A comparative analysis of whole plastid genomes from the apiales: Expansion and contraction of the inverted repeat, mitochondrial to plastid transfer of DNA, and identification of highly divergent noncoding regions

Systematic Botany

Volumn 40, Issue 1, 2015, Pages 336-351

  Downie, Stephen R ^a   Jansen, Robert K ^b,c  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^c KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

Author keywords

Apiaceae; Araliaceae; intergenic spacer regions; intracellular transfer; plastid DNA

Indexed keywords

ANTHRISCUS CEREFOLIUM; APIACEAE; APIALES; ARALIACEAE; CRITHMUM; CRITHMUM MARITIMUM; DAUCUS CAROTA SUBSP. SATIVUS; HYDROCOTYLE VERTICILLATA; MAGNOLIOPHYTA; PANAX; PETROSELINUM; PETROSELINUM CRISPUM;

EID: 84923336928     PISSN: 03636445     EISSN: 15482324     Source Type: Journal    
DOI: 10.1600/036364415X686620     Document Type: Article

References (107)

1. Aii, J., Y. Kishima, T. Mikami, and T. Adachi. 1997. Expansion of the IR in the chloroplast genomes of buckwheat species is due to incorporation of an SSC sequence that could be mediated by an inversion. Current Genetics 31: 276-279
2. Aldrich, J., B. W. Cherney, E. Merlin, and L. Christopherson. 1988. The role of insertions/deletions in the evolution of the intergenic region between psbA and trnH in the chloroplast genome. Current Genetics 14: 137-146
3. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. Journal of Molecular Biology 215: 403-410
4. Bach, I. C., A. Olesen, and P. W. Simon. 2002. PCR-based markers to differentiate the mitochondrial genomes of petaloid and male fertile carrot (Daucus carota L.). Euphytica 127: 353-365
5. Banasiak, , M. Piwczynski, T. Ulinski, S. R. Downie, M. F. Watson, B. Shakya, and K. Spalik. 2013. Dispersal patterns in space and time: a case study of Apiaceae subfamily Apioideae. Journal of Biogeography 40: 1324-1335
6. Bergthorsson, U., K. L. Adams, B. Thomason, and J. D. Palmer. 2003. Widespread horizontal transfer of mitochondrial genes in flowering plants. Nature 424: 197-201
7. Bergthorsson, U., A. O. Richardson, G. J. Young, L. R. Goertzen, and J. D. Palmer. 2004. Massive horizontal transfer of mitochondrial genes from diverse land plant donors to the basal angiosperm Amborella. Proceedings of the National Academy of Sciences USA 101: 17747-17752
8. Bock, R. 2010. The give-And-Take of DNA: horizontal gene transfer in plants. Trends in Plant Science 15: 11-22
9. Bock, R. and J. N. Timmis. 2008. Reconstructing evolution: gene transfer from plastids to the nucleus. BioEssays 30: 556-566
10. Boudreau, E. and M. Turmel. 1995. Gene rearrangements in Chlamydomonas chloroplast DNAs are accounted for by inversions and by the expansion/contraction of the inverted repeat. Plant Molecular Biology 27: 351-364
11. Cai, Z., M. Guisinger, H. G. Kim, E. Ruck, J. C. Blazier, V. McMurtry, J. V. Kuehl, J. Boore, and R. K. Jansen. 2008. Extensive reorganization of the plastid genome of Trifolium subterraneum (Fabaceae) is associated with numerous repeated sequences and novel DNA insertions. Journal of Molecular Evolution 67: 696-704
12. Cai, Z., C. Penaflor, J. V. Kuehl, J. Leebens-Mack, J. E. Carlson, C. W. dePamphilis, J. L. Boore, and R. K. Jansen. 2006. Complete plastid genome sequences of Drimys, Liriodendron, and Piper: implications for the phylogenetic relationships of magnoliids. BMC Evolutionary Biology 6: 77
