Plant Systematics and Evolution

, Volume 285, Issue 3–4, pp 209–232

Closing the gaps: phylogenetic relationships in the Brassicaceae based on DNA sequence data of nuclear ribosomal ITS region

  • Suzanne I. Warwick
  • Klaus Mummenhoff
  • Connie A. Sauder
  • Marcus A. Koch
  • Ihsan A. Al-Shehbaz
Original Article

Abstract

Sequence data from the nuclear encoded ribosomal internal transcribed spacer (ITS) region were used to determine monophyly of tribes, tribal limits, and tribal relationships of 96 so far unassigned or tentatively assigned genera (represented by 101 taxa/accessions) within the Brassicaceae. Maximum-parsimony and maximum-likelihood analyses of 185 ITS Brassicaceae sequences, which also included representatives of each of the 34 currently recognized tribes, supported the separate phylogenetic distinctness of these tribes and permitted the tribal assignment of all but 12 of the unassigned genera into tribal clades. The data support the recognition of eight new, well-resolved, uni- or oligogeneric tribes recognized herein as the Alyssopsideae [96% bootstrap support (BS); including the central and southwestern Asian Alyssopsis and Calymmatium], Asteae (100% BS; including the Mexican Asta), Eudemeae (97% BS; South American Brayopsis, Eudema, and Xerodraba), Kernereae (96% BS; European Kernera and Rhizobotrya), Notothlaspideae (100% BS; New Zealandic Notothlaspi), Oreophytoneae (100% BS; eastern African Oreophyton and southern European Murbeckiella), and Yinshanieae (100% BS; Chinese Yinshania), as well as the moderately supported Microlepidieae (75% BS; Australian Microlepidium and Carinavalva). Furthermore, the results fully support the recent findings that the tribes Schizopetaleae and Thelypodieae ought to be recognized as two distinct tribes instead of a single tribe, as well as provide some support for the re-establishment of the tribe Cremolobeae, bringing the total number to 44 tribes in the family. Nearly 92% (308) of the 336 genera in the family have been assigned to a tribe. The earlier-published Anastaticeae is taken here to replace the Malcolmieae.

Keywords

Brassicaceae ITS region Phylogeny Systematics Tribal assignments 

Supplementary material

606_2010_271_MOESM1_ESM.xls (137 kb)
Supplementary material (XLS 137 kb)

References

  1. Al-Shehbaz IA (1984) The tribes of Cruciferae (Brassicaceae) in the southeastern United States. J Arnold Arbor 65:343–373Google Scholar
  2. Al-Shehbaz IA (1986) The genera of Lepidieae (Cruciferae; Brassicaceae) in the southeastern United States. J Arnold Arbor 67:265–311Google Scholar
  3. Al-Shehbaz IA (1987) The genera of Alysseae (Cruciferae; Brassicaceae) in the southeastern United States. J Arnold Arbor 68:185–240Google Scholar
  4. Al-Shehbaz IA (1988a) The genera of Arabideae (Cruciferae; Brassicaceae), the southeastern United States. J Arnold Arbor 69:85–166Google Scholar
  5. Al-Shehbaz IA (1988b) The genera of Anchonieae (Hesperideae) (Cruciferae; Brassicaceae), the southeastern United States. J Arnold Arbor 69:193–212Google Scholar
  6. Al-Shehbaz IA (1988c) The genera of Sisymbrieae (Cruciferae; Brassicaceae), the southeastern United States. J Arnold Arbor 69:213–237Google Scholar
  7. Al-Shehbaz IA (2002) Noccaea nepalensis, a new species from Nepal, and four new combinations in Noccaea (Brassicaceae). Adansonia sér 3 24:89–92Google Scholar
