The Brassicaceae include several major crop plants and numerous important model species in comparative evolutionary research such as Arabidopsis, Brassica, Boechera, Thellungiella, and Arabis species. As any evolutionary hypothesis needs to be placed in a temporal context, reliably dated major splits within the evolution of Brassicaceae are essential. We present a comprehensive time-calibrated framework with important divergence time estimates based on whole-chloroplast sequence data for 29 Brassicaceae species. Diversification of the Brassicaceae crown group started at the Eocene-to-Oligocene transition. Subsequent major evolutionary splits are dated to ∼20 million years ago, coinciding with the Oligocene-to-Miocene transition, with increasing drought and aridity and transient glaciation events. The age of the Arabidopsis thaliana crown group is 6 million years ago, at the Miocene and Pliocene border. The overall species richness of the family is well explained by high levels of neopolyploidy (43% in total), but this trend is neither directly associated with an increase in genome size nor is there a general lineage-specific constraint. Our results highlight polyploidization as an important source for generating new evolutionary lineages adapted to changing environments. We conclude that species radiation, paralleled by high levels of neopolyploidization, follows genome size decrease, stabilization, and genetic diploidization.

Central European Institute of Technology Masaryk University Brno 625 00 Czech Republic

Centre for Organismal Studies Heidelberg Heidelberg University 69120 Heidelberg Germany

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Aliyu O.M., Schranz M.E., Sharbel T.F. (2010). Quantitative variation for apomictic reproduction in the genus Boechera (Brassicaceae). Am. J. Bot. 97: 1719–1731. PubMed

Al-Shehbaz I.A. (2012). A generic and tribal synopsis of the Brassicaceae (Cruciferae). Taxon 61: 931–954.

Al-Shehbaz I.A., Beilstein M.A., Kellogg E.A. (2006). Systematics and phylogeny of the Brassicaceae (Cruciferae): an overview. Plant Syst. Evol. 259: 89–120.

Amborella Genome Project (2013). The Amborella genome and the evolution of flowering plants. Science 342: 1241089. PubMed

Appel O., Al-Shehbaz I.A. (2002). Cruciferae. In The Families and Genera of Vascular Plants, Vol. V, Kubitzki K., ed (Heidelberg, Germany: Springer Berlin; ), pp. 75–174.

Arias T., Pires J.C. (2012). A fully resolved chloroplast phylogeny of the brassica crops and wild relatives (Brassicaceae: Brassiceae): Novel clades and potential taxonomic implications. Taxon 61: 980–988.

Arias T., Beilstein M.A., Tang M., McKain M.R., Pires J.C. (2014). Diversification times among Brassica (Brassicaceae) crops suggest hybrid formation after 20 million years of divergence. Am. J. Bot. 101: 86–91. PubMed

Arrigo N., Barker M.S. (2012). Rarely successful polyploids and their legacy in plant genomes. Curr. Opin. Plant Biol. 15: 140–146. PubMed

Azim M.K., Khan I.A., Zhang Y. (2014). Characterization of mango (Mangifera indica L.) transcriptome and chloroplast genome. Plant Mol. Biol. 85: 193–208. PubMed

Bailey C.D., Koch M.A., Mayer M., Mummenhoff K., O’Kane S.L. Jr., Warwick S.I., Windham M.D., Al-Shehbaz I.A. (2006). Toward a global phylogeny of the Brassicaceae. Mol. Biol. Evol. 23: 2142–2160. PubMed

Becker H.F. (1961). Oligocene plants from the upper Ruby river basin, southwestern Montana. GSA Memoirs 82: 1–122.

Beilstein M.A., Al-Shehbaz I.A., Kellogg E.A. (2006). Brassicaceae phylogeny and trichome evolution. Am. J. Bot. 93: 607–619. PubMed

Beilstein M.A., Nagalingum N.S., Clements M.D., Manchester S.R., Mathews S. (2010). Dated molecular phylogenies indicate a Miocene origin for Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 107: 18724–18728. PubMed PMC

Benedict J.C., DeVore M.L., Pigg K.B. (2011). Prunus and Oemleria (Rosaceae) flowers from the late early Eocene Republic flora of northeastern Washington state, USA. Int. J. Plant Sci. 172: 948–958.