13. Calviño, C. I. and S. R. Downie. 2007. Circumscription and phylogeny of Apiaceae subfamily Saniculoideae based on chloroplast DNA sequences. Molecular Phylogenetics and Evolution 44: 175-191
14. Chevreux, B., T. Pfisterer, and S. Suhai. 2000. Automatic assembly and editing of genomic sequences. In: Suhai S. (ed), Genomics and proteomics-functional and computational aspects. New York: Kluwer Academic/Plenum Publishers
15. Chumley, T. W., J. D. Palmer, J. P. Mower, H. M. Fourcade, P. J. Calie, J. L. Boore, and R. K. 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. Molecular Biology and Evolution 23: 2175-2190
16. Cordes, J. M. 2009. A systematic study of poison hemlock (Conium, Apiaceae). M. S. thesis. Urbana, Illinois: University of Illinois at Urbana-Champaign
17. Cosner, M. E., R. K. Jansen, J. D. Palmer, and S. R. Downie. 1997. The highly rearranged chloroplast genome of Trachelium caeruleum (Campanulaceae): multiple inversions, inverted repeat expansion and contraction, transposition, insertions/deletions, and several repeat families. Current Genetics 31: 419-429
18. Danderson, C. A. 2011. A phylogenetic study of the Arracacia clade (Apiaceae). Ph. D. thesis. Urbana, Illinois: University of Illinois at Urbana-Champaign
19. Degtjareva, G. V., E. V. Kljuykov, T. H. Samigullin, C. M. Valiejo-Roman, and M. G. Pimenov. 2009. Molecular appraisal of Bunium and some related arid and subarid geophilic Apiaceae-Apioideae taxa of the ancient Mediterranean. Botanical Journal of the Linnean Society 160: 149-170
20. Degtjareva, G. V., M. D. Logacheva, T. H. Samigullin, E. I. Terentieva, and C. M. Valiejo-Roman. 2012. Organization of chloroplast psbA-TrnH intergenic spacer in dicotyledonous angiosperms of the family Umbelliferae. Biochemistry (Moscow) 77: 1056-1064
21. Downie, S. R. and D. S. Katz-Downie. 1999. Phylogenetic analysis of chloroplast rps16 intron sequences reveals relationships within the woody southern African Apiaceae subfamily Apioideae. Canadian Journal of Botany 77: 1120-1135
22. Downie, S. R. and J. D. Palmer. 1992. Use of chloroplast DNA rearrangements in reconstructing plant phylogeny. Pp. 14-35 in Molecular Systematics of Plants, eds. P. S. Soltis, D. E. Soltis, and J. J. Doyle. New York: Chapman and Hall
23. Downie, S. R., D. S. Katz-Downie, and K.-J. Cho. 1996. Phylogenetic analysis of Apiaceae subfamily Apioideae using nucleotide sequences from the chloroplast rpoC1 intron. Molecular Phylogenetics and Evolution 6: 1-18
24. Downie, S. R., D. S. Katz-Downie, and M. F. Watson. 2000. A phylogeny of the flowering plant family Apiaceae based on chloroplast DNA rpl16 and rpoC1 intron sequences: towards a suprageneric classification of subfamily Apioideae. American Journal of Botany 87: 273-292
25. Downie, S. R., D. S. Katz-Downie, F.-J. Sun, and C.-S. Lee. 2008. Phylogeny and biogeography of Apiaceae tribe Oenantheae inferred from nuclear rDNA ITS and cpDNA psbI-50trnK(UUU) sequences, with emphasis on theNorth American endemics clade. Botany 86: 1039-1064
26. Downie, S. R., G. M. Plunkett, M. F. Watson, K. Spalik, D. S. Katz-Downie, C. M. Valiejo-Roman, E. I. Terentieva, A. V. Troitsky, B.-Y. Lee, J. Lahham, and A. El-Oqlah. 2001. Tribes and clades within Apiaceae subfamily Apioideae: the contribution of molecular data. Edinburgh Journal of Botany 58: 301-330
