Skip to main content
SpringerLink
Log in

Evolutionary conservation of angiosperm flower development at the molecular and genetic levels

  • Published:
Journal of Biosciences Aims and scope Submit manuscript

Abstract

Flowers consist primarily of four basic organ types whose relative positions are universally conserved within the angiosperms. A model has been proposed to explain how a small number of regulatory genes, acting alone and in combination, specify floral organ identity. This model, known widely as the ABC model of flower development, is based on molecular generic experiments in two model organisms,Arabidopsis thaliana and Antirrhinum majus.Both of these species are considered to be eudicots, a clade within the angiosperms with a relatively conserved floral architecture. In this review, the application of the ABC model derived from studies of these typical eudicot species is considered with respect to angiosperms whose floral structure deviates from that of the eudicots. It is concluded that the model is universally applicable to the angiosperms as a whole, and the enormous diversity seen among angiosperms flowers is due to genetic pathways that are downstream, or independent, of the genetic programme that specifies floral organ identity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Ainsworth C, Crossley S, Buchanan-Wollaston V, Thangavelu M and Parker J 1995 Male and female flowers of the dioecious plant sorrel show different patterns of MADS box gene expression;Plant Cell 7 1583–1598

    Article  CAS  Google Scholar 

  • Angenent G C, Franken J, Busscher M, Colombo L and van Tunen A J 1993 Petal and stamen formation in petunia is regulated by the homeotic gene fbp 1;Plant J. 4 101–112

    Article  CAS  Google Scholar 

  • Bowman J L, Alvarez J, Weigel D, Meyerowitz E M and Smyth D R 1993 Control of flower development inArabidopsis thaliana byAPETALA1 and interacting genes;Development 119 721–743

    CAS  Google Scholar 

  • Bowman J L, Smyth D K and Meyerowitz E M 1989 Genes directing flower development inArabidopsis;Plant Cell 1 37–52

    Article  CAS  Google Scholar 

  • Bowman J L, Smyth D R and Meyerowitz E M 1991 Genetic interactions among floral homeotic genes ofArabidopsis;Development 112 1–20

    CAS  PubMed  Google Scholar 

  • Brunner A, Rottmann W, Sheppard L, Ktutovskii K and Strauss S 1997 Characterization ofPTAG1 andPTAG2, two genes fromPopulus trichocarpa homologous to theArabidopsis floral homeotic geneAGAMOUS;Keystone Symposium: Evolution of Plant Development, Taos, NM, p 22

  • Carpenter R and Coen E S 1990 Floral homeotic mutations produced by transposon-mutagenesis inAntirrhinum majus;Genes Dev,4 1483–1493

    Article  CAS  Google Scholar 

  • Chase M W, Soltis D E, Olmstead R G, Morgan D, Les D H, Mishler B D, Duvall M R, Price R A, Hills H G, Qiu Y-L, Kron K A, Rettig J H, Conti E, Palmer J D, Manhart J R, Sytsma K J, Michaels H J, Kress W J, Karol K G, Clark W D, Hedrén M, Gaut B S, Jansen R K, Kim K-J, Wimpee A. F, Smith J F, Furnier G R, Strauss S H, Xiang Q Y, Plunkett G M, Soltis P S, Swensen S M.Williams S E, Gadek P A, Quinn A. J, Eguiarte L E, Golenberg E, Learn Jr G H, Graham S W, Barrett S C H, Dayanandan S and Albert V 1993 Phylogenetics of seed plants: an analysis of nucleotide sequences from the plastid generbcL;Ann. Mo. Bot. Gard. 80 528–580

    Article  Google Scholar 

  • Coen E S and Meyerowitz E M 1991 The war of the whorls: genetic interactions controlling flower development;Nature (London) 353 31–37

    Article  CAS  Google Scholar 

  • Crane P R, Friis E M and Pedersen K R 1995 The origin and early diversification of angiosperms;Nature (London) 374 27–33

    Article  CAS  Google Scholar 

  • Cronquist A 1988The Evolution and Classification of Flowering Plants (New York: New York Bot. Garden)

    Google Scholar 

  • Dellaporta S L and Calderon-Urrea A 1993 Sex determination in flowering plants;Plant Cell 5 1241–1251

    Article  CAS  Google Scholar 

  • Di Laurenzio L, Struwe L, Pepper A, Kizirian D and Albert V 1997 Gene expression analysis of sepal identity in Clermontia (Lobelioideae: Campanulaceae): homeosis and floral diversification in the Hawaiin archipelago;Keystone Symposium: Evolution of Plant Development, Taos, NM, p 24

