Abstract
Sequence data from nuclear (ITS) and chloroplast (trnL-F) regions for 89 accessions representing 56 out of 64 species from all five genera of the tribe Chorisporeae (plus Dontostemon tibeticus) have been studied to test the monophyly of the tribe and its component genera, clarify its boundaries, and elucidate its phylogenetic position in the family. Both data sets showed strong support for the monophyly of the Chorisporeae as currently delimited, though the position of its tentative member D. tibeticus was not resolved by ITS. Parrya and Pseudoclausia are poly- and paraphyletic with regard to each other, and Chorispora is either polyphyletic or at least paraphyletic (comprising Diptychocarpus) within a weakly supported monophyletic clade. The incongruence in branching pattern among the markers was most likely caused by hybridization and possibly influenced by incomplete lineage sorting. The present results suggest uniting Pseudoclausia, Clausia podlechii, and Achoriphragma with Parrya and transferring P. beketovii and P. saposhnikovii to Leiospora (Euclidieae). We also obtained support for splitting Chorispora into two geographically defined groups, one of which is closer to Diptychocarpus. Both data sets revealed a close relationship of the Chorisporeae to Dontostemoneae, while ITS also indicated affinity to Hesperideae. Therefore, the position of Chorisporeae needs further verification.
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Al-Shehbaz IA (1984) The tribes of Cruciferae (Brassicaceae) in the southeastern United States. J Arnold Arbor 65:343–373
Al-Shehbaz IA (1988) The genera of Anchonieae (Hesperideae) (Cruciferae; Brassicaceae) in the southeastern United States. J Arnold Arbor 69:193–212
Al-Shehbaz IA (2000) What is Nasturtium tibeticum (Brassicaceae)? Novon 10:334–336
Al-Shehbaz IA (2010) Parrya R. Brown. In: Flora of North America Editorial Committee (eds) Flora of North America, vol 7. Oxford University Press, New York, pp 511–514
Al-Shehbaz IA, Warwick SI (2007) Two new tribes (Dontostemoneae and Malcolmieae) in the Brassicaceae (Cruciferae). Harvard Pap Bot 12:429–433
Al-Shehbaz IA, Beilstein MA, Kellogg EA (2006) Systematics and phylogeny of the Brassicaceae (Cruciferae): an overview. Pl Syst Evol 259:89–120
Al-Shehbaz IA, Grant JR, Lipkin R, Murray DF, Parker CL (2007) Parrya nauruaq (Brassicaceae), a new species from Alaska. Novon 17:275–278
Appel O, Al-Shehbaz IA (2003) Cruciferae. In: Kubitzki K, Bayer C (eds) The families and genera of vascular plants 5. Springer, Berlin & Heidelberg, pp 75–174
Aras S, Duran A, Yenilmez G (2003) Isolation of DNA for RAPD analysis from dry leaf material of some Hesperis L. specimens. Pl Molec Biol Reporter 21:461a–461f
Avetisian VE (1990) A review of the system of Brassicaceae of flora of Caucasus. Bot J (Moscow & Leningrad) 75:1029–1032
Bailey CD, Koch MA, Mayer M, Mummenhoff K, SLJr O’Kane, Warwick SI, Windham MD, Al-Shehbaz IA (2006) Towards a global phylogeny of the Brassicaceae. Mol Biol Evol 23:2142–2160
Beilstein MA, Al-Shehbaz IA, Kellogg EA (2006) Brassicaceae phylogeny and trichome evolution. Am J Bot 93:607–619
Beilstein MA, Al-Shehbaz IA, Mathews S, Kellogg EA (2008) Brassicaceae phylogeny inferred from phytochrome A and ndhF sequence data: tribes and trichomes revisited. Am J Bot 95:1307–1327
Beilstein MA, Nagalingum NS, Clements MD, Manchester SR, Mathews S (2010) Dated molecular phylogenies indicate a Miocene origin for Arabidopsis thaliana. Proc Natl Acad Sci USA 107:18724–18728
Bentham G, Hooker JD (1862) Genera plantarum 1. Ranunculaceas-Cornaceas, London
Blattner FR (1999) Direct amplification of the entire ITS region from poorly preserved plant material using recombinant PCR. Biotechnology 27:1180–1185
Botschantzev VP (1955) De Cruciferis notae criticae. Notul Syst Herb Inst Bot Acad Sci USSR 17:160–178
