Abstract
Several lines of evidence suggest that homeotic changes played a considerable role during the evolution of flowers. This, however, is difficult to reconcile with the predominant evolutionary theory which rejects any drastic, saltational change of the phenotype as reasonable mode of evolution due to its assumed negative impact on the fitness of the affected organism. A better understanding of the evolutionary potential of homeotic transitions requires a study of the performance of respective mutant varieties in the wild. Here we introduce ``Stamenoid petals'' (Spe), a variety of Capsella bursa-pastoris (shepherd's purse), as a suitable model to study the evolutionary potential of floral homeotic mutants. In the flowers of the Spe variety all petals are transformed into stamens, while all other floral organs are unaffected. In contrast to most other homeotic mutants the Spe variety occurs on several locations in relatively large and stable populations in the wild. Due to its close relationship to the model plant Arabidopsis thaliana, the Spe variety of C. bursa-pastoris can be rigorously studied, from the molecular genetic basis of the phenotype to its consequences on the fitness in wild habitats. Investigations on Spe may thus help to clarify whether homeotic transformations have the potential to contribute to macroevolution.
Similar content being viewed by others
References
A. Acarkan M. Roßberg M. Koch R. Schmidt (2000) ArticleTitleComparative genome analysis reveals extensive conservation of genome organisation for Arabidopsis thaliana and Capsella rubella Plant J. 23 55–62 Occurrence Handle10929101 Occurrence Handle1:CAS:528:DC%2BD3cXlvFWnsrw%3D Occurrence Handle10.1046/j.1365-313x.2000.00790.x
V. A. Albert M. H. G. Gustaffson Laurenzio L. Di (1998) Ontogenetic systematics, molecular developmental genetics, and the angiosperm petal D. E. Soltis P. S. Soltis J. J. Doyle (Eds) Molecular systematics of plants II Kluwer Academic Publishers Boston, USA 349–374
B. A. Ambrose S. Espinosa-Matías S. Vázquez-Santana F. Vergara-Silva E. Martínez J. Márquez-Guzmán E. R. Alvarez-Buylla (2006) ArticleTitleComparative developmental series of the Mexican triurids support a euanthial interpretation for the unusual reproductive axes of Lacandonia schismatica (Triuridaceae) Amer. J. Bot. 93 15–35
G. C. Angenent L. Colombo (1996) ArticleTitleMolecular control of ovule development Trends Pl. Sci. 1 228–232
Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815.
W. Arthur (2002) ArticleTitleThe emerging conceptual framework of evolutionary developmental biology Nature 415 757–764 Occurrence Handle11845200 Occurrence Handle1:CAS:528:DC%2BD38XhsFais70%3D
S. C. H. Barrett (2002) ArticleTitleThe evolution of plant sexual diversity Nat. Rev. Genet. 3 274–284 Occurrence Handle11967552 Occurrence Handle1:CAS:528:DC%2BD38XjtFOrtrk%3D Occurrence Handle10.1038/nrg776
R. M. Bateman W. A. DiMichele (2002) Generating and filtering major phenotypic novelties: neoGoldschmidtian saltation revisited Q. C. B. Cronk R. M. Bateman J. A. Hawkins (Eds) Developmental genetics and plant evolution Taylor & Francis London 109–159
D. A. Baum M. J. Donoghue (2002) Transference of function, heterotopy and the evolution of plant development Q. C. B. Cronk R. M. Bateman J. A. Hawkins (Eds) Developmental genetics and plant evolution Taylor & Francis London 52–69
A. Becker G. Theißen (2003) ArticleTitleThe major clades of MADS-box genes and their role in the development and evolution of flowering plants Molec. Phylogenet. Evol. 29 464–489 Occurrence Handle14615187 Occurrence Handle1:CAS:528:DC%2BD3sXovVWnur4%3D Occurrence Handle10.1016/S1055-7903(03)00207-0
K. Bomblies N. Dagenais D. Weigel (1999) ArticleTitleRedundant enhancers mediate transcriptional repression of AGAMOUS by APETALA2 Dev. Biol. 216 260–264 Occurrence Handle10588876 Occurrence Handle1:CAS:528:DyaK1MXnslCqsb0%3D Occurrence Handle10.1006/dbio.1999.9504
J. L. Bowman (1997) ArticleTitleEvolutionary conservation of angiosperm flower development at the molecular and genetic levels J. Biosci. 22 515–527
Bowman J. L. (2006) Comparative developmental genetics of the Brassicaceae. Pl. Syst. Evol. 259.
