Molecular phylogenetics and taxonomy of the genus boechera and related genera (Brassicaceae: Boechereae)

Systematic Botany

Volumn 38, Issue 1, 2013, Pages 192-209

  Alexander, Patrick J ^a   Windham, Michael D ^b   Beck, James B ^b   Al Shehbaz, Ihsan A ^c   Allphin, Loreen ^d   Bailey, C Donovan ^a  

^a NEW MEXICO STATE UNIVERSITY   (United States)

^b DUKE UNIVERSITY   (United States)

^c MISSOURI BOTANICAL GARDEN   (United States)

^d BRIGHAM YOUNG UNIVERSITY   (United States)

Author keywords

Borodinia; cytonuclear incongruence; hybrid speciation; low copy nuclear loci; molecular systematics; Yosemitea

Indexed keywords

EID: 84874543002     PISSN: 03636445     EISSN: 15482324     Source Type: Journal    
DOI: 10.1600/036364413X661917     Document Type: Article

References (91)

1. Al-Shehbaz, I. A. 2003. Transfer of most North American species of Arabis to Boechera (Brassicaceae). Novon 13: 381-391. (Pubitemid 38024801)
2. Al-Shehbaz, I. A., M. A. Beilstein, and E. A. Kellogg. 2006. Systematics and phylogeny of the Brassicaceae (Cruciferae): an overview. Plant Systematics and Evolution 259: 89-120. (Pubitemid 44048122)
3. Al-Shehbaz, I. A. and M. D. Windham. 2010. Boechera. Pp. 347-412 in Flora of North America north of Mexico Vol 7., eds. Flora of North America Committee. New York and Oxford: Oxford University Press.
4. Alexander, P. J., G. Rajanikanth, C. D. Bacon, and C. D. Bailey. 2007. Rapid inexpensive recovery of high quality plant DNA using a reciprocating saw and silica-based columns. Molecular Ecology Notes 7: 5-9. (Pubitemid 46046570)
5. Aliyu, O. M., M. E. Schranz, and T. F. Sharbel. 2010. Quantitative variation for apomictic reproduction in the genus Boechera (Brassicaceae). American Journal of Botany 91: 1719-1731.
6. Bailey, C. D. and J. J. Doyle. 1999. Potential phylogenetic utility of the low-copy nuclear gene pistillata in dicotyledonous plants: comparison to nrDNA ITS and trnL intron in Sphaerocardamum and other Brassicaceae. Molecular Phylogenetics and Evolution 13: 20-30. (Pubitemid 129499316)
7. Bailey, C. D., M. Koch, M. S. Mayer, K. Mummenhoff, S. L. O'Kane Jr., S. I. Warwick, M. D. Windham, and I. A. Al-Shehbaz. 2006. Toward a global phylogeny of the Brassicaceae. Molecular Biology and Evolution 23: 2142-2160. (Pubitemid 44536823)
8. Beck, J. B., P. J. Alexander, L. Allphin, I. A. Al-Shehbaz, C. Rushworth, C. D. Bailey, and M. D.Windham. 2012. Does hybridization drive the transition to asexuality in diploid Boechera? Evolution 66: 985-995.
9. Beilstein, M. A., I. A. Al-Shehbaz, and E. A. Kellogg. 2006. Brassicaceae phylogeny and trichome evolution. American Journal of Botany 93: 607-619.
10. Beilstein, M. A., I. A. Al-Shehbaz, S. Mathews, and E. A. Kellogg. 2008. Brassicaceae phylogeny inferred from phytochrome A and ndhF sequence data: tribes and trichomes revisited. American Journal of Botany 95: 1307-1327.
11. Birky, C. W. Jr., T. Maruyama, and P. Fuerst. 1983. An approach to population and evolutionary genetic theory for genes in mitochondria and chloroplasts, and some results. Genetics 103: 513-527. (Pubitemid 13125930)
12. Bishop, J. G., A. M. Dean, and T. Mitchell-Olds. 2000. Rapid evolution in plant chitinases: Molecular targets of selection in plant-pathogen coevolution. Evolution 97: 5322-5327. (Pubitemid 30313717)
13. Bloom, C. T., C. C. Baskin, and J. M. Baskin. 1990. Germination ecology of the facultative biennial Arabis laevigata variety laevigata. American Midland Naturalist 124: 214-230.
14. Bloom, T. C., J. M. Baskin, and C. C. Baskin. 2001. Ecological life history of the facultative woodland biennial Arabis laevigata var. laevigata (Brassicaceae): survivorship. The Journal of the Torrey Botanical Society 128: 93-108. (Pubitemid 32818327)