  • Drews G N, Bowman J L and Meyerowitz EM 1991 Negative Regulation of theArabidopsis Homeotic GeneAGAMOUS by theAPETALA2 Product;Cell 65 991–1002

    Article  CAS  Google Scholar 

  • Endress P K 1994Diversity and Evolutionary biology of Tropical Flowers (Cambridge: Cambridge University Press)

    Google Scholar 

  • Ford V S and Gottlieb L D 1992Bicalyx is a natural homeotic floral varient;Nature (London) 358 671–673

    Article  Google Scholar 

  • Goto K and Meyerowitz E M 1994 Function and regulation of theArabidopsis floral homeotic genePISTILLATA;Genes Dev.8 1548–1560

    Article  CAS  Google Scholar 

  • Grant S, Houben A, Vyskot B, Siroky J, Pan W-H, Macas J and Saedler H 1994 Genetics of sex determination in flowering plants; Dev.Genet. 15 214–230

    Article  Google Scholar 

  • Gustafson-Brown C, Savidge B and Yanofsky M F 1994 Regulation of the Arabidopsis floral homeotic geneAPETAIA1;Cell 76 131–143

    Article  CAS  Google Scholar 

  • Halfter U, Ali N, Stockhaus J, Ren L and Chua N H 1994 Ectopic expression of a single homeotic gene, the Petunia gene green petal, is sufficient to convert sepals to petaloid organs;EMBO J. 13 1443–1449

    Article  CAS  Google Scholar 

  • Hansen G, Estruch J J, Sommer H and Spena A 1993 NTGLO: a tobacco homologue of the GLOBOSA floral homeotic gene of Antirrhinum majus: cDNA sequence and expression pattern;Mol. Gen. Genet. 239 310–312

    CAS  PubMed  Google Scholar 

  • Hardenack S, Ye D, Saedler H and Grant S 1994 Comparison of MADS box gene expression in developing male and female flowers of the dioecious plant white campion;Plant. Cell 6 1775–1787

    Article  CAS  Google Scholar 

  • Heywood V H 1993Flowering Plants of the World (New York: Oxford University Press)

    Google Scholar 

  • Hill J P and Lord E M 1989 Floral development inArabidosis thaliana: a comparison of the wild type and the homeoticpistillata mutant;Can. J. Bot. 67 2922–2936

    Article  Google Scholar 

  • Innes R L, Remphrey W R and Lenz L M 1989 An analysis of the development of single and double flowers inPotentillafrutocosa;Can. J. Bot. 67 1071–1079

    Article  Google Scholar 

  • Irish E E and Nelson T 1989 Sex determination in monoecious and dioecious plants;Plant Cell 1 737–744

    Article  Google Scholar 

  • Irish V F and Sussex I M 1990 Function of theapetala1-1 gene during Arabidopsis floral development;Plant Cell 2 741–751

    Article  CAS  Google Scholar 

  • Jack T, Brockman L L and Meyerowitz E M 1992 The homeotic geneAPETALA3 of Arabidopsis thaliana encodes a MADS-box and is expressed in petals and stamens;Cell 68 683–697

    Article  CAS  Google Scholar 

  • Jack T, Fox G L, and Meyerowitz E M 1994 Arabidopsis homeotic geneAPETALA3 ectopic expression: transcriptional and post-transcriptional regulation determine floral organ identity;Cell. 76 703–716

    Article  CAS  Google Scholar 

  • Jofuku K D, den Boer B G W, Van Montagu M and Okamuro J K 1994 Control of Arabidoppsis flower and seed development by the homeotic geneAPETALA2;Plant Cell 6 1211–1225

    Article  CAS  Google Scholar 

  • Kempin S A Mandel M A and Yanofsky M F 1993 Conversion of perianth into reproductive organs by ectopic expression of the tobacco floral homeotic gene NAG 1;Plant Physiol. 103 10041–1046

    Article  Google Scholar 

  • Kirchoff B K 1991 Homeosis in the flowers of the Zingiberales;Am. J. Bot. 78 833–837

    Article  Google Scholar 

  • Komaki M K, Okada K, Nishino E and Shimura Y 1988 Isolation and characterization of novel mutants ofArabidopsis thaliana defective in flower development;Development 104 195–203

    Google Scholar 

  • Krizek B A and Meyerowitz E M 1996 TheArabidopsis homeotic genesAPETALA3 andPISTIILATA are sufficient to provide the B class organ identity function;Development 122 11–22