  8. Al-Shehbaz IA, Warwick SI (2005) A synopsis of Eutrema (Brassicaceae). Harvard Pap Bot 10:129–135CrossRefGoogle Scholar
  9. Al-Shehbaz IA, Warwick SI (2007) Two new tribes (Dontostemoneae and Malcolmieae) in the Brassicaceae (Cruciferae). Harvard Pap Bot 12:429–433CrossRefGoogle Scholar
  10. Al-Shehbaz IA, Yang G, Lu LL, Cheo TY (1998) Delimitation of the Chinese genera Yinshania, Hilliella, and Cochleariella (Brassicaceae). Harvard Pap Bot 3:79–94Google Scholar
  11. Al-Shehbaz IA, Beilstein MA, Kellogg EA (2006) Systematics and phylogeny of the Brassicaceae (Cruciferae): an overview. Pl Syst Evol 259:89–120CrossRefGoogle Scholar
  12. Alvarez I, Wendel JF (2003) Ribosomal ITS sequences and plant phylogenetic inference. Mol Phylogenet Evol 29:417–434PubMedCrossRefGoogle Scholar
  13. Appel O, Al-Shehbaz IA (2003) Cruciferae. In: Kubitzki K, Bayer C (eds) The families and genera of vascular plants, vol 5. Springer, Berlin, pp 75–174Google Scholar
  14. Avetisian VE (1983) The system of the family Brassicaceae. Bot Zhurn (Moscow and Leningrad) 68:1297–1305 (in Russian)Google Scholar
  15. Bailey CD, Doyle JJ (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. Mol Phylogenet Evol 13:20–30PubMedCrossRefGoogle Scholar
  16. Bailey CD, Price RA, Doyle JJ (2002) Systematics of the Halimolobine Brassicaceae: evidence from three loci and morphology. Syst Bot 27:318–322Google Scholar
  17. Bailey CD, Carr TG, Harris SA, Hughes CE (2003) Characterization of angiosperm nrDNA polymorphism, parology and pseudogenes. Mol Phylogenet Evol 29:435–455PubMedCrossRefGoogle Scholar
  18. Bailey CD, Koch MA, Mayer M, Mummenhoff K, O’Kane SL Jr, Warwick SI, Windham MD, Al-Shehbaz IA (2006) Toward a global phylogeny of the Brassicaceae. Mol Biol Evol 23:2142–2160PubMedCrossRefGoogle Scholar
  19. Beilstein MA, Windham MD (2003) A phylogenetic analysis of western North American Draba (Brassicaceae) based on nuclear ribosomal DNA sequences from the ITS region. Syst Bot 28:584–592Google Scholar
  20. Beilstein MA, Al-Shehbaz IA, Kellogg EA (2006) Brassicaceae phylogeny and trichome evolution. Am J Bot 93:607–619CrossRefGoogle Scholar
  21. Beilstein MA, Al-Shehbaz IA, Mathews S, Kellogg EA (2008) Brassicaceae phylogeny inferred from phytochrome A and NDHF sequence data: tribes and trichomes revisted. Am J Bot 95:1307–1327CrossRefGoogle Scholar
  22. Bleeker W, Franzke A, Pollmann K, Brow AHD, Hurka H (2002a) Phylogeny and biogeography of southern hemisphere high-mountain Cardamine species (Brassicaceae). Aust Syst Bot 15:575–581CrossRefGoogle Scholar
  23. Bleeker W, Weber-Sparenberg C, Hurka H (2002b) Chloroplast DNA variation and biogeography in the genus Rorippa Scop. (Brassicaceae). Pl Biol 4:104–111CrossRefGoogle Scholar
  24. Bleeker W, Klausmeyer S, Peintinger M, Dienst M (2008) DNA sequences identify invasive alien Cardamine at Lake Constance. Biol Conserv 141:692–698CrossRefGoogle Scholar
  25. Boissier E, Buhse F (1860) Aufzählung der auf einer Reise durch Transkaukasian und Persien gesammelten Pflanzen. Nouv Mem Soc Nat Mosc 18:22Google Scholar
  26. Couvreur TLP, Franzke A, Al-Shehbaz IA, Bakker FT, Koch MA, Mummenhoff K (2010) Molecular phylogenetics, temporal diversification and principles of evolution in the mustard family (Brassicaceae). Mol Biol Evol 27:55–71PubMedCrossRefGoogle Scholar