15. Böcher, T. W. 1951. Cytological and embryological studies in the amphiapomictic Arabis holboellii complex. Biologiske Skrifter Kongelige Danske Videnskabernes Selskab 6: 1-59.
16. Böcher, T. W. 1954. Experimental taxonomic studies in the Arabis holboellii complex. Svensk Botanisk Tidskrift 48: 31-44.
17. Böcher, T. W. 1969. Further studies in the Arabis holboellii complex. Botanisk Tidsskrift 64: 141-161.
18. Boufford, D. E. and S. A. Spongberg. 1983. Eastern Asian-eastern North American phytogeographical relationships-a history from the time of Linnaeus to the twentieth century. Annals of the Missouri Botanical Garden 70: 423-439.
19. Bruyns, P. V., R. J. Mapaya, and T. J. Hedderson. 2006. A new subgeneric classification for Euphorbia (Euphorbiaceae) in southern Africa based on ITS and psbA-trnH sequence data. Taxon 55: 397-420. (Pubitemid 44030926)
20. Chan, K. M. A. and S. A. Levin. 2005. Leaky prezygotic isolation and porous genomes: rapid introgression of maternally inherited DNA. Evolution 59: 720-729. (Pubitemid 40589284)
21. Dobes, C., C. Kiefer, M. Kiefer, and M. A. Koch. 2007a. Plastidic trnFUUC pseudogenes in North American genus Boechera (Brassicaceae): Mechanistic aspects of evolution. Plant Biology 9: 502-515. (Pubitemid 47264664)
22. Dobes, C., M. Koch, and T. Sharbel. 2006. Embryology, karyology, and modes of reproduction in the North American genus Boechera (Brassicaceae): a compilation of seven decades of research. Annals of the Missouri Botanical Garden 93: 517-533.
23. Dobes, C., T. Mitchell-Olds, and M. A. Koch. 2004a. Intraspecific diversification in North American Boechera stricta (=Arabis drummondii), Boechera + divaricarpa, and Boechera holboellii (Brassicaceae) inferred from nuclear and chloroplast markers-an integrative approach. American Journal of Botany 91: 2087-2101. (Pubitemid 43193709)
24. Dobes, C. H., T. Mitchell-Olds, and M. A. Koch. 2004b. Extensive chloroplast haplotype variation indicates Pleistocene hybridization and radiation of North American Arabis drummondii, A. + divaricarpa, and A. holboellii (Brassicaceae). Molecular Ecology 13: 349-370. (Pubitemid 38143379)
25. Dobes, C., T. F. Sharbel, and M. Koch. 2007b. Towards understanding the dynamics of hybridization and apomixis in the evolution of the genus Boechera (Brassicaceae). Systematics and Biodiversity 5: 321-331. (Pubitemid 47172734)
26. Dorn, R. 2001. Vascular plants of Wyoming, ed. 3. Cheyenne: Mountain West Publishing.
27. Goloboff, P. A. 1999. Analyzing large data sets in reasonable times: solutions for composite optima. Cladistics 15: 415-428. (Pubitemid 30203168)
28. Goloboff, P. A. 2000. NONA (NO NAME) ver. 2. Tucumán: Published by the author.
29. Goloboff, P. A., J. S. Farris, and K. C. Nixon. 2008. TNT, a free program for phylogenetic analysis. Cladistics 24: 774-786.
30. Hedtke, S. M. and D. M. Hillis. 2011. The potential role of androgenesis in cytoplasmic-nuclear phylogenetic discordance. Systematic Biology 60: 87-109.
31. Holmgren, N. H. 2005. Brassicaceae. Pp. 174-418 in Intermountain Flora: Vascular plants of the Intermountain West, Vol. 2, part B, eds. N. H. Holmgren, P. K.Holmgren, and A. Cronquist. Bronx: New York Botanical Garden Press.
32. Hopkins, M. L. 1937. Arabis in eastern and central North America. Rhodora 39: 63-98, 106-148, 155-186.
33. Jordon-Thaden, I., I. Hase, I. A. Al-Shehbaz, and M. A. Koch. 2010. Molecular phylogeny and systematics of the genus Draba (Brassicaceae) and identification of its most closely related genera. Molecular Phylogenetics and Evolution 55: 524-540.