D. Bradley R. Carpenter H. Sommer N. Hartley E. Coen (1993) ArticleTitleComplementary floral homeotic phenotypes result from opposite orientations of a transposon at the plena locus of Antirrhinum Cell 72 85–95 Occurrence Handle8093684 Occurrence Handle1:CAS:528:DyaK3sXltlamu7g%3D Occurrence Handle10.1016/0092-8674(93)90052-R
S. B. Carroll (2001) ArticleTitleChance and necessity: the evolution of morphological complexity and diversity Nature 409 1102–1109 Occurrence Handle11234024 Occurrence Handle1:CAS:528:DC%2BD3MXhs1Gjur4%3D Occurrence Handle10.1038/35059227
E. Coen (2001) ArticleTitleGoethe and the ABC model of flower development C.R. Acad. Sci. Paris, Sciences de la vie 324 1–8
E. S. Coen E. M. Meyerowitz (1991) ArticleTitleThe war of the whorls: genetic interactions controlling flower development Nature 353 31–37 Occurrence Handle1715520 Occurrence Handle1:STN:280:DyaK3MzltFejtg%3D%3D Occurrence Handle10.1038/353031a0
J. Conner Z. Liu (2000) ArticleTitle LEUNIG, a putative transcriptional corepressor that regulates AGAMOUS expression during flower development Proc. Natl. Acad. Sci. USA 97 12902–12907 Occurrence Handle11058164 Occurrence Handle1:CAS:528:DC%2BD3cXotFyktr0%3D Occurrence Handle10.1073/pnas.230352397
M. Coquillat (1951) ArticleTitleSur les plants les plus communes de la surface du globe Bull. Mens. Soc. Linn. Lyon 20 165–170
P. Cubas C. Vincent E. Coen (1999) ArticleTitleAn epigenetic mutation responsible for natural variation in floral symmetry Nature 401 157–161 Occurrence Handle10490023 Occurrence Handle1:CAS:528:DyaK1MXlvFKhu7Y%3D Occurrence Handle10.1038/43657
K. V. O. Dahlgren (1919) ArticleTitleErblichkeitsversuche mit einer dekandrischen Capsella bursa-pastoris (L.) Svensk Bot. Tidskr. 13 48–60
C. Darwin (1876) The variation of animals and plants under domestication. 2nd ed D. Appleton New York
S. Bodt ParticleDe J. Raes Y. Peer ParticleVan de G. Theissen (2003) ArticleTitleAnd then there were many: MADS goes genomic Trends Pl. Sci. 8 475–483 Occurrence Handle10.1016/j.tplants.2003.09.006 Occurrence Handle1:CAS:528:DC%2BD3sXnvFShsro%3D
M. K. Deyholos L. E. Sieburth (2000) ArticleTitleSeparable whorl-specific expression and negative regulation by enhancer elements within the AGAMOUS second intron Plant Cell 12 1799–1810 Occurrence Handle11041877 Occurrence Handle1:CAS:528:DC%2BD3cXotFais7k%3D Occurrence Handle10.1105/tpc.12.10.1799
M. R. Dietrich (2003) ArticleTitleRichard Goldschmidt: hopeful monsters and other `heresies' Nature Rev. Genet. 4 68–74 Occurrence Handle1:CAS:528:DC%2BD38XpvVent7o%3D Occurrence Handle10.1038/nrg979 Occurrence Handle12509755
G. Ditta A. Pinyopich P. Robles S. Pelaz M. F. Yanofsky (2004) ArticleTitleThe SEP4 gene of Arabidopsis thaliana functions in floral organ and meristem identity Curr. Biol. 14 1935–1940 Occurrence Handle15530395 Occurrence Handle1:CAS:528:DC%2BD2cXpsVOrtrw%3D Occurrence Handle10.1016/j.cub.2004.10.028