  27. Crespo MB, Lledo MD, Fay MF, Chase MW (2000) Subtribe Vellinae (Brassiceae, Brassicaceae): a combined analysis of ITS nrDNA sequences and morphological data. Ann Bot 86:53–62CrossRefGoogle Scholar
  28. Crespo MB, Rios S, Vivero JL, Prados J, Hernandez-Bermejo E, Lledo MD (2005) A new spineless species of Vella (Brassicaceae) from the high mountains of south-eastern Spain. Bot J Linn Soc 149:121–128CrossRefGoogle Scholar
  29. de Candolle AP (1821) Mémoire sur la famille des Crucifères. Mém Mus Hist Nat 7(1):169–252Google Scholar
  30. Denham D, Clapperton H (1826) Narrative of travels and discoveries in northern and central Africa. John Murray, LondonGoogle Scholar
  31. Dobeš C, Mitchell-Olds T, Koch M (2003) Multiple hybrid formation in natural populations: concerted evolution of the internal transcribed spacer of nuclear ribosomal DNA (ITS) in North American Arabis divaricarpa (Brassicaceae). Mol Biol Evol 20:333–350Google Scholar
  32. Dobeš C, Mitchell-Olds T, Koch M (2004) Intraspecific diversification in North American Boechera stricta (=Arabis drummondii), Boechera × divaricarpa, and Boechera holboellii (Brassicaceae) inferred from nuclear and chloroplast molecular markers an integrative approach. Am J Bot 91:2087–2101CrossRefGoogle Scholar
  33. Francisco-Ortega J, Fuertes-Aguilar J, Gómez-Campo C, Santos-Guerra A, Jansen RK (1999) Internal transcribed spacer sequence phylogeny of Crambe (Brassicaceae): molecular data reveal two Old World disjunctions. Mol Phylogenet Evol 11:361–380PubMedCrossRefGoogle Scholar
  34. Francisco-Ortega J, Fuertes-Aguilar J, Kim SC, Santos-Guerra A, Crawford DJ, Jansen RK (2002) Phylogeny of the Macaronesian endemic Crambe section Dendrocrambe (Brassicaceae) based on internal transcribed spacer sequences of nuclear ribosomal DNA. Am J Bot 89:1984–1990CrossRefGoogle Scholar
  35. Franzke A, Mummenhoff K (1999) Recent hybrid speciation in Cardamine (Brassicaceae)—conversion of nuclear ribosomal ITS sequences in statu nascendi. Theor Appl Genet 98:831–834CrossRefGoogle Scholar
  36. Franzke A, Pollmann K, Bleeker W, Kohrt R, Hurka H (1998) Molecular systematics of Cardamine and allied genera (Brassicaceae): ITS and non-coding chloroplast DNA. Folia Geobot Phytotax 33:225–240Google Scholar
  37. Franzke A, Hurka H, Janssen D, Neuffer B, Friesen N, Markov M, Mummenhoff K (2004) Molecular signals for late Tertiary/early Quaternary range splits of an Eurasian steppe plant: Clausia aprica (Brassicaceae). Mol Ecol 13:2789–2795PubMedCrossRefGoogle Scholar
  38. Franzke A, German D, Al-Shehbaz IA, Mummenhoff K (2009) Arabidopsis family ties: Molecular phylogeny and age estimates in the Brassicaceae. Taxon 58:425–437Google Scholar
  39. Gazzani S, Li M, Maistri S, Scarponi E, Graziola M, Barbaro E, Wunder J, Furini A, Saedler H, Varotto C (2009) Evolution of MIR168 paralogs in Brassicaceae BMC. Evol Biol 9:62CrossRefGoogle Scholar
  40. German DA, Al-Shehbaz IA (2008) Five additional tribes (Aphragmeae, Biscutelleae, Calepineae, Conringieae, and Erysimeae) in the Brassicaceae (Cruciferae). Harvard Pap Bot 13:165–170CrossRefGoogle Scholar
  41. German DA, Friesen N, Neuffer B, Al-Shehbaz IA, Hurka H (2009) Contribution to ITS phylogeny of the Brassicaceae, with a special reference to some Asian taxa. Pl Syst Evol 283:33–56CrossRefGoogle Scholar