34. Kantama, L., T. F. Sharbel,M. E. Schranz, T. Mitchell-Olds, S. de Vries, and H. de Jong. 2007. Diploid apomicts of the Boechera holboellii complex display large-scale chromosome substitutions and aberrant chromosomes. Proceedings of the National Academy of Sciences USA 104: 14026-14031. (Pubitemid 350003329)
35. Kartesz, J. T. and The Biota of North America Program (BONAP). 2011. North American plant atlas. Chapel Hill, North Carolina URL: http://www.bonap.org/MapSwitchboard.html [accessed January 2011].
36. Kiefer, C., C. Dobes, and M. A. Koch. 2009a. Boechera or not? Phylogeny and phylogeography of eastern North American Boechera species (Brassicaceae). Taxon 58: 1109-1121.
37. Kiefer, C., C. Dobes, T. F. Sharbel, and M. A. Koch. 2009b. Phylogeographic structure of the chloroplast DNA gene pool in North American Boechera-A genus and continental-wide perspective. Molecular Phylogenetics and Evolution 52: 303-311.
38. Knight, C. A., H. Vogel, J. Kroymann, A. Shumate, H. Witsenboer, and T. Mitchell-Olds. 2006. Expression profiling and local adaptation of Boechera holboellii populations for water use efficiency across a naturally occurring water stress gradient. Molecular Ecology 15: 1229-1237.
39. Koch, M. A., J. Bishop, and T. Mitchell-Olds. 1999. Molecular systematics and evolution of Arabidopsis and Arabis. Plant Biology 1: 529-537. (Pubitemid 29514361)
40. Koch, M. A., C. Dobes, and T. Mitchell-Olds. 2003. Multiple hybrid formation in natural populations: concerted evolution of the internal transcribed spacer of nuclear ribosomalDNA(ITS) in NorthAmerican Arabis divaricarpa (Brassicaceae). Molecular Biology and Evolution 20: 338-350. (Pubitemid 36427168)
41. Koch, M. A., B. Haubold, and T. Mitchell-Olds. 2000. Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae). Molecular Biology and Evolution 17: 1483-1498.
42. Koch, M. A., B. Haubold, and T. Mitchell-Olds. 2001. Molecular systematics of the Brassicaceae: Evidence from coding plastidic matK and nuclear Chs sequences. American Journal of Botany 88: 534-544. (Pubitemid 33644899)
43. Linder, C. R. and L. H. Rieseberg. 2004. Reconstructing patterns of reticulate evolution in plants. American Journal of Botany 91: 1700-1708. (Pubitemid 43193727)
44. Löve, A ́ . and D. Löve 1976 Nomenclatural notes on arctic plants. Botaniska Notiser 128 497-523.
45. Mace, E. S., H. K. Buhariwalla, and J. H. Crouch. 2003. A high-throughput DNA extraction protocol for tropical molecular breeding programs. Plant Molecular Biology Reporter 21: 459-460.
46. McDade, L. 1990. Hybrids and phylogenetic systematics I. Patterns of character expression in hybrids and their implications for cladistic analysis. Evolution 44: 1685-1700.
47. McKay, J. K., J. G. Bishop, J. Z. Lin, J. H. Richards, A. Sala, and T. Mitchell-Olds. 2001. Local adaptation across a climatic gradient despite small effective population size in the rare sapphire rockcress. Proceedings of the Royal Society Biological Sciences Series B 268: 1715-1721. (Pubitemid 32758608)
48. Miller, M. A., M. T. Holder, R. Vos, P. E. Midford, T. Liebowitz, L. Chan, P. Hoover, and T. Warnow. 2010. The CIPRES Portals. CIPRES. URL: http://www.phylo.org/portal2/[accessed December 2010 to March 2011].
49. Mitchell-Olds, T. 2001. Arabidopsis thaliana and its wild relatives: a model system for ecology and evolution. Trends in Ecology & Evolution 16: 693-700. (Pubitemid 33082109)
50. Müller, K. 2005. SeqState: primer design and sequence statistics for phylogenetic DNA datasets. Applied Bioinformatics 4: 65-69. (Pubitemid 41043903)
51. Naumova, T. N., J. van der Laak, J. Osadtchiy, F. Matzk, A. Kravtchenko, J. Bergervoet, K. S. Ramulu, and K. Boutilier. 2001. Reproductive development in apomictic populations of Arabis holboellii (Brassicaceae). Sexual Plant Reproduction 14: 195-200. (Pubitemid 34018132)
52. Nixon, K. C. 1999-2002. WinClada ver. 1.0000. Ithaca: Published by the author.