G. N. Drews J. L. Bowman E. M. Meyerowitz (1991) ArticleTitleNegative regulation of the Arabidopsis homeotic gene AGAMOUS by the APETALA2 product Cell 65 991–1002 Occurrence Handle1675158 Occurrence Handle1:CAS:528:DyaK3MXksVehtbY%3D Occurrence Handle10.1016/0092-8674(91)90551-9
M. Egea-Cortines H. Saedler H. Sommer (1999) ArticleTitleTernary complex formation between the MADS-box proteins SQUAMOSA, DEFICIENS and GLOBOSA is involved in the control of floral architecture in Antirrhinum majus EMBO J. 18 5370–5379 Occurrence Handle10508169 Occurrence Handle1:CAS:528:DyaK1MXntFKqsLo%3D Occurrence Handle10.1093/emboj/18.19.5370
R. Favaro A. Pinyopich R. Battaglia M. Kooiker L. Borghi G. Ditta M. F. Yanofsky M. M. Kater L. Colombo (2003) ArticleTitleMADS-box protein complexes control carpel and ovule development in Arabidopsis Pl. Cell 15 2603–2611 Occurrence Handle1:CAS:528:DC%2BD3sXpt1Ortbk%3D Occurrence Handle10.1105/tpc.015123
S. Ferrario R. G. Immink G. C. Angenent (2004) ArticleTitleConservation and diversity in flower land Curr. Opin. Pl. Biol. 7 84–91 Occurrence Handle10.1016/j.pbi.2003.11.003
V. S. Ford L. D. Gottlieb (1992) ArticleTitle Bicalyx is a natural homeotic floral variant Nature 358 671–673 Occurrence Handle10.1038/358671a0
R. G. Franks C. Wang J. Z. Levin Z. Liu (2002) ArticleTitle SEUSS, a member of a novel family of plant regulatory proteins, repress floral homeotic gene expression with LEUNIG Development 129 253–263 Occurrence Handle11782418 Occurrence Handle1:CAS:528:DC%2BD38XovVahtA%3D%3D
M. J. Fray P. Puangsomlee J. Goodrich G. Coupland E. J. Evans A. E. Arthur D. J. Lydiate (1997) ArticleTitleThe genetics of stamenoid petal production in oilseed rape (Brassica napus) and equivalent variant in Arabidopsis thaliana Theor. Appl. Genet. 94 731–736 Occurrence Handle1:CAS:528:DyaK2sXks1KrsbY%3D Occurrence Handle10.1007/s001220050472
S. F. Gilbert J. M. Opitz R. A. Raff (1996) ArticleTitleResynthesizing evolutionary and developmental biology Dev. Biol. 173 357–372 Occurrence Handle8605997 Occurrence Handle1:CAS:528:DyaK28Xps1CksA%3D%3D Occurrence Handle10.1006/dbio.1996.0032
J. Goodrich P. Puangsomlee M. Martin D. Long E. Meyerowitz G. Coupland (1997) ArticleTitleA Polycomb-group gene regulates gene expression in Arabidopsis Nature 386 44–51 Occurrence Handle9052779 Occurrence Handle1:CAS:528:DyaK2sXhslChsLs%3D Occurrence Handle10.1038/386044a0
W. Gottschalk (1971) Die Bedeutung der Genmutation für die Evolution der Pflanze Gustav Fischer Stuttgart
S. J. Gould (1977) Ontogeny and phylogeny Harvard University Press Cambridge, MA, USA
E. S. Haag J. R. True (2001) ArticleTitleFrom mutants to mechanisms? Assessing the candidate gene paradigm in evolutionary biology Evolution 55 1077–1084 Occurrence Handle11475043 Occurrence Handle1:CAS:528:DC%2BD3MXlvVGrtbk%3D