  42. Goodson BE, Santos-Guerra A, Jansen RK (2006) Molecular systematics of Descurainia (Brassicaceae) in the Canary Islands: biogeographic and taxonomic implications. Taxon 55:671–682CrossRefGoogle Scholar
  43. Grundt HH, Popp M, Brochmann C, Oxelman B (2004) Polyploid origins in a circumpolar complex in Draba (Brassicaceae) inferred from cloned nuclear DNA sequences and fingerprints. Mol Phylogenet Evol 32:695–710PubMedCrossRefGoogle Scholar
  44. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704PubMedCrossRefGoogle Scholar
  45. Guindon S, Lethiec F, Duroux P, Gascuel O (2005) PHYML Online—a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res 33 (Suppl. S, Web Server issue): W557–W559. http://atgc.lirmm.fr/phyml/
  46. Hall JC, Sytsma KJ, Iltis HH (2002) Phylogeny of Capparaceae and Brassicaceae based on chloroplast sequence data. Am J Bot 89:1826–1842CrossRefGoogle Scholar
  47. Hall JC, Iltis HH, Systma KJ (2004) Molecular phylogenetics of core Brassicales, placement of orphan genera Emblingia, Forchhammeria, Tirania, and character evolution. Syst Bot 29:654–699CrossRefGoogle Scholar
  48. Hayek A (1911) Entwurf eines Cruciferensystems auf phylogenetischer Grundlage. Beih Bot Centralbl 27:127–335Google Scholar
  49. Hedge IC (1976) A systematic and geographical survey of the Old World Cruciferae. In: Vaughan JG, MacLeod AJ, Jones BMG (eds) The biology and chemistry of the Cruciferae. Academic, London, pp 1–145Google Scholar
  50. Hedge IC, Rechinger KH (1968) Cruciferae. In: Rechinger KH (ed) Flora Iranica 57. Akademische Druck-U. Verlagsanstalt, Graz, pp 1–372Google Scholar
  51. Heenan PB, Mitchell AD (2003) Phylogeny, biogeography and adaptive radiation of Pachycladon (Brassicaceae) in the mountains of South Island, New Zealand. J Biogeogr 30:1737–1749CrossRefGoogle Scholar
  52. Heenan PB, Mitchell AD, Koch M (2002) Molecular systematics of the New Zealand Pachycladon (Brassicaceae) complex: generic circumscription and relationship to Arabidopsis sens. lat. and Arabis sens. lat. N Z J Bot 40:543–562Google Scholar
  53. Heenan PB, Mitchell AD, McLenachan PA, Lockhart PJ, de Lange PJ (2007) Natural variation and conservation of Lepidium sisymbrioides Hook. f. and L. solandri Kirk (Brassicaceae) in South Island, New Zealand, based on morphological and DNA sequence data. N Z J Bot 45:237–264Google Scholar
  54. Holmgren PK, Holmgren NH, Barnett LC (eds) (1990) Index herbariorum, Part I: the herbaria of the world, 8th edn. New York Botanical Garden, New YorkGoogle Scholar
  55. Hong RL, Hamaguchi L, Busch MA, Weigel D (2003) Regulatory elements of the floral homeotic gene AGAMOUS identified by phylogenetic footprinting and shadowing. Pl Cell 15:1296–1309CrossRefGoogle Scholar
  56. Janchen E (1942) Das System der Cruciferen. Oesterr Bot Z 91:1–28CrossRefGoogle Scholar
  57. Johnston JS, Pepper AE, Hall AE, Chen ZJ, Hodnett G, Drabek J, Lopez R, Price HJ (2005) Evolution of genome size in Brassicaceae. Ann Bot 95:229–235PubMedCrossRefGoogle Scholar
  58. Khosravi AR, Mohsenzadeh S, Mummenhoff K (2008a) Phylogenetic position of Brossardia papyracea (Brassicaceae) based on sequences of nuclear ribosomal DNA. Feddes Repert 119:13–23CrossRefGoogle Scholar