Bennett M.D., Leitch I.J., Price H.J., Johnston J.S. (2003). Comparisons with Caenorhbditis (∼100 Mb) and Drosophila (∼175 Mb) using flow cytometry show genome size in Arabidopsis to be ∼157 Mb and thus ∼25% larger than the Arabidopsis Genome Initiative estimates of ∼125 Mb. Ann. Bot. (Lond.) 91: 1–11. PubMed PMC

Blondel J., Aronson J., Bodiou J.Y., Boeuf G. (2010). The Mediterranean Region: Biological Diversity through Time and Space. (Oxford, UK: Oxford University Press; ).

Bowers J.E., Chapman B.A., Rong J., Paterson A.H. (2003). Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422: 433–438. PubMed

Braby M.F., Trueman J.W.H. (2006). Evolution of larval host plant associations and adaptive radiation in pierid butterflies. J. Evol. Biol. 19: 1677–1690. PubMed

Burrell A.M., Taylor K.G., Williams R.J., Cantrell R.T., Menz M.A., Pepper A.E. (2011). A comparative genomic map for Caulanthus amplexicaulis and related species (Brassicaceae). Mol. Ecol. 20: 784–798. PubMed

Castresana J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17: 540–552. PubMed

Cheng F., Mandáková T., Wu J., Xie Q., Lysak M.A., Wang X. (2013). Deciphering the diploid ancestral genome of the Mesohexaploid Brassica rapa. Plant Cell 25: 1541–1554. PubMed PMC

Couvreur T.L., Franzke A., Al-Shehbaz I.A., Bakker F.T., Koch M.A., Mummenhoff K. (2010). Molecular phylogenetics, temporal diversification, and principles of evolution in the mustard family (Brassicaceae). Mol. Biol. Evol. 27: 55–71. PubMed

De Bodt S., Maere S., Van de Peer Y. (2005). Genome duplication and the origin of angiosperms. Trends Ecol. Evol. (Amst.) 20: 591–597. PubMed

DeVries P.J. (2001). Butterflies. In The Encyclopedia of Biodiversity, I–V, Levin S.A., ed (San Diego, CA: Academic Press; ), pp. 559–573.

Doležel J., Bartoš J. (2005). Plant DNA flow cytometry and estimation of nuclear genome size. Ann. Bot. (Lond.) 95: 99–110. PubMed PMC

Doležel J., Binarová P., Lucretti S. (1989). Analysis of nuclear DNA content in plant cells by flow cytometry. Biol. Plant. 31: 113–120.

Doležel J., Greilhuber J., Suda J. (2007). Estimation of nuclear DNA content in plants using flow cytometry. Nat. Protoc. 2: 2233–2244. PubMed

Doležel J., Sgorbati S., Lucretti S. (1992). Comparison of three fluorochromes for flow cytometric estimation of nuclear DNA content in plants. Physiol. Plant. 85: 625–631.

Drummond A.J., Ho S.Y.W., Phillips M.J., Rambaut A. (2006). Relaxed phylogenetics and dating with confidence. PLoS Biol. 4: e88. PubMed PMC

Drummond A.J., Suchard M.A., Xie D., Rambaut A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29: 1969–1973. PubMed PMC

Eckardt N.A. (2006). Functional Divergence of AP3 Genes in the MAD World of Flower Development. Plant Cell 18: 1779–1781.

Edger P.P., et al. (2015). The butterfly plant arms-race escalated by gene and genome duplications. Proc. Natl. Acad. Sci. USA 112: 8362–8366. PubMed PMC

Ehrendorfer F. (1980). Polyploidy and distribution. In Polyploidy. Biological Relevance, Lewis W.H., ed (New York, London: Plenum Press; ), pp. 45–59.