T. A. Hill C. D. Day S. C. Zondlo A. G. Thackeray V. F. Irish (1998) ArticleTitleDiscrete spatial and temporal cis-acting elements regulate transcription of the Arabidopsis floral homeotic gene APETALA3 Development 125 1711–1721 Occurrence Handle9521909 Occurrence Handle1:CAS:528:DyaK1cXjslels70%3D
M. H. Hoffmann M. Bremer K. Schneider F. Burger E. Stolle G. Moritz (2003) ArticleTitleFlower visitors in a natural population of Arabidopsis thaliana Pl. Biol. 5 491–494 Occurrence Handle10.1055/s-2003-44784
T. Honma K. Goto (2001) ArticleTitleComplexes of MADS-box proteins are sufficient to convert leaves into floral organs Nature 409 525–529 Occurrence Handle11206550 Occurrence Handle1:CAS:528:DC%2BD3MXpvVentg%3D%3D Occurrence Handle10.1038/35054083
H. Hurka S. Freundner A. H. D. Brown U. Plantholt (1989) ArticleTitleAspartat aminotransferase isozymes in the genus Capsella (Brassicaceae): subcellular location, gene duplication and polymorphism Biochem. Genet. 27 77–90 Occurrence Handle2712824 Occurrence Handle1:CAS:528:DyaL1MXhvV2lsL8%3D Occurrence Handle10.1007/BF00563019
H. Hurka S. Düring (1994) ArticleTitleGenetic control of plastidic L-glutamate dehydrogenase isozymes in the genus Capsella (Brassicaceae) Heredity 72 126–131 Occurrence Handle1:CAS:528:DyaK2cXjtF2mu7k%3D
H. Hurka B. Neuffer (1997) ArticleTitleEvolutionary processes in the genus Capsella (Brassicaceae) Pl. Syst. Evol. 206 295–316 Occurrence Handle10.1007/BF00987954
H. Hurka W. Bleeker B. Neuffer (2003) ArticleTitleEvolutionary process associated with biological invasions in the Brassicaceae Biol. Invasions 5 281–292 Occurrence Handle10.1023/B:BINV.0000005571.19401.81
H. Hurka M. Paetsch W. Bleeker B. Neuffer (2005) ArticleTitleEvolution within the Brassicaceae Nova Acta Leopoldina NF92, Nr. 342 113–127
H. H. Iltis (2000) ArticleTitleHomeotic sexual translocation and the origin of maize (Zea mays, Poaceae): a new look at an old problem Economic Bot. 54 7–42
T. Jack L. Sieburth E. Meyerowitz (1997) ArticleTitleTargeted misexpression of AGAMOUS in whorl 2 of Arabidopsis flowers Plant J. 11 825–839 Occurrence Handle9161038 Occurrence Handle1:CAS:528:DyaK2sXjs1Clu70%3D Occurrence Handle10.1046/j.1365-313X.1997.11040825.x
A. Kanno H. Saeki T. Kameya H. Saedler G. Theißen (2003) ArticleTitleHeterotopic expression of class B floral homeotic genes supports a modified ABC model for tulip (Tulipa gesneriana) Pl. Molec. Biol. 52 831–841 Occurrence Handle1:CAS:528:DC%2BD3sXmtVentbk%3D Occurrence Handle10.1023/A:1025070827979
E. A. Kellogg (2000) ArticleTitleThe grasses: A case study in macroevolution Annual Rev. Ecol. Syst. 31 217–238 Occurrence Handle10.1146/annurev.ecolsys.31.1.217
M. A. Koch M. Kiefer (2005) ArticleTitleGenome evolution among Cruciferous plants: a lecture from the comparison of the genetic maps of three diploid species – Capsella rubella, Arabidopsis lyrata ssp. petraea, and A. thaliana Amer. J. Bot. 92 761–767