  59. Khosravi AR, Mohsenzadeh S, Mummenhoff K (2008b) Analysis of the phylogenetic position of Acanthocardamum erinaceum (Boiss.) Thell. (Brassicaceae) based on ITS-sequences shows that it should be transferred to Aethionema as A. erinaceum. Nord J Bot 26:25–30Google Scholar
  60. Khosravi AR, Mohsenzadeh S, Mummenhoff K (2009) Phylogenetic relationships of Old World Brassicaceae from Iran based on nuclear ribosomal DNA sequences. Biochem Syst Ecol 37:106–115CrossRefGoogle Scholar
  61. Kiefer C, Dobes C, Koch MA (2009) Boechera or not? Phylogeny and phylogeography of eastern North American Boechera species (Brassicaceae). Taxon 58:1109–1121Google Scholar
  62. Koch M (2003) Molecular phylogenetics, evolution and population biology in the Brassicaceae. In: Sharma AK, Sharma A (eds) Plant genome: biodiversity and evolution. Phanerogams, vol 1. Science, Enfield, pp 1–35Google Scholar
  63. Koch M, Al-Shehbaz IA (2000) Molecular systematics of the Chinese Yinshania (Brassicaceae): evidence from plastid and nuclear ITS DNA sequence data. Ann Mo Bot Gard 87:246–272CrossRefGoogle Scholar
  64. Koch M, Al-Shehbaz IA (2002) Molecular data indicate complex intra- and intercontinental differentiation of American Draba (Brassicaceae). Ann Mo Bot Gard 89:88–109CrossRefGoogle Scholar
  65. Koch M, Al-Shehbaz IA (2004) Taxonomic and phylogenetic evaluation of the American “Thlaspi” species: identity and relationship to the Eurasian genus Noccaea (Brassicaceae). Syst Bot 29:375–384CrossRefGoogle Scholar
  66. Koch M, Al-Shehbaz IA (2009) Molecular systematics and evolution. In: Gupta S (ed) Biology and breeding of crucifers. CRC, Boca Raton, pp 1–18CrossRefGoogle Scholar
  67. Koch M, Mummenhoff K (2001) Thlaspi s.str. (Brassicaceae) versus Thlaspi s.l.: morphological and anatomical characters in the light of ITS nrDNA sequence data. Pl Syst Evol 227:209–225CrossRefGoogle Scholar
  68. Koch M, Mummenhoff K (2006) Evolution and phylogeny of the Brassicaceae. Pl Syst Evol 259:81–83CrossRefGoogle Scholar
  69. Koch M, Bishop J, Mitchell-Olds T (1999a) Molecular systematics and evolution of Arabidopsis and Arabis. Pl Biol (Stuggt) 1:529–537CrossRefGoogle Scholar
  70. Koch M, Mummenhoff K, Hurka H (1999b) Molecular phylogenetics of Cochlearia (Brassicaceae) and allied genera based on nuclear ribosomal ITS DNA sequence analysis contradict traditional concepts of their evolutionary relationship. Pl Syst Evol 216:207–230CrossRefGoogle Scholar
  71. Koch M, Al-Shehbaz IA, Mummenhoff K (2003a) Molecular systematics, evolution, and population biology in the mustard family Brassicaceae: a review of a decade of studies. Ann Mo Bot Gard 90:151–171CrossRefGoogle Scholar
  72. Koch M, Dobeš C, Mitchell-Olds T (2003b) Multiple hybrid formation in natural populations: Concerted evolution of the internal transcribed spacer of nuclear ribosomal DNA (ITS) in North American Arabis divaricarpa (Brassicaceae). Mol Biol Evol 20:338–350PubMedCrossRefGoogle Scholar
  73. Koch M, Dobeš C, Keifer C, Schmickl R, Klimeš L, Lysak MA (2007) Supernetwork identifies multiple events of plastid trnF(GAA) pseudogene evolution in the Brassicaceae. Mol Biol Evol 24:63–73PubMedCrossRefGoogle Scholar
  74. Kress WJ, Wurdack KJ, Zimmer EA, Weigt LA, Janzen DH (2005) Use of DNA barcodes to identify flowering plants. Proc Natl Acad Sci USA 102:8369–8374PubMedCrossRefGoogle Scholar