Ermolaeva M.D., Wu M., Eisen J.A., Salzberg S.L. (2003). The age of the Arabidopsis thaliana genome duplication. Plant Mol. Biol. 51: 859–866. PubMed

Fawcett J.A., Maere S., Van de Peer Y. (2009). Plants with double genomes might have had a better chance to survive the Cretaceous-Tertiary extinction event. Proc. Natl. Acad. Sci. USA 106: 5737–5742. PubMed PMC

Flagel L.E., Wendel J.F. (2009). Gene duplication and evolutionary novelty in plants. New Phytol. 183: 557–564. PubMed

Franzke A., German D., Al-Shehbaz I.A., Mummenhoff K. (2009). Arabidopsis family ties: molecular phylogeny and age estimates in Brassicaceae. Taxon 58: 425–437.

Franzke A., Koch M.A., Couvreur T.L.P., Lysak M.A., Mummenhoff K. (2010). On the age of the mustard family (Brassicaceae). Nature 467: 755.

Franzke A., Lysak M.A., Al-Shehbaz I.A., Koch M.A., Mummenhoff K. (2011). Cabbage family affairs: the evolutionary history of Brassicaceae. Trends Plant Sci. 16: 108–116. PubMed

Garcia-Castellanos D., Estrada F., Jiménez-Munt I., Gorini C., Fernàndez M., Vergés J., De Vicente R. (2009). Catastrophic flood of the Mediterranean after the Messinian salinity crisis. Nature 462: 778–781. PubMed

Garcia-Castellanos D., Villaseñor A. (2011). Messinian salinity crisis regulated by competing tectonics and erosion at the Gibraltar arc. Nature 480: 359–363. PubMed

Haudry A., et al. (2013). An atlas of over 90,000 conserved noncoding sequences provides insight into crucifer regulatory regions. Nat. Genet. 45: 891–898. PubMed

Hedge I.C. (1976). A systematic and geographical survey of the Old World Cruciferae. In The Biology and Chemistry of the Cruciferae, Vaughan J.G., Macleod A.J., Jones B.M.G., eds (London: Academic Press; ), pp. 1–45.

Henry Y., Bedhomme M., Blanc G. (2006). History, protohistory and prehistory of the Arabidopsis thaliana chromosome complement. Trends Plant Sci. 11: 267–273. PubMed

Hofberger J.A., Lyons E., Edger P.P., Chris Pires J., Eric Schranz M. (2013). Whole genome and tandem duplicate retention facilitated glucosinolate pathway diversification in the mustard family. Genome Biol. Evol. 5: 2155–2173. PubMed PMC

Hohmann N., Schmickl R., Chiang T.-Y., Lučanová M., Kolář F., Marhold K., Koch M.A. (2014). Taming the wild: resolving the gene pools of non-model Arabidopsis lineages. BMC Evol. Biol. 14: 224. PubMed PMC

Imbrie J., et al. (1993). On the structure and origin of major glaciation cycles 2. The 100,000‐year cycle. Paleoceanography 8: 699–735.

Jakobsson M., Hagenblad J., Tavaré S., Säll T., Halldén C., Lind-Halldén C., Nordborg M. (2006). A unique recent origin of the allotetraploid species Arabidopsis suecica: Evidence from nuclear DNA markers. Mol. Biol. Evol. 23: 1217–1231. PubMed

Jiao Y., et al. (2011). Ancestral polyploidy in seed plants and angiosperms. Nature 473: 97–100. PubMed

Jiao Y., et al. (2012). A genome triplication associated with early diversification of the core eudicots. Genome Biol. 13: R3. PubMed PMC

Joly S., Heenan P.B., Lockhart P.J. (2009). A Pleistocene inter-tribal allopolyploidization event precedes the species radiation of Pachycladon (Brassicaceae) in New Zealand. Mol. Phylogenet. Evol. 51: 365–372. PubMed

Jordon-Thaden I., Koch M. (2008). Species richness and polyploid patterns in the genus Draba (Brassicaceae): a first global perspective. Plant Ecol. Divers. 1: 255–263.

Jordon-Thaden I.E., Al-Shehbaz I.A., Koch M.A. (2013). Species richness of the globally distributed, arctic–alpine genus Draba L. (Brassicaceae). Alp. Bot. 123: 97–106.