Botschantzev VP (1972) On Parrya R Br., Neuroloma Andrz. and some other genera (Cruciferae). Bot J (Moscow & Leningrad) 57:664–673
Botschantzev VP (1980) Two new genera of the family Cruciferae. Bot J (Moscow & Leningrad) 65:425–427
Busch NA (1939) Cruciferae. In: Komarov VL, Busch NA (eds) Flora URSS 8, 14–606. Academy of Sciences Press, Moscow & Leningrad
Carlsen T, Bleeker W, Hurka H, Elven R, Brochmann C (2009) Biogeography and phylogeny of Cardamine (Brassicaceae). Ann Mo Bot Gard 96:215–236
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 27:55–71
Czerepanov SK (1995) Vascular plants of Russia and adjacent states (the former USSR). Cambridge University Press, Cambridge
Dierschke T, Mandáková T, Lysak MA, Mummenhoff K (2009) A bicontinental origin of polyploid Australian/New Zealand Lepidium species (Brassicaceae)? Evidence from genomic in situ hybridization. Ann Bot 104(4):681–688
Dorofeyev VI (2004) System of family Cruciferae B. Juss. (Brassicaceae Burnett). Turczaninowia 7(3):43–52
Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure from small amounts of fresh leaf tissue. Phylochem Bull 19:11–15
Dvořák F (1968) Study of the characters of the genus Parrya R. Br. Přirod Fak Univ Purk Brno 497:343–359
Dvořák F (1969) Parrya microcarpa Ledeb. Fl. Ross. 1, 1842: 132. Feddes Repert 80(4–6):315–322
Dvořák F (1972) Study of the evolutional relationship of the tribe Hesperideae. Folia Fac Sci Nat Univ Purkynianae Brun Biol 13(4):1–82
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 33:225–240
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 13:2789–2795
Franzke A, German D, Al-Shehbaz IA, Mummenhoff K (2009) Arabidopsis’s family ties: molecular phylogeny and age estimates in the Brassicaceae. Taxon 58(2):425–437
German DA (2009) A check-list and the system of the Cruciferae of Altai. Komarovia 6(2):80–88
German DA, Al-Shehbaz IA (2008a) Five additional tribes (Aphragmeae, Biscutelleae, Calepineae, Conringieae and Erysimeae) in the Brassicaceae (Cruciferae). Harvard Pap Bot 13:165–170
German DA, Al-Shehbaz IA (2008b) Dendroarabis, a new Asian genus of Brassicaceae. Harvard Pap Bot 13:289–291
German DA, Al-Shehbaz IA (2010) Nomenclatural novelties in miscellaneous Asian Brassicaceae (Cruciferae). Nordic J Bot 28:646–651
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 283:33–56
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 32:695–710
Hayek A (1911) Entwurf eines Cruciferensystems auf phylogenetischer Grundlage. Beih Bot Centralbl 27:127–335
Holmgren PK, Holmgren NH (1998) [continuously updated]. Index Herbariorum: a global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. <http://sweetgum.nybg.org/ih/>
Jaén-Molina R, Caujapé-Castells J, Reyes-Betancort JA, Akhani H, Fernández-Palacios O, Pérez de Paz J, Febles-Hernández R, Marrero-Rodríguez Á (2009) The molecular phylogeny of Matthiola R. Br. (Brassicaceae) inferred from ITS sequences, with special emphasis on the Macaronesian endemics. Mol Phylogenet Evol 53:972–981
Janchen E (1942) Das System der Cruciferen. Österr Bot Ztg 91:1–28
Jordon-Thaden I, Hase I, Al-Shehbaz IA, Koch MA (2010) Molecular phylogeny and systematics of the genus Draba (Brassicaceae) and identification of its most closely related genera. Mol Phylogenet Evol 55(2):524–540
Kamelin RV (1998) Materials on the history of the flora of Asia: the Altai Mountain Country. Altai University Press, Barnaul
Kamelin RV (2002) The Cruciferae (brief survey of the system). Altai University Press, Barnaul
Khosravi AR, Mohsenzadeh S, Mummenhoff K (2009) Phylogenetic relationships of Old World Brassicaceae from Iran based on nuclear ribosomal DNA sequences. Biochem Syst Ecol 37:106–115
Koch M, Al-Shehbaz IA (2002) Molecular data indicate complex intra- and intercontinental differentiation of American Draba (Brassicaceae). Ann Missouri Bot Gard 89:88–109