  75. Kropf M, Kadereit JW, Comes HP (2003) Differential cycles of range contraction and expansion in European high mountain plants during the Late Quaternary: insights from Pritzelago alpina (L.) O. Kuntze (Brassicaceae). Mol Ecol 12:931–949PubMedCrossRefGoogle Scholar
  76. Li G, Wang Z, Xu G (2010) Molecular phylogenetic studies of Isatis and allied genera based on the internal transcribed spacer region of 18S-26S rDNA. Unpublished Genbank SequenceGoogle Scholar
  77. Lihová J, Aguilar JF, Marhold K, Feliner GN (2004) Origin of the disjunct tetraploid Cardamine amporitana (Brassicaceae) assessed with nuclear and chloroplast sequence data. Am J Bot 91:1231–1242CrossRefGoogle Scholar
  78. Lihová J, Marhold K, Kudoh H, Koch MA (2006a) Worldwide phylogeny and biogeography of Cardamine flexuosa (Brassicaceae) and its relatives. Am J Bot 93:1206–1221CrossRefGoogle Scholar
  79. Lihová J, Shimizu KK, Marhold K (2006b) Allopolyploid origin of Cardamine asarifolia (Brassicaceae): incongruence between plastid and nuclear ribosomal DNA sequences solved by a single-copy nuclear gene. Mol Phylogenet Evol 39:759–786PubMedCrossRefGoogle Scholar
  80. Lysak MA, Lexer C (2006) Towards the era of comparative evolutionary genomics in Brassicaceae. Pl Syst Evol 259:175–198CrossRefGoogle Scholar
  81. Lysak MA, Koch MA, Beaulieau JM, Meister A, Leitch IJ (2009) The dynamic ups and downs of genome size evolution in Brassicaceae. Mol Biol Evol 26:85–98. doi:10.1093/molbev/msn223 PubMedCrossRefGoogle Scholar
  82. Marhold K, Lihová J, Perny M, Bleeker W (2004) Comparative ITS and AFLP analysis of diploid Cardamine (Brassicaceae) taxa from closely related polyploid complexes. Ann Bot 93:507–520PubMedCrossRefGoogle Scholar
  83. McBreen K, Heenan PB (2006) Phylogenetic relationships of Pachycladon (Brassicaceae) species based on three nuclear and two chloroplast DNA markers. N Z J Bot 44:377–386Google Scholar
  84. Mengoni A, Baker AJM, Bazzicalupo M, Reeves RD, Adigüzel N, Chianni E, Galardi F, Gabbriella R, Gonnelli C (2003) Evolutionary dynamics of nickel hyperaccumulation in Alyssum revealed by ITS nrDNA analysis. New Phytol 159:691–699CrossRefGoogle Scholar
  85. Mitchell AD, Heenan PB (2000) Systematic relationships of New Zealand endemic Brassicaceae inferred from nrDNA ITS sequence data. Syst Bot 25:98–105CrossRefGoogle Scholar
  86. Mitchell-Olds T, Al-Shehbaz IA, Koch M, Sharbel TF (2005) Crucifer evolution in the post-genomic era. In: Henry RJ (ed) Plant diversity and evolution: genotypic and phenotypic variation in higher plants. CAB International, Wallingford, pp 119–137CrossRefGoogle Scholar
  87. Moazzeni H, Zarre S, Al-Shehbaz IA, Mummenhoff K (2007) Seed-coat microsculpturing and its systematic application in Isatis (Brassicaceae) and allied genera in Iran. Flora 202:447–454Google Scholar
  88. Moazzeni H, Zarre S, Al-Shehbaz IA, Mummenhoff K (2010) Phylogeny of Isatis (Brassicaceae) and allied genera based on ITS sequences of nuclear ribosomal DNA and morphological characters. Flora 205 (in press). doi:10.1016/j.flora.2009.12.028
  89. Mummenhoff K, Franzke A, Koch M (1997) Molecular phylogenetics of Thlaspi sl (Brassicaceae) based on chloroplast DNA restriction site variation and sequences of the internal transcribed spacers of nuclear ribosomal DNA. Can J Bot 75:469–482Google Scholar
