH Fourcade, TW Chumley, JL Boore, RK Jansen, CW dePamphilis 2005 Identifying the basal angiosperm node in chloroplast genome phylogenies: sampling one's way out of the Felsenstein zone. Mol Biol Evol 22: 1948-1963.
40. Li X-X, Z-K Zhou 2007 The higher-level phylogeny of monocots based on matK, rbcL, and 18S rDNA sequences. Acta Phytotaxon Sin 45:113-133.
41. Maddison WP, DR Maddison 2003 MacClade, version 4.0. Sinauer, Sunderland, MA.
42. Mathews S 2009 Phylogenetic relationships among seed plants: persistent questions and the limits of molecular data. Am J Bot 96:228-236.
43. McNeal JR, JV Kuehl, JL Boore, CW dePamphilis 2007 Complete plastid genome sequences suggest strong selection for retention of photosynthetic genes in the parasitic plant genus Cuscuta. BMC Plant Biol 7:57.
44. Moore MJ, CD Bell, PS Soltis, DE Soltis 2007 Using plastid genomescale data to resolve enigmatic relationships among basal angiosperms. Proc Natl Acad Sci USA 104:19363-19368.
45. Moore MJ, A Dhingra, PS Soltis, R Shaw, WG Farmerie, KM Folta, DE Soltis 2006 Rapid and accurate pyrosequencing of angiosperm plastid genomes. BMC Plant Biol 6:17.
46. Moore MJ, PS Soltis, CD Bell, JG Burleigh, DE Soltis 2010 Phylogenetic analysis of 83 plastid genes further resolves the early diversification of eudicots. Proc Natl Acad Sci USA 107:4623-4628.
47. Nickrent DL, JP Der, FE Anderson 2005 Discovery of the photosynthetic relatives of the "Maltese mushroom" Cynomorium. BMC Evol Biol 5:38.
48. Palmer JD 1991 Plastid chromosomes: structure and evolution. Pages 5-53 in RG Hermann, ed. Cell culture and somatic cell genetics of plants. Vol 7A. The molecular biology of plastids. Academic Press, Vienna.
49. Philippe H, Y Zhou, H Brinkmann, N Rodrigue, F Delsuc 2005 Heterotachy and long-branch attraction in phylogenetics. BMC Evol Biol 5:50.
50. Plunkett GM, SR Downie 2000 Expansion and contraction of the chloroplast inverted repeat in Apiaceae subfamily Apioideae. Syst Bot 25:648-667.
51. Qiu Y-L, L Li, TA Hendry, R Li, DW Taylor, MJ Issa, AJ Ronen, ML Vekaria, AM White 2006 Reconstructing the basal angiosperm phylogeny: evaluating information content of mitochondrial genes. Taxon 55:837-856.
52. Raubeson LA, RK Jansen 1992 A rare chloroplast-DNA structural mutation is shared by all conifers. Biochem Syst Ecol 20:17-24.
53. Raubeson LA, RK Jansen 2005 Chloroplast genomes of plants. Pages 45-68 in RJ Henry, ed. Plant diversity and evolution: genotypic and phenotypic variation in higher plants. CABI, Cambridge, MA.
54. Saarela JM, HS Rai, JA Doyle, PK Endress, S Mathews, AD Marchant, BG Briggs, SW Graham 2007 Hydatellaceae identified as a new branch near the base of the angiosperm phylogenetic tree. Nature 446:312-315.
55. Schäferhoff B, KF Müller, T Borsch 2009 Caryophyllales phylogenetics: disentangling Phytolaccaceae and Molluginaceae and description of Microteaceae as a new isolated family. Willdenowia 39: 209-228.
56. Soltis DE, MA Gitzendanner, PS Soltis 2007 A 567-taxon data set for angiosperms: the challenges posed by Bayesian analyses of large data sets. Int J Plant Sci 168:137-157.
57. Soltis DE, PS Soltis 2004 Amborella not a "basal angiosperm"? Not so fast. Am J Bot 91:997-1001.
58. Soltis DE, PS Soltis, MW Chase, ME Mort, DC Albach, M Zanis, V Savolainen, et al 2000 Angiosperm phylogeny inferred from 18S rDNA, rbcL, and atpB sequences. Bot J Linn Soc 133:381-461.
59. Soltis DE, PS Soltis, TG Collier, ML Edgerton 1991 Chloroplast DNA variation within and among genera of the Heuchera group (Saxifragaceae): evidence for chloroplast transfer and paraphyly. Am J Bot 78:1091-1112.
60. Soltis DE, PS Soltis, PK Endress, MW Chase 2005 Phylogeny and evolution of angiosperms. Sinauer, Sunderland, MA.
61. Soltis PS, SF Brockington, M-J Yoo, A Piedrahita, M Latvis, MJ Moore, AS Chanderbali, DE Soltis 2009 Floral variation and floral genetics in basal angiosperms. Am J Bot 96:110-128.
62. Stamatakis A 2006 RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690.
63. Swofford DL 2000 PAUP*: phylogenetic analysis using parsimony (*and other methods), version 4. Sinauer, Sunderland, MA.
64. Wang H, MJ Moore, PS Soltis, CD Bell, SF Brockington, R Alexandre, CC Davis, M Latvis, SR Manchester, DE Soltis 2009 Rosid radiation and the rapid rise of angiosperm-dominated forests. Proc Natl Acad Sci USA 106:3853-3858.
65. Wang RJ, CL Cheng, CC Chang, CL Wu, TM Su, SM Chaw 2008 Dynamics and evolution of the inverted repeat-large single copy junctions in the chloroplast genomes of monocots. BMC Evol Biol 8:36.
66. Wojciechowski MF, M Lavin, MJ Sanderson 2004 A phylogeny of legumes (Leguminosae) based on analysis of the plastid matK gene resolves many well-supported subclades within the family. Am J Bot 91:1846-1862.
67. Wolfe KH, WH Li, PM Sharp 1987 Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc Natl Acad Sci USA 84:9054-9058.
68. Worberg A, MH Alford, D Quandt, T Borsch 2009 Huerteales sister to Brassicales plus Malvales, and newly circumscribed to include Dipentodon, Gerrardina, Huertea, Perrottetia, and Tapiscia. Taxon 58:468-478.
69. Worberg A, D Quandt, A-M Barniske, C Löhne, KW Hilu, T Borsch 2007 Phylogeny of basal eudicots: insights from non-coding and rapidly evolving DNA. Org Divers Evol 7:55-77.
70. Wortley AH, PJ Rudall, DJ Harris, RW Scotland 2005 How much data are needed to resolve a difficult phylogeny? case study in Lamiales. Syst Biol 54:697-709.
71. Wurdack KJ, CC Davis 2009 Malpighiales phylogenetics: gaining ground on one of the most recalcitrant clades in the angiosperm tree of life. Am J Bot 96:1551-1570.
72. Wyman SK, RK Jansen, JL Boore 2004 Automatic annotation of organellar genomes with DOGMA. Bioinformatics 20:3252-3255.
73. Yang Z 1998 On the best evolutionary rate for phylogenetic analysis. Syst Biol 47:125-133.
74. ZanisMJ, DE Soltis, PS Soltis, SMathews,MJ Donoghue 2002 The root of the angiosperms revisited. Proc Natl Acad Sci USA 99:6848-6853.
75. Zhang Z-H, C-Q Li, J Li 2009 Phylogenetic placement of Cynomorium in Rosales inferrred from sequences of the inverted repeat region of the chloroplast genome. J Syst Evol 47:297-304.