27. Downie, S. R., R. G. Olmstead, G. Zurawski, D. E. Soltis, P. S. Soltis, J. C. Watson, and J. D. Palmer. 1991. Six independent losses of the chloroplast DNA rpl2 intron in dicotyledons: molecular and phylogenetic implications. Evolution 45: 1245-1259
28. Downie, S. R., K. Spalik, D. S. Katz-Downie, and J.-P. Reduron. 2010. Major clades within Apiaceae subfamily Apioideae as inferred by phylogenetic analysis of nrDNA ITS sequences. Plant Diversity and Evolution 128: 111-136
29. Feist, M. A. E., S. R. Downie, A. R. Magee, and M. Liu. 2012. Revised generic delimitations for Oxypolis and Ptilimnium (Apiaceae) based on leaf morphology, comparative fruit anatomy, and phylogenetic analysis of nuclear rDNA ITS and cpDNA trnQ-TrnK intergeneric spacer sequence data. Taxon 61: 402-418
30. Goulding, S. E., R. G. Olmstead, C. W. Morden, and K. H. Wolfe. 1996. Ebb and flow of the chloroplast inverted repeat. Molecular & General Genetics 252: 195-206
31. Goremykin, V. V., F. Salamini, R. Velasco, and R. Viola. 2009. Mitochondrial DNA of Vitis vinifera and the issue of rampant horizontal gene transfer. Molecular Biology and Evolution 26: 99-110
32. Guisinger, M. M., T. W. Chumley, J. V. Kuehl, J. L. Boore, and R. K. Jansen. 2010. Implications of the plastid genome sequence of Typha (Typhaceae, Poales) for understanding genome evolution in Poaceae. Journal of Molecular Evolution 70: 149-166
33. Guisinger, M. M., J. V. Kuehl, J. L. Boore, and R. K. Jansen. 2011. Extreme reconfiguration of plastid genomes in the angiosperm family Geraniaceae: rearrangements, repeats, and codon usage. Molecular Biology and Evolution 28: 583-600
34. Haberle, R. C., H. M. Fourcade, J. L. Boore, and R. K. Jansen. 2008. Extensive rearrangements in the chloroplast genome of Trachelium caeruleum are associated with repeats and tRNA genes. Journal of Molecular Evolution 66: 350-361
35. Hansen, D. R., S. G. Dastidar, Z. Cai, C. Penaflor, J. V. Kuehl, J. L. Boore, and R. K. Jansen. 2007. Phylogenetic and evolutionary implications of complete genome sequences of four early-diverging angiosperms: Buxus (Buxaceae), Chloranthus (Chloranthaceae), Dioscorea (Dioscoreaceae), and Illicium (Schisandraceae). Molecular Phylogenetics and Evolution 45: 547-563
36. Hoot, S. B. and J. D. Palmer. 1994. Structural rearrangements, including parallel inversions, within the chloroplast genome of Anemone and related genera. Journal of Molecular Evolution 38: 274-281
37. Iorizzo, M., D. Grzebelus, D. Senalik, M. Szklarczyk, D. Spooner, and P. Simon. 2012a. Against the traffic: The first evidence for mitochondrial DNA transfer into the plastid genome. Mobile Genetic Elements 2: 261-266
38. Iorizzo, M., D. Senalik, M. Szklarczyk, D. Grzebelus, D. Spooner, and P. Simon. 2012b. De novo assembly of the carrot mitochondrial genome using next generation sequencing of whole genomic DNA provides first evidence of DNA transfer into an angiosperm plastid genome. BMC Plant Biology 12: 61
39. Jansen, R. K., L. A. Raubeson, J. L. Boore, C. W. dePamphilis, T. W. Chumley, R. C. Haberle, S. K. Wyman, A. J. Alverson, R. Peery, S. J. Herman, H. M. Fourcade, J. V. Kuehl, J. R. McNeal, J. Leebens-Mack, and L. Cui. 2005. Methods for obtaining and analyzing whole chloroplast genome sequences. Methods in Enzymology 395: 348-384