Kagale S., Robinson S.J., Nixon J., Xiao R., Huebert T., Condie J., Kessler D., Clarke W.E., Edger P.P., Links M.G., Sharpe A.G., Parkin I.A.P. (2014). Polyploid evolution of the Brassicaceae during the Cenozoic era. Plant Cell 26: 2777–2791. PubMed PMC

Karl R., Koch M.A. (2013). A world-wide perspective on crucifer speciation and evolution: phylogenetics, biogeography and trait evolution in tribe Arabideae. Ann. Bot. (Lond.) 112: 983–1001. PubMed PMC

Katoh K., Kuma K., Toh H., Miyata T. (2005). MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 33: 511–518. PubMed PMC

Katoh K., Misawa K., Kuma K., Miyata T. (2002). MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30: 3059–3066. PubMed PMC

Kelly L.J., et al. (2015). Analysis of the giant genomes of Fritillaria (Liliaceae) indicates that a lack of DNA removal characterizes extreme expansions in genome size. New Phytol. 8: http://dx.doi.org/10.1111/nph.13471. PubMed DOI PMC

Kiefer C., Dobeš C., Koch M.A. (2009a). Boechera or not? Phylogeny and phylogeography of eastern North American Boechera species (Brassicaceae). Taxon 58: 1109–1121.

Kiefer C., Dobeš C., Sharbel T.F., Koch M.A. (2009b). Phylogeographic structure of the chloroplast DNA gene pool in North American Boechera--a genus and continental-wide perspective. Mol. Phylogenet. Evol. 52: 303–311. PubMed

Kiefer C., Koch M.A. (2012). A continental-wide perspective: the genepool of nuclear encoded ribosomal DNA and single-copy gene sequences in North American Boechera (Brassicaceae). PLoS One 7: e36491. PubMed PMC

Kiefer M., Schmickl R., German D.A., Mandáková T., Lysak M.A., Al-Shehbaz I.A., Franzke A., Mummenhoff K., Stamatakis A., Koch M.A. (2014). BrassiBase: introduction to a novel knowledge database on Brassicaceae evolution. Plant Cell Physiol. 55: e3. PubMed

Knobloch E.D., Mai D.H. (1986). Monograph of the fruits and seeds in the Cretaceous of Central Europe. Rozpravy Ústreõdního Ústavu Geologickéh 47: 1–219.

Koch M. (2002). Genetic differentiation and speciation in prealpine Cochlearia: Allohexaploid Cochlearia bavarica Vogt (Brassicaceae) compared to its diploid ancestor Cochlearia pyrenaica DC. in Germany and Austria. Plant Syst. Evol. 232: 35–49.

Koch M., Bishop J., Mitchell‐Olds T. (1999). Molecular systematics and evolution of Arabidopsis and Arabis. Plant Biol. 1: 529–537.

Koch M., Haubold B., Mitchell-Olds T. (2001). Molecular systematics of the Brassicaceae: evidence from coding plastidic matK and nuclear Chs sequences. Am. J. Bot. 88: 534–544. PubMed

Koch M., Huthmann M., Hurka H. (1998). Isozymes, speciation and evolution in the polyploid complex Cochlearia L. (Brassicaceae). Bot. Acta 111: 411–425.

Koch M., Al-Shehbaz I.A., Mummenhoff K. (2003). Molecular systematics, evolution, and population biology in the mustard family (Brassicaceae). Ann. Mo. Bot. Gard. 90: 151–171.

Koch M.A. (2012). Mid-Miocene divergence of Ionopsidium and Cochlearia and its impact on the systematics and biogeography of the tribe Cochlearieae (Brassicaceae). Taxon 61: 76–92.

Koch M.A., Al-Shehbaz I.A. (2009). Molecular systematics and evolution of “wild” crucifers (Brassicaceae or Cruciferae). In Biology and Breeding of Crucifers, S.K. Gupta, ed (Boca Raton, FL: Taylor and Francis Group; ), pp. 1–19.