53. Oyama, R. K., M. J. Clauss, N. Formanová , J. Kroymann, K. J. Schmid, H. Vogel, K. Weniger, A. J. Windsor, and T. Mitchell-Olds. 2008. The shrunken genome of Arabidopsis thaliana. Plant Systematics and Evolution 273: 257-271.
54. Pelser, P. B., B. Nordenstam, J. W. Kadereit, and L. E. Watson. 2007. An ITS phylogeny of tribe Senecioneae (Asteraceae) and a new delimitation of Senecio L. Taxon 56: 1077-1104.
55. Rambaut, A. 2002. Se-Al v.2.0a11. Edinburgh: Published by the author.
56. Rollins, R. C. 1941. A monographic study of Arabis in western North America. Rhodora 43: 289-325, 348-411, 425-485.
57. Rollins, R. C. 1993. The Cruciferae of continental North America. Palo Alto: Stanford University Press.
58. Roy, B. A. 1995. The breeding systems of six species of Arabis (Brassicaceae). American Journal of Botany 82: 869-877. (Pubitemid 26451166)
59. Roy, B. A. 2001. Patterns of association between crucifers and their flower mimic pathogens: host jumps are more common than coevolution or cospeciation. Evolution 55: 41-53. (Pubitemid 32175284)
60. Roy, B. A. and R. A. Raguso. 1997. Olfactory versus visual cues in a floral mimicry system. Oecologia 109: 414-426.
61. Roy, B. A. and L. H. Rieseberg. 1989. Evidence for apomixis in Arabis. Heredity 80: 506-508. (Pubitemid 20089148)
62. Rushworth, C. A., B.-H. Song, C.-R. Lee, and T. Mitchell-Olds. 2011. Boechera, a model system for ecological genomics. Molecular Ecology 20: 4843-4857.
63. Schneider, H., S. Russell, C. Cox, F. Bakker, S. Henderson, F. Rumsey, J. Barrett, M. Gibby, and J. Vogel. 2004. Chloroplast phylogeny of asplenioid ferns based on rbcL and trnL-F spacer sequences (Polypodiidae, Aspleniaceae) and its implications for biogeography. Systematic Botany 29: 260-274. (Pubitemid 38681978)
64. Schranz, M. E., C. Dobes, M. Koch, and T. Mitchell-Olds. 2005. Sexual reproduction, hybridization, apomixis, and polyploidization in the genus Boechera (Brassicaceae). American Journal of Botany 92: 1797-1810. (Pubitemid 41540861)
65. Schranz, M. E., L. Kantama, H. de Jong, and T. Mitchell-Olds. 2006. Asexual reproduction in a close relative of Arabidopsis: a genetic investigation of apomixis in Boechera (Brassicaceae). The New Phytologist 171: 425-438.
66. Schranz,M. E., A. J.Windsor, B.-H. Song, A. Lawton-Rauh, and T. Mitchell-Olds. 2007. Comparative genetic mapping in Boechera stricta, a close relative of Arabidopsis. Plant Physiology 144: 286-298.
67. Sharbel, T. F. and T. Mitchell-Olds. 2001. Recurrent polyploid origins and chloroplast phylogeography in the Arabis holboellii complex (Brassicaceae). Heredity 87: 59-69.
68. Sharbel, T. F., T. Mitchell-Olds, C. Dobes, L. Kantama, and H. de Jong. 2005. Biogeographic distribution of polyploidy and B chromosomes in the apomictic Boechera holboellii complex. Cytogenetic and Genome Research 109: 283-292. (Pubitemid 40470334)
69. Sharbel, T. F., M.-L. Voigt, J. M. Corral, G. Galla, J. Kumlehn, C. Klukas, F. Schreiber, H. Vogel, and B. Rotter. 2010. Apomictic and sexual ovules of Boechera display heterochronic global gene expression patterns. The Plant Cell 22: 655-671.
70. Sharbel, T. F., M.-L. Voigt, J. M. Corral, T. Thiel, A. Varshney, J. Kumlehn, H. Vogel, and B. Rotter. 2009. Molecular signatures of apomictic and sexual ovules in the Boechera holboellii complex. The Plant Journal 58: 870-882.
71. Sharbel, T. F., M.-L. Voigt, T. Mitchell-Olds, L. Kantama, and H. de Jong. 2004. Is the aneuploid chromosome in an apomictic Boechera holboellii a genuine B chromosome? Cytogenetic and Genome Research 106: 173-183. (Pubitemid 39077862)
72. 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. (Pubitemid 46955026)