E. M. Kramer Stilio V. S. Di P. M. Schluter (2003) ArticleTitleComplex patterns of gene duplication in the APETALA3 and PISTILLATA lineages of the Ranunculaceae Intern. J. Pl. Sci. 164 1–11 Occurrence Handle1:CAS:528:DC%2BD3sXhslOhurs%3D Occurrence Handle10.1086/344694
B. A. Krizek J. C. Fletcher (2005) ArticleTitleMolecular mechanisms of flower development: An armchair guide Nature Rev. Genet. 6 688–698 Occurrence Handle1:CAS:528:DC%2BD2MXps1erur8%3D Occurrence Handle10.1038/nrg1675 Occurrence Handle16151374
B. A. Krizek E. M. Meyerowitz (1996) ArticleTitleThe Arabidopsis homeotic genes APETALA3 and PISTILLATA are sufficient to provide the B class organ identity function Development 122 11–22 Occurrence Handle8565821 Occurrence Handle1:CAS:528:DyaK28XnvVWmug%3D%3D
J.-Y. Lee K. Mummenhoff J. L. Bowman (2002) ArticleTitleAllopolyploidization and evolution of species with reduced floral structures in Lepidium L. (Brassicaceae) Proc. Natl. Acad. Sci. USA 99 16835–16840 Occurrence Handle12481035 Occurrence Handle1:CAS:528:DC%2BD3sXhvV2gtg%3D%3D Occurrence Handle10.1073/pnas.242415399
E. B. Lewis (1994) ArticleTitleHomeosis: the first 100 years Trends Genet. 10 341–343 Occurrence Handle7985234 Occurrence Handle1:STN:280:DyaK2M%2Fns1Gitw%3D%3D Occurrence Handle10.1016/0168-9525(94)90117-1
Z. Liu E. M. Meyerowitz (1995) ArticleTitle LEUNIG regulates AGAMOUS expression in Arabidopsis flowers Development 121 975–991 Occurrence Handle7743940 Occurrence Handle1:CAS:528:DyaK2MXltVamtLk%3D
Z. Liu R.G. Franks V.P. Klink (2000) ArticleTitleRegulation of gynoecium marginal tissue formation by LEUNIG and AINTEGUMENTA Plant Cell 12 1879–1892 Occurrence Handle11041883 Occurrence Handle1:CAS:528:DC%2BD3cXotFaisL0%3D Occurrence Handle10.1105/tpc.12.10.1879
B. K. Mable A. V. Robertson S. Dart Berardo C. di L. Witham (2005) ArticleTitleBreakdown of self-incompatibility in the perennial Arabidopsis lyrata (Brassicaceae) and its genetic consequences Evolution 59 1437–1448 Occurrence Handle16153030
M. T. Masters (1869) Vegetable teratology: an account of the principle deviations from the usual construction of plants Ray Society London
R. Mauricio (2001) ArticleTitleMapping quantitative trait loci in plants: uses and caveats for evolutionary biology Nature Rev. Genet. 2 370–381 Occurrence Handle1:CAS:528:DC%2BD3MXjtlGjsLg%3D Occurrence Handle10.1038/35072085 Occurrence Handle11331903
E. M. Meyerowitz D. R. Smyth J. L. Bowman (1989) ArticleTitleAbnormal flowers and pattern formation in floral development Development 106 209–217
T. Mitchell-Olds (2001) ArticleTitle Arabidopsis thaliana and its wild relatives: a model system for ecology and evolution Trends Ecol. Evol. 16 693–700 Occurrence Handle10.1016/S0169-5347(01)02291-1
Murbeck S. V. (1918) Über staminale Pseudapetalie und deren Bedeutung für die Frage nach der Herkunft der Blütenkrone. Lunds Universitets Arsskrift N.F. Avd. 2, Bd. 14, Nr. 25, Lund.
Opiz P. M. (1821) 2. Capsella apetala Opiz. Eine neue merkwürdige Pflanze. Flora Nr. 28, oder: Botanische Zeitung, Regensburg, 28. Juli 1821.