Koch M.A., Dobeš C., Kiefer C., Schmickl R., Klimes L., Lysak M.A. (2007). Supernetwork identifies multiple events of plastid trnF(GAA) pseudogene evolution in the Brassicaceae. Mol. Biol. Evol. 24: 63–73. PubMed

Koch M.A., German D.A. (2013). Taxonomy and systematics are key to biological information: Arabidopsis, Eutrema (Thellungiella), Noccaea and Schrenkiella (Brassicaceae) as examples. Front. Plant Sci. 4: 267. PubMed PMC

Koch M.A., Haubold B., Mitchell-Olds T. (2000). Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae). Mol. Biol. Evol. 17: 1483–1498. PubMed

Koch M.A., Kiefer C. (2006). Molecules and migration: biogeographical studies in cruciferous plants. Plant Syst. Evol. 259: 121–142.

Koch M.A., Kiefer M., German D.A., Al-Shehbaz I.A., Franzke A., Mummenhoff K., Schmickl R. (2012). BrassiBase: Tools and biological resources to study characters and traits in the Brassicaceae—version 1.1. Taxon 61: 1001–1009.

Koch M.A., Matschinger M. (2007). Evolution and genetic differentiation among relatives of Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 104: 6272–6277. PubMed PMC

Koch M.A., Wernisch M., Schmickl R. (2008). Arabidopsis thaliana’s wild relatives: an updated overview on systematics, taxonomy and evolution. Taxon 57: 933.

Lanfear R., Calcott B., Kainer D., Mayer C., Stamatakis A. (2014). Selecting optimal partitioning schemes for phylogenomic datasets. BMC Evol. Biol. 14: 82. PubMed PMC

Lanfear R., Calcott B., Ho S.Y., Guindon S. (2012). Partitionfinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol. Biol. Evol. 29: 1695–1701. PubMed

Leitch I.J., Bennett M.D. (2007). Genome size and its uses: the impact of flow cytometry. In Flow Cytometry with Plant Cells, J. Doležel, J. Greilhuber, and J. Suda, eds (Weinheim, Germany: Wiley-VCH Verlag), pp. 153–176.

Leitch I.J., Bennett M.D. (2004). Genome downsizing in polyploid plants. Biol. J. Linn. Soc. Lond. 82: 651–663.

Leitch A.R., Leitch I.J. (2008). Genomic plasticity and the diversity of polyploid plants. Science 320: 481–483. PubMed

Lim K.Y., Kovarik A., Matyasek R., Chase M.W., Clarkson J.J., Grandbastien M.A., Leitch A.R. (2007). Sequence of events leading to near-complete genome turnover in allopolyploid Nicotiana within five million years. New Phytol. 175: 756–763. PubMed

Lysak M.A., Berr A., Pecinka A., Schmidt R., McBreen K., Schubert I. (2006). Mechanisms of chromosome number reduction in Arabidopsis thaliana and related Brassicaceae species. Proc. Natl. Acad. Sci. USA 103: 5224–5229. PubMed PMC

Lysak M.A., Koch M.A. (2011). Phylogeny, genome, and karyotype evolution of crucifers (Brassicaceae). In Genetics and Genomics of the Brassicaceae, Schmidt R., Bancroft I., eds (New York: Springer; ), pp. 1–31.

Lysak M.A., Koch M.A., Beaulieu J.M., Meister A., Leitch I.J. (2009). The dynamic ups and downs of genome size evolution in Brassicaceae. Mol. Biol. Evol. 26: 85–98. PubMed

Lysak M.A., Koch M.A., Pecinka A., Schubert I. (2005). Chromosome triplication found across the tribe Brassiceae. Genome Res. 15: 516–525. PubMed PMC

Magallón S., Gómez‐Acevedo S., Sánchez‐Reyes L.L., Hernández‐Hernández T. (2015). A metacalibrated time‐tree documents the early rise of flowering plant phylogenetic diversity. New Phytol. 207: 437–453. PubMed

Mandáková T., Heenan P.B., Lysak M.A. (2010b). Island species radiation and karyotypic stasis in Pachycladon allopolyploids. BMC Evol. Biol. 10: 367. PubMed PMC