40. Jansen, R. K. and T. A. Ruhlman. 2012. Plastid genomes of seed plants. Pp. 103-126 in Genomics of chloroplasts and mitochondria, advances in photosynthesis and respiration, eds. R. Bock and V. Knoop. Dordrecht: Springer
41. Jeanmougin, F., J. D. Thompson, M. Gouy, D. G. Higgins, and T. J. Gibson. 1998. Multiple sequence alignment with ClustalX. Trends in Biochemical Sciences 23: 403-405
42. Johansson, J. T. 1998. Chloroplast DNA restriction site mapping and the phylogeny of Ranunculus (Ranunculaceae). Plant Systematics and Evolution 213: 1-19
43. Johansson, J. T. and R. K. Jansen. 1993. Chloroplast DNA variation and phylogeny of the Ranunculaceae. Plant Systematics and Evolution 187: 29-49
44. Kelchner, S. A. 2002. Group II introns as phylogenetic tools: structure, function, and evolutionary constraints. American Journal of Botany 89: 1651-1669
45. Kim, Y.-D. and R. K. Jansen. 1994. Characterization and phylogenetic distribution of a chloroplast DNA rearrangement in the Berberidaceae. Plant Systematics and Evolution 193: 107-114
46. Kim, K.-J. and H.-L. Lee. 2004. Complete chloroplast genome sequences from Korean ginseng (Panax schinseng Nees) and comparative analysis of sequence evolution among 17 vascular plants. DNA Research 11: 247-261
47. Kleine, T., U. G. Maier, and D. Leister. 2009. DNA transfer from organelles to the nucleus: the idiosyncratic genetics of endosymbiosis. Annual Review of Plant Biology 60: 115-138
48. Knoop, V. 2004. The mitochondrial DNA of land plants: peculiarities in phylogenetic perspective. Current Genetics 46: 123-139
49. Knox, E. B. and J. D. Palmer. 1999. The chloroplast genome arrangement of Lobelia thuliniana (Lobeliaceae): expansion of the inverted repeat in an ancestor of the Campanulales. Plant Systematics and Evolution 214: 49-64
50. Kress, W. J., K. J. Wurdack, E. A. Zimmer, L. A. Weigt, and D. H. Janzen. 2005. Use of DNA barcodes to identify flowering plants. Proceedings of the National Academy of Sciences USA 102: 8369-8374
51. Ku, C., W.-C. Chung, L.-L. Chen, and C.-H. Kuo. 2013. The complete plastid genome sequence of Madagascar periwinkle Catharanthus roseus (L.) G. Don: plastid genome evolution, molecular marker identification, and phylogenetic implications in asterids. PLoS ONE 8: e68518
52. Kubo, T. and T. Mikami. 2007. Organization and variation of angiosperm mitochondrial genome. Physiologia Plantarum 129: 6-13
53. Kurtz, S. and C. Schleiermacher. 1999. REPuter: fast computation of maximal repeats in complete genomes. Bioinformatics 15: 426-427
54. Lee, B.-Y. and S. R. Downie. 2000. Phylogenetic analysis of cpDNA restriction sites and rps16 intron sequences reveals relationships among Apiaceae tribes Caucalideae, Scandiceae and related taxa. Plant Systematics and Evolution 221: 35-60
55. Lee, B.-Y., G. A. Levin, and S. R. Downie. 2001. Relationships within the spiny-fruited umbellifers (Scandiceae subtribes Daucinae and Torilidinae) as assessed by phylogenetic analysis of morphological characters. Systematic Botany 26: 622-642
56. Liao, C., S. R. Downie, Q. Li, Y. Yu, X. He, and B. Zhou. 2013. New insights into the phylogeny of Angelica and its allies (Apiaceae) with emphasis on East Asian species, inferred from nrDNA, cpDNA, and morphological evidence. Systematic Botany 38: 266-281