S. Pelaz G. S. Ditta E. Baumann E. Wisman M. F. Yanofsky (2000) ArticleTitleB and C floral organ identity functions require SEPALLATA MADS-box genes Nature 405 200–203 Occurrence Handle10821278 Occurrence Handle1:CAS:528:DC%2BD3cXjsFyjsr0%3D Occurrence Handle10.1038/35012103
A. Pinyopich G. S. Ditta B. Savidge S. J. Liljegren E. Baumann E. Wisman M. F. Yanofsky (2003) ArticleTitleAssessing the redundancy of MADS-box genes during carpel and ovule development Nature 424 85–88 Occurrence Handle12840762 Occurrence Handle1:CAS:528:DC%2BD3sXltVelsbw%3D Occurrence Handle10.1038/nature01741
H. Reichert (1998) ArticleTitleEine kronblattlose Sippe des Hirtentäschels (Capsella bursa-pastoris) seit Jahren bestandsbildend bei Gau-Odernheim/Rheinhessen Hessische Floristische Rundbriefe 47 IssueID4 53–55
J. L. Riechmann E. M. Meyerowitz (1997) ArticleTitleMADS domain proteins in plant development Biol. Chem. 378 1079–1101 Occurrence Handle9372178 Occurrence Handle1:CAS:528:DyaK2sXmvFOju70%3D Occurrence Handle10.1515/bchm.1997.378.10.1079
R. Riedl (1977) ArticleTitleA systems-analytical approach to macro-evolutionary phenomena Quarterly Rev. Biol. 52 351–370 Occurrence Handle1:STN:280:DyaE1c7hs1CnsA%3D%3D Occurrence Handle10.1086/410123
De Craene L. P. Ronse (2003) ArticleTitleThe evolutionary significance of homeosis in flowers: a morphological perspective Int. J. Pl. Sci. 164 IssueID5 Suppl. S225–S230 Occurrence Handle10.1086/376878
P. J. Rudall (2003) ArticleTitleMonocot pseudanthia revisited: floral structure of the mycoheterotrophic family Triuridaceae Int. J. Pl. Sci. 164 IssueIDSuppl. 5 S307–S320 Occurrence Handle10.1086/376879
P. J. Rudall R. M. Bateman (2002) ArticleTitleRoles of synorganisation, zygomorphy and heterotopy in floral evolution: the gynostemium and labellum of orchids and other lilioid monocots Biol. Rev. 77 403–441 Occurrence Handle12227521 Occurrence Handle10.1017/S1464793102005936
P. J. Rudall R. Bateman (2003) ArticleTitleEvolutionary change in flowers and inflorescences: evidence from naturally occurring terata Trends Pl. Sci. 8 76–82 Occurrence Handle1:CAS:528:DC%2BD3sXht1Gitb4%3D Occurrence Handle10.1016/S1360-1385(02)00026-2
R. Rutishauser P. Moline (2005) ArticleTitleEvo-devo and the search for homology (“sameness”) in biological systems Theory Biosci. 124 213–241 Occurrence Handle10.1016/j.thbio.2005.09.005 Occurrence Handle17046357
R. Sattler (1988) ArticleTitleHomeosis in plants Amer. J. Bot. 75 1606–1617 Occurrence Handle10.2307/2444710
Schlechtendal, D. E. L. (1823) Flora Berolinensis. Berolini 1823.
K. K. Shimizu M. D. Purugganan (2005) ArticleTitleEvolutionary and ecological genomics of Arabidopsis Pl. Physiol. 138 578–584 Occurrence Handle1:CAS:528:DC%2BD2MXmtVaqurw%3D Occurrence Handle10.1104/pp.105.061655
K. Shimizu J. M. Cork A. L. Caicedo C. A. Mays R. C. Moore K. M. Olsen S. Ruzsa G. Coop C. D. Bustamante P. Awadalla M. D. Purugganan (2004) ArticleTitleDarwinian selection on a selfing locus Science 306 2081–2084 Occurrence Handle15604405 Occurrence Handle1:CAS:528:DC%2BD2cXhtVOjsLrM Occurrence Handle10.1126/science.1103776
G. H. Shull (1914) ArticleTitleDuplicate genes for capsule-form in Capsella bursa-pastoris Z. Abst. u. Vererbl. 12 97–149 Occurrence Handle10.1007/BF01837282
G. L. Stebbins (1950) Variation and evolution in plants Columbia University. Press New York
A. Steimer H. Schöb U. Grossniklaus (2004) ArticleTitleEpigenetic control of plant development: new layers of complexity Curr. Opin. Plant Biol. 7 11–19 Occurrence Handle14732436 Occurrence Handle1:CAS:528:DC%2BD2cXltFWqsg%3D%3D Occurrence Handle10.1016/j.pbi.2003.11.008
G. Theißen (2000) ArticleTitleEvolutionary developmental genetics of floral symmetry: the revealing power of Linnaeus' monstrous flower Bioessays 22 209–213 Occurrence Handle10684579 Occurrence Handle10.1002/(SICI)1521-1878(200003)22:3<209::AID-BIES1>3.0.CO;2-J
Theißen G. (2001a) Development of floral organ identity: stories from the MADS house. Curr. Opin. Pl. Biol. 4: 75–85.