Mandáková T., Joly S., Krzywinski M., Mummenhoff K., Lysak M.A. (2010a). Fast diploidization in close mesopolyploid relatives of Arabidopsis. Plant Cell 22: 2277–2290. PubMed PMC

Mandáková T., Lysak M.A. (2008). Chromosomal phylogeny and karyotype evolution in x=7 crucifer species (Brassicaceae). Plant Cell 20: 2559–2570. PubMed PMC

Mandáková T., Mummenhoff K., Al-Shehbaz I.A., Mucina L., Mühlhausen A., Lysak M.A. (2012). Whole-genome triplication and species radiation in the southern African tribe Heliophileae (Brassicaceae). Taxon 61: 989–1000.

Mandáková T., Schranz M.E., Sharbel T.F., de Jong H., Lysak M.A. (2015). Karyotype evolution in apomictic Boechera and the origin of the aberrant chromosomes. Plant J. 82: 785–793. PubMed

Mau M., Lovell J.T., Corral J.M., Kiefer C., Koch M.A., Aliyu O.M., McKay J., Sharbel T.F. (2015). Hybrid apomicts trapped in the ecological niches of their sexual ancestors. Proc. Natl. Acad. Sci. USA 112: E2357–E2365. PubMed PMC

Mayrose I., Zhan S.H., Rothfels C.J., Magnuson-Ford K., Barker M.S., Rieseberg L.H., Otto S.P. (2011). Recently formed polyploid plants diversify at lower rates. Science 333: 1257. PubMed

Ming R., et al. (2008). The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus). Nature 452: 991–996. PubMed PMC

Moore M.J., Soltis P.S., Bell C.D., Burleigh J.G., Soltis D.E. (2010). Phylogenetic analysis of 83 plastid genes further resolves the early diversification of eudicots. Proc. Natl. Acad. Sci. USA 107: 4623–4628. PubMed PMC

Mummenhoff K., Franzke A., Koch M. (1997). Molecular data reveal convergence in fruit characters used in the classification of Thlaspi s.l. (Brassicaceae). Bot. J. Linn. Soc. 125: 183–199.

Mummenhoff K., Polster A., Mühlhausen A., Theissen G. (2009). Lepidium as a model system for studying the evolution of fruit development in Brassicaceae. J. Exp. Bot. 60: 1503–1513. PubMed

Müller K., Quandt D., Müller J., Neinhuis C. (2010). PhyDE, Version 0.9971: Phylogenetic Data Editor. Available at http://www.phyde.de.

Njuguna W., Liston A., Cronn R., Ashman T.-L., Bassil N. (2013). Insights into phylogeny, sex function and age of Fragaria based on whole chloroplast genome sequencing. Mol. Phylogenet. Evol. 66: 17–29. PubMed

Paradis E., Claude J., Strimmer K. (2004). APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20: 289–290. PubMed

Pauwels M., Vekemans X., Godé C., Frérot H., Castric V., Saumitou-Laprade P. (2012). Nuclear and chloroplast DNA phylogeography reveals vicariance among European populations of the model species for the study of metal tolerance, Arabidopsis halleri (Brassicaceae). New Phytol. 193: 916–928. PubMed

Roux C., Castric V., Pauwels M., Wright S.I., Saumitou-Laprade P., Vekemans X. (2011). Does speciation between Arabidopsis halleri and Arabidopsis lyrata coincide with major changes in a molecular target of adaptation? PLoS One 6: e26872. PubMed PMC

Rögl F. (1999). Mediterranean and Paratethys. Facts and hypotheses of an Oligocene to Miocene paleogeography (short overview). Geologica Carpathica 50: 339–349.