57. Logacheva, M. D., C. M. Valiejo-Roman, and M. G. Pimenov. 2008. ITS phylogeny of West Asian Heracleum species and related taxa of Umbelliferae-Tordylieae W. D. J. Koch, with notes on evolution of their psbA-TrnH sequences. Plant Systematics and Evolution 270: 139-157
58. Lohse, M., O. Drechsel, and R. Bock. 2007. OrganellarGenomeDRAW (OGDRAW): a tool for the easy generation of high-quality custom graphical maps of plastid and mitochondrial genomes. Current Genetics 52: 267-274
59. Lowe, T. M. and S. R. Eddy. 1997. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Research 25: 955-964
60. Magee, A. R., B.-E. van Wyk, P. M. Tilney, and S. R. Downie. 2010. Phylogenetic position of African and Malagasy Pimpinella species and related genera (Apiaceae, Pimpinelleae). Plant Systematics and Evolution 288: 201-211
61. Mardanov, A. V., N. V. Ravin, B. B. Kuznetsov, T. H. Samigullin, A. S. Antonov, T. V. Kolganova, and K. G. Skyabin. 2008. Complete sequence of the duckweed (Lemna minor) chloroplast genome: structural organization and phylogenetic relationships to other angiosperms. Journal of Molecular Evolution 66: 555-564
62. Michel, F., K. Umesono, and H. Ozeki. 1989. Comparative and functional anatomy of group II catalytic introns-A review. Gene 82: 5-30
63. Moore, M. J., A. Dhingra, P. S. Soltis, R. Shaw, W. G. Farmerie, K. M. Folta, and D. E. Soltis. 2006. Rapid and accurate pyrosequencing of angiosperm plastid genomes. BMC Plant Biology 6: 17
64. Mower, J. P., S. Stefanovic, W. Hao, J. S. Gummow, K. Jain, D. Ahmed, and J. D. Palmer. 2010. Horizontal acquisition of multiple mitochondrial genes from a parasitic plant followed by gene conversion with host mitochondrial genes. BMC Biology 8: 150
65. Nicolas, A. N. and G. M. Plunkett. 2009. The demise of subfamily Hydrocotyloideae (Apiaceae) and the re-Alignment of its genera across the entire order Apiales. Molecular Phylogenetics and Evolution 53: 134-151
66. Palmer, J. D. 1983. Chloroplast DNA exists in two orientations. Nature 301: 92-93
67. Palmer, J. D. 1985a. Comparative organization of chloroplast genomes. Annual Review of Genetics 19: 325-354
68. Palmer, J. D. 1985b. Evolution of chloroplast and mitochondrial DNA in plants and algae. Pp. 131-240 in Monographs in evolutionary biology: Molecular evolutionary genetics, Chapter 3, ed. R. J. MacIntyre. New York: Plenum Publishing Corporation
69. Palmer, J. D. 1986. Isolation and structural analysis of chloroplast DNA. Methods in Enzymology 118: 167-186
70. Palmer, J. D. 1990. Contrasting modes and tempos of genome evolution in land plant organelles. Trends in Genetics 6: 115-120
71. Palmer, J. D. 1991. Plastid chromosomes: structure and evolution. Pp. 5-53 in Cell culture and somatic cell genetics of plants, Vol. 7A, eds. L. Bogorad and I. K. Vasil. San Diego: Academic Press
72. Perry, A. S. and K. H. Wolfe. 2002. Nucleotide substitution rates in legume chloroplast DNA depend on the presence of the inverted repeat. Journal of Molecular Evolution 55: 501-508
73. Perry, A. S., S. Brennan, D. J. Murphy, T. A. Kavanagh, and K. H. Wolfe. 2002. Evolutionary re-organization of a large operon in adzuki bean chloroplast DNA caused by inverted repeat movement. DNA Research 9: 157-162
74. Peery, R., J. V. Kuehl, J. L. Boore, and L. Raubeson. 2006. Comparisons of three Apiaceae chloroplast genomes-coriander, dill and fennel. Abstract, Botany 2006 Meeting
75. Peery, R., S. R. Downie, J. V. Kuehl, J. L. Boore, and L. Raubeson. 2007. Chloroplast genome evolution in Apiaceae. Abstract, Botany 2007 Meeting