Theißen G. (2001b) Flower development: genetics of identity. Nature 414: 491.
G. Theißen (2005) ArticleTitleBirth, life and death of developmental control genes: New challenges for the homology concept Theory Biosci. 124 199–212 Occurrence Handle17046356
G. Theißen (2006) ArticleTitleThe proper place of hopeful monsters in evolutionary biology Theory Biosci. 124 349–369 Occurrence Handle10.1016/j.thbio.2005.11.002 Occurrence Handle17046365
G. Theißen H. Saedler (2001) ArticleTitleFloral quartets Nature 409 469–471 Occurrence Handle11206529 Occurrence Handle10.1038/35054172
G. Theißen A. Becker Rosa A. Di A. Kanno J. T. Kim T. Münster K.-U. Winter H. Saedler (2000) ArticleTitleA short history of MADS-box genes in plants Pl. Molec. Biol. 42 115–149 Occurrence Handle10.1023/A:1006332105728
Trattinnick L. (1821) Botanische Bemerkungen. Flora 1821, p. 723.
F. Vergara-Silva (2003) ArticleTitlePlants and the conceptual articulation of evolutionary developmental biology Biol. Philos. 18 249–284 Occurrence Handle10.1023/A:1023936102602
G. P. Wagner (2000) ArticleTitleWhat is the promise of developmental evolution: Part I: Why lis developmental biology necessary to explain evolutionary innovations? J. Exp. Zool. (Mol. Dev. Evol.) 288 95–98 Occurrence Handle1:STN:280:DC%2BD3cvitFegtQ%3D%3D Occurrence Handle10.1002/1097-010X(20000815)288:2<95::AID-JEZ1>3.0.CO;2-5
G. P. Wagner M. D. Laubichler (2004) ArticleTitleRupert Riedl and the re-synthesis of evolutionary and developmental biology: body plan and evolvability J. Exp. Zool. (Mol. Dev. Evol.) 302B 92–102 Occurrence Handle10.1002/jez.b.20005
G. P. Wagner G. B. Müller (2002) ArticleTitleEvolutionary innovations overcome ancestral constraints: a re-examination of character evolution in male sepsid flies (Diptera: Sepsidae) Evol. Dev. 4 1–6 Occurrence Handle11868655 Occurrence Handle10.1046/j.1525-142x.2002.01059.x
P. Westrich (1990) Die Wildbienen Baden-Württembergs: Allgemeiner Teil: Lebensräume, Verhalten, Ökologie, Schutz Ulmer Stuttgart
Wiegmann, A. F. (1823) Correspondenz. Flora 1823.
S. Xing M. G. Rosso S. Zachgo (2005) ArticleTitle ROXY1, a member of the plant glutaredoxin family, is required for petal development in Arabidopsis thaliana Development 132 1555–1565 Occurrence Handle15728668 Occurrence Handle1:CAS:528:DC%2BD2MXjslGlsrc%3D Occurrence Handle10.1242/dev.01725
K. Zunk K. Mummenhoff H. Hurka (1999) ArticleTitlePhylogenetic relationship in tribe Lepidieae (Brassicaceae) based on chloroplast DNA restriction site variation Canad. J. Bot. 77 1504–1512 Occurrence Handle1:CAS:528:DC%2BD3cXht12jsb8%3D Occurrence Handle10.1139/cjb-77-10-1504
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Nutt, P., Ziermann, J., Hintz, M. et al. Capsella as a model system to study the evolutionary relevance of floral homeotic mutants. Plant Syst. Evol. 259, 217–235 (2006). https://doi.org/10.1007/s00606-006-0420-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00606-006-0420-2