Ruhfel B.R., Gitzendanner M.A., Soltis P.S., Soltis D.E., Burleigh J.G. (2014). From algae to angiosperms-inferring the phylogeny of green plants (Viridiplantae) from 360 plastid genomes. BMC Evol. Biol. 14: 23. PubMed PMC

Schmickl R., Jørgensen M.H., Brysting A.K., Koch M.A. (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. PubMed PMC

Schmickl R., Paule J., Klein J., Marhold K., Koch M.A. (2012). The evolutionary history of the Arabidopsis arenosa complex: diverse tetraploids mask the Western Carpathian center of species and genetic diversity. PLoS One 7: e42691. PubMed PMC

Schranz M.E., Lysak M.A., Mitchell-Olds T. (2006). The ABC’s of comparative genomics in the Brassicaceae: building blocks of crucifer genomes. Trends Plant Sci. 11: 535–542. PubMed

Schranz M.E., Mitchell-Olds T. (2006). Independent ancient polyploidy events in the sister families Brassicaceae and Cleomaceae. Plant Cell 18: 1152–1165. PubMed PMC

Schranz M.E., Mohammadin S., Edger P.P. (2012). Ancient whole genome duplications, novelty and diversification: the WGD Radiation Lag-Time Model. Curr. Opin. Plant Biol. 15: 147–153. PubMed

Sims H.J., Herendeen P.S., Lupia R., Christopher R.A., Crane P.R. (1999). Fossil flowers with Normapolles pollen from the Upper Cretaceous of southeastern North America. Rev. Palaeobot. Palynol. 106: 131–151.

Soltis D.E., Albert V.A., Leebens-Mack J., Bell C.D., Paterson A.H., Zheng C., Sankoff D., Depamphilis C.W., Wall P.K., Soltis P.S. (2009). Polyploidy and angiosperm diversification. Am. J. Bot. 96: 336–348. PubMed

Soltis P.S., Liu X., Marchant D.B., Visger C.J., Soltis D.E. (2014). Polyploidy and novelty: Gottlieb’s legacy. Philos. Trans. R. Soc. Lond. B Biol. Sci. 369: 20130351. PubMed PMC

Soltis D.E., Soltis P.S., Schemske D.W., Hancock J.F., Thompson J.N., Husband B.C., Judd W.S. (2007). Autopolyploidy in angiosperms: have we grossly underestimated the number of species? Taxon 56: 13–30.

Soltis D.E., Soltis P.S., Tate J.A. (2004). Advances in the study of polyploidy since plant speciation. New Phytol. 161: 173–191.

Stamatakis A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312–1313. PubMed PMC

Stebbins G.L., Jr. (1938). Cytological characteristics associated with the different growth habits in the dicotyledons. Am. J. Bot. 25: 189–198.

Stebbins G.L., Jr. (1950). Variation and Evolution in Plants. (London, UK: Oxford University Press; ).

Stevens P.F. (2001). Angiosperm Phylogeny Website 2001, onwards, Version 13. http://www.mobot.org/MOBOT/research/APweb/.

Takahashi M., Crane P.R., Ando H. (1999). Esgueiria futabensis sp. nov., a new angiosperm flower from the Upper Cretaceous (Lower Coniacian) of northeastern Honshu, Japan. Paleontological Research 3: 81–87.

Tang H., Bowers J.E., Wang X., Paterson A.H. (2010). Angiosperm genome comparisons reveal early polyploidy in the monocot lineage. Proc. Natl. Acad. Sci. USA 107: 472–477. PubMed PMC

Tank D.C., Eastman J.M., Pennell M.W., Soltis P.S., Soltis D.E., Hinchliff C.E., Brown J.W., Sessa E.B., Harmon L.J. (2015). Nested radiations and the pulse of angiosperm diversification: increased diversification rates often follow whole genome duplications. New Phytol. 207: 454–467. PubMed

Thompson J.D., Lavergne S., Affre L., Gaudeul M., Debussche M. (2005). Ecological differentiation of Mediterranean endemic plants. Taxon 54: 967–976.