76. Peery, R., S. R. Downie, R. K. Jansen, and L. A. Raubeson. 2011. Apiaceae organellar genomes. XVIII International Botanical Congress Abstract Book, p. 481
77. Plunkett, G. M., D. E. Soltis, and P. S. Soltis. 1996a. Higher level relationships of Apiales (Apiaceae and Araliaceae) based on phylogenetic analysis of rbcL sequences. American Journal of Botany 83: 499-515
78. Plunkett, G. M., D. E. Soltis, and P. S. Soltis. 1996b. Evolutionary patterns in Apiaceae: inferences based on matK sequence data. Systematic Botany 21: 477-495
79. Plunkett, G. M. and S. R. Downie. 1999. Major lineages within Apiaceae subfamily Apioideae: a comparison of chloroplast restriction site and DNA sequence data. American Journal of Botany 86: 1014-1026
80. Plunkett, G. M. and S. R. Downie. 2000. Expansion and contraction of the chloroplast inverted repeat in Apiaceae subfamily Apioideae. Systematic Botany 25: 648-667
81. Raubeson, L. A. and R. K. Jansen. 2005. Chloroplast genomes of plants. Pp. 45-68 in Plant diversity and evolution: Genotypic and phenotypic variation in higher plants, ed. R. J. Henry. London: CAB International
82. Raubeson, L. A., R. Peery, T. W. Chumley, C. Dziubek, H. M. Fourcade, J. L. Boore, and R. K. Jansen. 2007. Comparative chloroplast genomics: analyses including new sequences from the angiosperms Nuphar advena and Ranunculus macranthus. BMC Genomics 8: 174
83. Rice, D. W. and J. D. Palmer. 2006. An exceptional horizontal gene transfer in plastids: gene replacement by a distant bacterial paralog and evidence that haptophyte and cryptophyte plastids are sisters. BMC Biology 4: 31
84. Richardson, A. O. and J. D. Palmer. 2007. Horizontal gene transfer in plants. Journal of Experimental Botany 58: 1-9
85. Ruhlman, T. A. and R. K. Jansen. 2014. The plastid genomes of flowering plants. Pp. 3-38 in Chloroplast Biotechnology: Methods and Protocols, ed. P. Maliga. New York: Springer
86. Ruhlman, T., S.-B. Lee, R. K. Jansen, J. B. Hostetler, L. J. Tallon, C. D. Town, and H. Daniell. 2006. Complete plastid genome sequence of Daucus carota: implications for biotechnology and phylogeny of angiosperms. BMC Genomics 7: 222
87. Schattner, P., A. N. Brooks, and T. M. Lowe. 2005. The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Research 33: W686-W689
88. Schwartz, S., L. Elnitski, M. Li, M. Weirauch, C. Riemer, A. Smit, NISC Comparative Sequencing Program, E. D. Green, R. C. Hardison, and W. Miller. 2003. MultiPipMaker and supporting tools: alignments and analysis of multiple genomic DNA sequences. Nucleic Acids Research 31: 3518-3524
89. Shaw, J., E. B. Lickey, J. T. Beck, S. B. Farmer, W. Liu, J. Miller, K. C. Siripun, C. T. Winder, E. E. Schilling, and R. L. Small. 2005. The tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. American Journal of Botany 92: 142-166
90. Shaw, J., E. B. Lickey, E. E. Schilling, and R. L. Small. 2007. Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III. American Journal of Botany 94: 275-288
91. Sheveleva, E. V. and R. B. Hallick. 2004. Recent horizontal intron transfer to a chloroplast genome. Nucleic Acids Research 32: 803-810