  90. Mummenhoff K, Coja U, Brüggemann H (2001) Pachyphragma and Gagria (Brassicaceae) revisited: molecular data indicate close relationship to Thlaspi s.str. Folia Geobot 36:293–302CrossRefGoogle Scholar
  91. Mummenhoff K, Linder P, Friesen N, Bowman JL, Lee JY, Franzke A (2004) Molecular evidence for bicontinental hybridogenous genome constitution in Lepidium sensu stricto (Brassicaceae) species from Australia and New Zealand. Am J Bot 91:254–261CrossRefGoogle Scholar
  92. Mummenhoff K, Al-Shehbaz IA, Bakker FT, Linder HP, Mühlhaussen A (2005) Phylogeny, morphological evolution, and speciation of endemic Brassicaceae genera in the Cape flora of southern Africa. Ann Mo Bot Gard 92:400–424Google Scholar
  93. Mummenhoff K, Polster A, Mühlhausen A, Theissen G (2009) Lepidium as a model system for studying the evolution of fruit development in Brassicaceae. J Exper Bot 60:1503–1513CrossRefGoogle Scholar
  94. O’Kane SL Jr, Al-Shehbaz IA (2003) Phylogenetic position and generic limits of Arabidopsis (Brassicaceae) based on sequences of nuclear ribosomal DNA. Ann Mo Bot Gard 90:603–612CrossRefGoogle Scholar
  95. O’Kane SL Jr, Schaal B, Al-Shehbaz IA (1997) The origins of Arabidopsis suecica (Brassicaceae) as indicated by nuclear rDNA sequences. Syst Bot 21:559–566CrossRefGoogle Scholar
  96. Oyama RK, Clauss MJ, Formanova N, Kroymann J, Schmid KJ, Vogel H, Weniger K, Windsor AJ, Mitchell-Olds T (2008) The shrunken genome of Arabidopsis thaliana. Pl Syst Evol 273:257–271CrossRefGoogle Scholar
  97. Peer WA, Mamoudian M, Lahner B, Reeves RD, Murphy AS, Salt DE (2003) Identifying model metal hyperaccumulating plants: germplasm analysis of 20 Brassicaceae accessions from a wide geographical area. New Phytol 159:421–430CrossRefGoogle Scholar
  98. Pepper AE, Norwood LE (2001) Evolution of Caulanthus amplexicaulis var. barbarae (Brassicaceae), a rare serpentine endemic plant: A molecular phylogenetic perspective. Am J Bot 88:1479–1489CrossRefGoogle Scholar
  99. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818PubMedCrossRefGoogle Scholar
  100. Roy BA (2001) Patterns of association between crucifers and their flower-mimic pathogens: host jumps are more common than coevolution or cospeciation. Evolution 55:41–53PubMedGoogle Scholar
  101. Schulz OE (1936) Cruciferae. In: Engler A, Harms H (eds) Die Natürlichen Pflanzenfamilien, vol 17B, 2nd edn. Verlag von Wilhelm Engelmann, Leipzig, pp 227–658Google Scholar
  102. Swofford DL (2002) PAUP*: Phylogenetic analysis using parsimony (* and other methods). Version 4.0. Sinauer, SunderlandGoogle Scholar
  103. Warwick SI, Hall JC (2008) Phylogeny of Brassica and wild relatives. In: Gupta S (ed) Biology and breeding of crucifers. CRC, Boca Raton, pp 19–36Google Scholar
  104. Warwick SI, Sauder C (2005) Phylogeny of tribe Brassiceae based on chloroplast restriction site polymorphisms and nuclear ribosomal internal transcribed spacer (ITS) and chloroplast trnL intron sequences. Can J Bot 83:467–483CrossRefGoogle Scholar
  105. Warwick SI, Al-Shehbaz IA, Price RA, Sauder C (2002) Phylogeny of Sisymbrium (Brassicaceae) based on ITS sequences of nuclear ribosomal DNA. Can J Bot 80:1002–1017CrossRefGoogle Scholar
  106. Warwick SI, Al-Shehbaz IA, Sauder C, Harris JG, Koch M (2004a) Phylogeny of Braya and Neotorularia (Brassicaceae) based on nuclear ribosomal DNA and chloroplast trnL intron sequences. Can J Bot 82:376–392CrossRefGoogle Scholar