Tsuchimatsu T., Kaiser P., Yew C.-L., Bachelier J.B., Shimizu K.K. (2012). Recent loss of self-incompatibility by degradation of the male component in allotetraploid Arabidopsis kamchatica. PLoS Genet. 8: e1002838. PubMed PMC

Vanneste K., Maere S., Van de Peer Y. (2014). Tangled up in two: a burst of genome duplications at the end of the Cretaceous and the consequences for plant evolution. Philos. Trans. R. Soc. Lond. B Biol. Sci. 369: 20130353. PubMed PMC

Velasco R., et al. (2010). The genome of the domesticated apple (Malus × domestica Borkh.). Nat. Genet. 42: 833–839. PubMed

Vision T.J., Brown D.G., Tanksley S.D. (2000). The origins of genomic duplications in Arabidopsis. Science 290: 2114–2117. PubMed

Wang X., et al. ; Brassica rapa Genome Sequencing Project Consortium (2011). The genome of the mesopolyploid crop species Brassica rapa. Nat. Genet. 43: 1035–1039. PubMed

Warren B.H., Hawkins J.A. (2006). The distribution of species diversity across a flora’s component lineages: dating the Cape’s ‘relicts’. Proc. Biol. Sci. 273: 2149–2158. PubMed PMC

Warwick S.I., Al-Shehbaz I.A. (2006). Brassicaceae: Chromosome number index and database on CD-Rom. Plant Syst. Evol. 259: 237–248.

Warwick S.I., Mummenhoff K., Sauder C., Koch M.A., Al-Shehbaz I.A. (2010). Closing the gaps: Phylogenetic relationships in the Brassicaceae based on DNA sequence data of nuclear ribosomal ITS region. Plant Syst. Evol. 285: 209–232.

Weiss-Schneeweiss H., Greilhuber J., Schneeweiss G.M. (2006). Genome size evolution in holoparasitic Orobanche (Orobanchaceae) and related genera. Am. J. Bot. 93: 148–156. PubMed

Wheat C.W., Vogel H., Wittstock U., Braby M.F., Underwood D., Mitchell-Olds T. (2007). The genetic basis of a plant-insect coevolutionary key innovation. Proc. Natl. Acad. Sci. USA 104: 20427–20431. PubMed PMC

Wing S.L. (1987). Eocene and Oligocene floras and vegetation of the Rocky Mountains. Ann. Mo. Bot. Gard. 74: 748–784.

Yang J., Song N., Zhao X., Qi X., Hu Z., Zhang M. (2014). Genome survey sequencing provides clues into glucosinolate biosynthesis and flowering pathway evolution in allotetraploid Brassica juncea. BMC Genomics 15: e107. PubMed PMC

Biased Retention of Environment-Responsive Genes Following Genome Fractionation

Impact of whole-genome duplications on structural variant evolution in Cochlearia

The evolution of the hypotetraploid Catolobus pendulus genome - the poorly known sister species of Capsella

An updated classification of the Brassicaceae (Cruciferae)

The evolutionary history of Cardamine bulbifera shows a successful rapid postglacial Eurasian range expansion in the absence of sexual reproduction

Genome diploidization associates with cladogenesis, trait disparity, and plastid gene evolution

Chloroplast phylogenomics in Camelina (Brassicaceae) reveals multiple origins of polyploid species and the maternal lineage of C. sativa

Gradual evolution of allopolyploidy in Arabidopsis suecica

Genomic basis of parallel adaptation varies with divergence in Arabidopsis and its relatives

Linked by Ancestral Bonds: Multiple Whole-Genome Duplications and Reticulate Evolution in a Brassicaceae Tribe

Nested whole-genome duplications coincide with diversification and high morphological disparity in Brassicaceae

Genomic Blocks in Aethionema arabicum Support Arabideae as Next Diverging Clade in Brassicaceae

Chromosomal Evolution and Apomixis in the Cruciferous Tribe Boechereae

Genome Evolution in Arabideae Was Marked by Frequent Centromere Repositioning

Evolution of Tandem Repeats Is Mirroring Post-polyploid Cladogenesis in Heliophila (Brassicaceae)

Interspecific introgression mediates adaptation to whole genome duplication

The large genome size variation in the Hesperis clade was shaped by the prevalent proliferation of DNA repeats and rarer genome downsizing

Monophyletic Origin and Evolution of the Largest Crucifer Genomes

Sequencing of the genus Arabidopsis identifies a complex history of nonbifurcating speciation and abundant trans-specific polymorphism

Repeated Whole-Genome Duplication, Karyotype Reshuffling, and Biased Retention of Stress-Responding Genes in Buckler Mustard