73. Simmons, M. P. and H. Ochoterena. 2000. Gaps as characters in sequencebased phylogenetic analyses. Systematic Biology 49: 369-381.
74. Slotte, T., A. Ceplitis, E. Neuffer, H. Hurka, and M. Lascoux. 2006. Intrageneric phylogeny of Capsella (Brassicaceae) and the origin of the tetraploid C. bursa-pastoris based on chloroplast and nuclear DNA sequences. American Journal of Botany 93: 1714-1724. (Pubitemid 44790675)
75. Song, B.-H. and T. Mitchell-Olds. 2007. High genetic diversity and population differentiation in Boechera fecunda, a rare relative of Arabidopsis. Molecular Ecology 16: 4079-4088. (Pubitemid 47481053)
76. Song, B.-H., M. J. Clauss, A. Pepper, and T. Mitchell-Olds. 2006. Geographic patterns of microsatellite variation in Boechera stricta, a close relative of Arabidopsis. Molecular Ecology 15: 357-369.
77. Stamatakis, A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690. (Pubitemid 44642609)
78. Stamatakis, A., P. Hoover, and J. Rougemont. 2008. A rapid bootstrap algorithm for the RAxML web-servers. Systematic Biology 75: 758-771.
79. Taberlet, P., L. Gielly, G. Pautou, and J. Bouvet. 1991. Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Molecular Biology 17: 1105-1110.
80. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22: 4673-4680. (Pubitemid 24354800)
81. Tsitrone, A., M. Kirkpatrick, and D. A. Levin. 2003. A model for chloroplast capture. Evolution 57: 1776-1782. (Pubitemid 37096394)
82. van der Linde, K., G. Bächli, M. J. Toda, W.-X. Zhang, T. Katoh, Y.-G. Hu, and G. S. Spicer. 2007. Drosophila Fallén,1832 (Insecta, Diptera): proposed conservation of usage. Bulletin of Zoological Nomenclature 64: 238-242.
83. Warwick, S. I., K. Mummenhoff, C. A. Sauder, M. A. Koch, and I. A. Al-Shehbaz. 2010. Closing the gaps: phylogenetic relationships in the Brassicaceae based on DNA sequence data of nuclear ribosomal ITS region. Plant Systematics and Evolution 285: 209-232.
84. Wen, J. 1999. Evolution of eastern Asian and eastern North American disjunct distributions in flowering plants. Annual Review of Ecology and Systematics 30: 421-455. (Pubitemid 30065633)
85. White, T. J., T. Bruns, S. Lee, and J. Taylor. 1990. Amplification and direct sequencing of fungal ribosomal RNA gene for phylogenetics. Pp. 315-322 in PCR protocols: a guide to methods and applications, eds. M. Innis, D.Gelfand, J. Sninsky, andT. J.White. SanDiego: Academic Press.
86. Windham, M. D. and I. A. Al-Shehbaz. 2006. New and noteworthy species of Boechera (Brassicaceae) I: sexual diploids. Harvard Papers in Botany 11: 61-88.
87. Windham, M. D. and I. A. Al-Shehbaz. 2007a. New and noteworthy species of Boechera (Brassicaceae) II: apomictic triploids. Harvard Papers in Botany 11: 257-274.
88. Windham, M. D. and I. A. Al-Shehbaz. 2007b. New and noteworthy species of Boechera (Brassicaceae) III: additional sexual diploids and apomictic hybrids. Harvard Papers in Botany 12: 235-257.
89. Windham, M. D. and I. A. Al-Shehbaz. 2012. Boechera. Pp. 521-533 in The Jepson Manual: Vascular Plants of California, 2nd edition, eds. B. G. Baldwin, D. H. Goldman, D. J. Keil, R. Patterson, T. J. Rosatti, and D. H.Wilken. Berkeley: University of California Press.
90. Windsor, A. J., M. E. Schranz, N. Formanová , S. Gebauer-Jung, J. G. Bishop, D. Schnabelrauch, J. Kroymann, and T. Mitchell-Olds. 2006. Partial shotgun sequencing of the Boechera stricta genome reveals extensive microsynteny and promoter conservation with Arabidopsis. Plant Physiology 140: 1169-1182. (Pubitemid 43956205)
91. Xiang, Q.-Y., D. E. Soltis, and P. S. Soltis. 1998. The eastern Asian and eastern and western North American floristic disjunction: congruent phylogenetic patterns in seven diverse genera. Molecular Phylogenetics and Evolution 10: 178-190. (Pubitemid 128350308)