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 29:375–384
Koch MA, Al-Shehbaz IA (2009) Molecular systematics and evolution. In: Gupta SK (ed) Biology and breeding of crucifers. CRC, Boca Raton, pp 1–18
Koch M, Al-Shehbaz IA, Mummenhoff K (2003) Molecular systematics, evolution, and population biology in the mustard family (Brassicaceae). Ann Mo Bot Gard 90:151–171
Koch M, Dobeš C, Matschinger M, Bleeker W, Vogel J, Kiefer M, Mitschell-Olds T (2005) Evolution of the trnF(GAA) gene in Arabidopsis relatives and the Brassicaceae family: monophyletic origin and subsequent diversification of a plastidic pseudogene. Mol Biol Evol 22(4):1032–1043
Koch M, Dobeš C, Kiefer C, Schmickl R, Klimeš L, Lysak M (2007) Supernetwork identifies multiple events of plastid trnF(GAA) pseudogene evolution in the Brassicaceae. Mol Biol Evol 24(1):63–73
Koch MA, Karl R, Kiefer C, Al-Shehbaz IA (2010) Colonizing the American continent—systematics of the genus Arabis in North America (Brassicaceae). Am J Bot 97:1040–1057
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 91:1231–1242
Lihová J, Marhold K, Kudoh H, Koch MA (2006a) Worldwide phylogeny and biogeography of Cardamine flexuosa (Brassicaceae) and its relatives. Am J Bot 93:1206–1221
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 39:759–786
Lysak MA, Koch MA, Beaulieu JM, Meister A, Leitch IJ (2009) The dynamic ups and downs in genome size evolution in Brassicaceae. Mol Biol Evol 21:85–98
Mandáková T, Lysak MA (2008) Chromosomal phylogeny and karyotype evolution in x = 7 crucifer species (Brassicaceae). Plant Cell 20:2559–2570
Mandáková T, Joly S, Krzywinski M, Mummenhoff K, Lysak MA (2010) Fast diploidization in close mesopolyploid relatives of Arabidopsis. Plant Cell 22:2277–2290
Marhold K, Lihová J (2006) Polyploidy, hybridization and reticulate evolution: lessons from the Brassicaceae. Pl Syst Evol 259:143–174
Meyer CA (1831) Classis XV. Tetradynamia. In: Ledebour CF (ed), Flora Altaica, vol 3. Typis et impensis G. Reimeri, Berolini, pp 1–219
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 91:254–261
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 60:1503–1513
Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University
Ovczinnikov PN, Yunussov SY (1978) Cruciferae. In: Ovczinnikov PN (ed) Flora of Tajik SSR 5. Science Press, Leningrad, pp 7–273
Pakhomova MG (1974) Cruciferae. In: Vvedensky AI, Pakhomova MG (eds) Conspectus floraeAsiae Mediae 4. Uzbek Academia of Sciences Press, Tashkent, pp 34–217
Prantl K (1891) Cruciferae. In: Engler A, Prantl K (eds) Die natürlichen Pflanzenfamilien 3(2), Leipzig, 145–206
Ronquist R, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Schmickl R, Jorgenson M, Brysting A, Koch MA (2010) The evolutionary history of the Arabidopsis lyrata complex: a hybrid in the amphi-Beringian area closes a large distribution gap and builds up a genetic barrier. BMC Evol Biol 10:98
Schulz OE (1936) Cruciferae. In: Engler A, Harms H (eds) Die natürlichen Pflanzenfamilien 17b, 227–658. Verlag von Wilhelm Engelmann, Leipzig
Shimizu-Inatsugi R, Lihová J, Iwanaga H, Kudoh H, Marhold K, Savolainen O, Watanabe K, Yakubov VV, Shimizu KK (2009) The allopolyploid Arabidopsis kamchatica originated from multiple individuals of Arabidopsis lyrata and Arabidopsis halleri. Mol Ecol 18:4024–4048
Soják J (1982) Einige Bemerkungen zur Flora der UdSSR, vol 1. Sborn Národn Muz Praze, Rada B 1–2:101–109
Swofford DL (2003) PAUP*: Phylogenetic analysis using parsimony (* and other methods). Version 4b10. Sinauer Associates. Sunderland, Massachusetts
Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Pl Molec Biol 17:1105–1109
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
Vassiljeva AN (1969) Critical notes on the genus Parrya R. Br. Notul Syst Herb Inst Bot Acad Sci KazSSR 6:27–31