92. Shinozaki, K., M. Ohme, M. Tanaka, T. Wakasugi, N. Hayshida, T. Matsubayashi, N. Zaita, J. Chunwongse, J. Obokata, K. Yamaguchi-Shinozaki, C. Ohto, K. Torazawa, B. Y. Meng, M. Sugita, H. Deno, T. Kamogashira, K. Yamada, J. Kusuda, F. Takaiwa, A. Kato, N. Tohdoh, H. Shimada, and M. Sugiura. 1986. The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. The EMBO Journal 5: 2043-2049
93. Smith, D. R. 2011. Extending the limited transfer window hypothesis to inter-organelle DNA migration. Genome Biology and Evolution 3: 743-748
94. Straub, S. C. K., R. C. Cronn, C. Edwards, M. Fishbein, and A. Liston. 2013. Horizontal transfer of DNA from the mitochondrial to the plastid genome and its subsequent evolution in milkweeds (Apocynaceae). Genome Biology and Evolution 5: 1872-1885
95. Sun, F.-J., S. R. Downie, and R. L. Hartman. 2004. An ITS-based phylogenetic analysis of the perennial, endemic Apiaceae subfamily Apioideae of western North America. Systematic Botany 29: 419-431
96. Sun, F.-J. and S. R. Downie. 2010. Phylogenetic relationships among the perennial, endemic Apiaceae subfamily Apioideae of western North America: Additional data from the cpDNA trnF-TrnL-TrnT region continue to support a highly polyphyletic Cymopterus. Plant Diversity and Evolution 128: 151-172
97. Swofford, D. L. 2002. PAUP: Phylogenetic analysis using parsimony (and other methods), v. 4.0 beta 10. Sunderland: Sinauer Associates
98. Timme, R. E., J. V. Kuehl, J. L. Boore, and R. K. Jansen. 2007. A comparative analysis of the Lactuca and Helianthus (Asteraceae) plastid genomes: identification of divergent regions and categorization of shared repeats. American Journal of Botany 94: 302-312
99. Wang, R. J., C. L. Cheng, C. C. Chang, C. L. Wu, T. M. Su, and S. M. Chaw. 2008. Dynamics and evolution of the inverted repeat-large single copy junctions in the chloroplast genomes of monocots. BMC Evolutionary Biology 8: 36
100. Wang, W. and J. Messing. 2011. High-Throughput sequencing of three Lemnoideae (duckweeds) chloroplast genomes from total DNA. PLoS ONE 6: e24670
101. Weng, M.-L., J. C. Blazier, M. Govindu, and R. K. Jansen. 2014. Reconstruction of the ancestral plastid genome in Geraniaceae reveals a correlation between genome rearrangements, repeats and nucleotide substitution rates. Molecular Biology and Evolution, doi: 10.1093/ molbev/mst257
102. Wicke, S., G. M. Schneeweiss, C. W. dePamphilis, K. F. Müller, and D. Quandt. 2011. The evolution of the plastid chromosome in land plants: gene content, gene order, gene function. Plant Molecular Biology 76: 273-297
103. Wolfe, K. H., W.-H. Li, and P. M. Sharp. 1987. Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proceedings of the National Academy of Sciences USA 84: 9054-9058
104. Wyman, S. K., R. K. Jansen, and J. L. Boore. 2004. Automatic annotation of organellar genomes with DOGMA. Bioinformatics 20: 3252-3255
105. Yi, D.-K., H.-L. Lee, B.-Y. Sun, M.-Y. Chung, and K.-J. Kim. 2012. The complete chloroplast DNA sequence of Eleutherococcus senticosus (Araliaceae); Comparative evolutionary analyses with other three asterids. Molecules and Cells 33: 497-508
106. Yu, Y., S. R. Downie, X. He, X. Deng, and L. Yan. 2011. Phylogeny and biogeography of Chinese Heracleum (Apiaceae tribe Tordylieae) with comments on their fruit morphology. Plant Systematics and Evolution 296: 179-203
107. Yukawa, M., T. Tsudzuki, and M. Sugiura. 2005. The 2005 version of the chloroplast DNA sequence from tobacco (Nicotiana tabacum). Plant Molecular Biology Reporter 23: 359-365