  107. Warwick SI, Al-Shehbaz IA, Sauder CA, Murray DF, Mummenhoff K (2004b) Phylogeny of Smelowskia and related genera (Brassicaceae) based on nuclear ITS DNA and chloroplast trnL intron DNA sequences. Ann Mo Bot Gard 91:99–123Google Scholar
  108. Warwick SI, Al-Shehbaz IA, Sauder C (2006a) Phylogenetic position of Arabis arenicola and generic limits of Eutrema and Aphragmus (Brassicaceae) based on sequences of nuclear ribosomal DNA. Can J Bot 84:269–281CrossRefGoogle Scholar
  109. Warwick SI, Francis A, Al-Shehbaz IA (2006b) Brassicaceae: species checklist and database on CD-Rom. Pl Syst Evol 259:249–258CrossRefGoogle Scholar
  110. Warwick SI, Sauder CA, Al-Shehbaz IA (2006c) Molecular phylogeny, morphology and cytological diversity of Sisymbrium (Brassicaceae). In: Sharma AK, Sharma A (eds) Plant genome: biodiversity and evolution: phanerogams (Angiosperm–Dicotyledons), vol 1C. Oxford and IBH, New Delhi with Science, USA, pp 219–250Google Scholar
  111. Warwick SI, Sauder C, Al-Shehbaz IA, Jacquemoud F (2007) Phylogenetic relationships in the Brassicaceae tribes Anchonieae, Chorisporeae, Euclidieae, and Hesperideae based on nuclear ribosomal ITS DNA sequences. Ann Mo Bot Gard 94:56–78CrossRefGoogle Scholar
  112. Warwick SI, Sauder CA, Al-Shehbaz IA (2008) Phylogenetic relationships in the tribe Alysseae (Brassicaceae) based on nuclear ribosomal ITS DNA sequences. Can J Bot 86:315–336CrossRefGoogle Scholar
  113. Warwick SI, Sauder CA, Mayer MS, Al-Shehbaz IA (2009) Phylogenetic relationships in the tribes Schizopetaleae and Thelypodieae (Brassicaceae) based on nuclear ribosomal ITS region and chloroplast ndhF DNA sequences. Botany 87:961–985CrossRefGoogle Scholar
  114. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols. Academic, New York, pp 315–322Google Scholar
  115. Widmer A, Baltisberger M (1999) Molecular evidence for allopolyploid speciation and a single origin of the narrow endemic Draba ladina (Brassicaceae). Am J Bot 86:1282–1289PubMedCrossRefGoogle Scholar
  116. Yang YW, Lai KN, Tai PY, Ma DP, Li WH (1999) Molecular phylogenetic studies of Brassica, Rorippa, Arabidopsis and allied genera based on the internal transcribed spacer region of 18S–25S rDNA. Mol Phylogenet Evol 13:455–462PubMedCrossRefGoogle Scholar
  117. Yue JP, Sun H, Al-Shehbaz IA, Li JH (2006) Support for an expanded Solms-laubachia (Brassicaceae): evidence from sequences of chloroplast and nuclear genes. Ann Mo Bot Gard 93:402–411CrossRefGoogle Scholar
  118. Yue J-P, Sun H, Li J-H, Al-Shehbaz IA (2008) A synopsis of an expanded Solms-laubachia (Brassicaceae), and the description of four new species from western China. Ann Mo Bot Gard 95:520–538CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Suzanne I. Warwick
    • 1
  • Klaus Mummenhoff
    • 2
  • Connie A. Sauder
    • 1
  • Marcus A. Koch
    • 3
  • Ihsan A. Al-Shehbaz
    • 4
  1. 1.Eastern Cereal and Oilseed Research CentreAgriculture and Agri-Food CanadaOttawaCanada
  2. 2.FB Biologie/Chemie, BotanikUniversität OsnabrückBarbarastrasse IIGermany
  3. 3.Heidelberg Institute of Plant Sciences, Biodiversity and Plant SystematicsUniversity of HeidelbergHeidelbergGermany
  4. 4.Missouri Botanical GardenSt. LouisUSA

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