Vassiljeva AN (1974) Commentationes de systematica generis Neuroloma Andrz. Notul Syst Herb Inst Bot Acad Sci KazSSR 8:27–31
Warwick SI, Al-Shehbaz IA (2006) Brassicaceae: chromosome number index and database on CD-ROM. Pl Syst Evol 259:237–248
Warwick SI, Sauder C (2005) Phylogeny of tribe Brassiceae (Brassicaceae) based on chloroplast restriction site polymorphisms and nuclear ribosomal internal transcribed spacer and chloroplast trnL intron sequences. Canad J Bot 83:467–483
Warwick SI, Al-Shehbaz IA, Sauder C, Harris JG, Koch M (2004a) Phylogeny of Braya and Neotorularia (Brassicaceae) based on nuclear ribosomal internal transcribed spacer and chloroplast trnL intron sequences. Canad J Bot 82:376–392
Warwick SI, Al-Shehbaz IA, Sauder C, Murray DF, Mummenhoff K (2004b) Phylogeny of Smelowskia and related genera (Brassicaceae) based on nuclear ITS DNA and chloroplast trnL intron sequences. Ann Mo Bot Gard 91:99–123
Warwick SI, Francis A, Al-Shehbaz IA (2006a) Brassicaceae: checklist and database on CD-ROM. Pl Syst Evol 259:249–258
Warwick SI, Sauder CA, Al-Shehbaz IA (2006b) 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 219–250
Warwick SI, Sauder CA, Al-Shehbaz IA, Jacquemoud F (2007) Phylogenetic relationships in the tribes Anchonieae, Chorisporeae, Euclidieae, and Hesperideae (Brassicaceae) based on nuclear ribosomal ITS DNA sequences. Ann Mo Bot Gard 94:56–78
Warwick SI, Mummenhoff K, Sauder CA, Koch MA, Al-Shehbaz IA (2010) Closing the gaps: phylogenetic relationships in the Brassicaceae based on DNA sequence data of nuclear ribosomal ITS region. Pl Syst Evol 285:209–232
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 315–322
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 93:402–411
Yue JP, 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 95:520–538
Yue JP, Sun H, Baum DA, Li JH, Al-Shehbaz IA, Ree R (2009) Molecular phylogeny of Solms-laubachia (Brassicaceae) s.l., based on multiple nuclear and plastid DNA sequences, and its biogeographic implications. J Syst Evol 47(5):204–411
Zhao B, Liu L, Tan D, Wang J (2010) Analysis of phylogenetic relationships of Brassicaceae species based Chs sequences. Biochem Syst Ecol 38:731–739
Zhou TY, Lu LL, Yang G, Al-Shehbaz IA (2001) Brassicaceae (Cruciferae). In: Wu ZY, Raven PH (eds) Flora of China 8, Science Press, Beijing, and Missouri Botanical Garden Press, St Louis, 1–193
Acknowledgments
Financial support for stay of the first author at the Department of Functional Genomics and Proteomics of Masaryk University was provided by the South Moravian Region (project “Brain”). This work was supported by research grants from the Grant Agency of the Czech Academy of Science (IAA601630902) and the Czech Ministry of Education (MSM0021622415). Fieldwork was supported by the National Geographic Foundation of the USA (grant no. 8773-10). We thank the curators and directors of the herbaria, as well as A.Y. Korolyuk, A.L. Ebel, G.A. Lazkov, S.V. Smirnov, H. Hurka, H. Moazzeni, and K. Mummenhoff, for supplying plant material. Two anonymous reviewers are highly appreciated for valuable comments and notes.
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Supplementary material 1 Results of parsimony analysis of ITS including the strict consensus of 10,000 MPTs and results of bootstrap and jackknife analyses. (PDF 96 kb)
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Supplementary material 2 Results of parsimony analysis of trnL-F including the strict consensus of 10,000 MPTs and results of bootstrap and jackknife analyses. (PDF 84 kb)
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German, D.A., Grant, J.R., Lysak, M.A. et al. Molecular phylogeny and systematics of the tribe Chorisporeae (Brassicaceae). Plant Syst Evol 294, 65–86 (2011). https://doi.org/10.1007/s00606-011-0452-0
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DOI: https://doi.org/10.1007/s00606-011-0452-0