    CAS  PubMed  Google Scholar 

  • Kunst L, Klenz J E, Martinez-Zapater J and Haughn G W 1989AP2 gene determines the identity of perianth organs in flowers ofArabidopsis thaliana;Plant Cell 1 1195–1208

    Article  Google Scholar 

  • Kyozuka J, Southerton S and Dennis E S 1997aEucalyptus has functional equivalents of theArabidopsis AP1 gene;Plant. Mol. Biol (in press)

  • Kyozuka J, Konishi S, Morita M, Izawa T, Kobayashi T, Nakagawa M, Amano E and Shimamoto K 1997b Molecular mechanisms determining rice panicle and spiklet formation;Keystone Symposium: Evolution of Plant Development, Taos, NM, p 26

  • Lehmann N L and Sattler R 1993 Homeosis in floral development ofSanguinaria canadensis andS canadensis ‘Multiplex’ (Papaveraceae);Am. J. Bot 80 1323–1335

    Article  Google Scholar 

  • Lehmann N L and Sattler R 1994 Floral development and homeosis inActaea rubra (Ranunculaceae);Int. J. Plant Sci. 155 658–671

    Article  Google Scholar 

  • Liu Z and Meyerowitz E M 1995LEUNIG regulatesAGAMOUS expression inArabidopsis flowers;Development 121 975–991

    CAS  PubMed  Google Scholar 

  • Luo D, Carpenter R, Vincent C, Copsey L and Coen E 1996 Origin of floral asymmetry inAntirrhinum;Nature (London) 383 794–799

    Article  CAS  Google Scholar 

  • MacIntyre J P and Lacroix A. R 1996 Comparative development of perianth and androecial primordia of the single flower and the homeotic double-flowered mutant inHibiscus rosa-sinensis (Malvaceae);Can. J. Bot. 74 1871–1882

    Article  Google Scholar 

  • Mandel M A, Bowman J L, Kempin S A, Ma H, Meyerowitz E M and Yanofsky M F 1992 Manipulation of Flower Structure in Transgenic Tobacco;Cell 71 133–143

    Article  CAS  Google Scholar 

  • Martinez E and Ramos A. H 1989 Lacandoniaceae (Triuridales): Una nueva familia de Mexico;Ann. M. Bot. Gard. 76 128–135

    Article  Google Scholar 

  • Mena M, Ambrose B A, Meeley R B, Briggs S P, Yanofsky M F and Schmidt R J 1996 Diversification of C-function activity in maize flower development;Science 274 1537–1540

    Article  CAS  Google Scholar 

  • Meyerowitz E M, Smyth D R and Bowman J L 1989 Abnormal flowers and pattern formation in floral development;Development 106 209–217

    Google Scholar 

  • Mizukami Y and Ma H 1992 Ectopic expression of the floral homeotic geneAGAMOUS in transgenic Arabidopsis plants alters floral organ identity;Cell 71 119–131

    Article  CAS  Google Scholar 

  • Nagato Y 1994 Embryo and flower development in rice and apomixis in Chinese chive(Allium tuberosum); inApomixis: exploiting hybris vigor in rice (ed.) G S Khush (Los Banos, Phillipines: IRRI)

    Google Scholar 

  • Pnueli L, Abu-Abeid M, Zamir D, Nacken W, Schwarz-Sommer Zand Lifschitz E 1991 The MADS box gene family in tomato: temporal expression during floral development, conserved secondary structures and homology with homeotic genes fromAntirrhinum andArabidopsis;Plant J. 1 255–266

    Article  CAS  Google Scholar 

  • Purugganan M.D, Rounsley S D, Schmidt R J and Yanofsky M F 1995 Molecular evolution of flower development: diversification of the plant MADS-box regulatory gene family;Genetics 140 345–356

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sakai H, Medrano L J and Meyerowitz E M 1995 Arabidopsis floral boundary maintenance bySUPER-MAN;Nature (London) 378 199–203

    Article  CAS  Google Scholar 

  • Schwarz-Sommer Z, Huijser P, Nacken W, Saedler H and Sommer H 1990 Genetic control of flower development: homeotic genesof Antirrhinum majus;Science 250 931–936

    Article  CAS  Google Scholar 

  • Soltis D E, Soltis P S, Nickrent D L, Johnson L A, Hahn W J, Hoot S B, Sweere J A, Kuzoff R K, Kron K A, Chase M W, Swensen S M, Zimmer E A, Chaw. S-M, Gillespie L J, Kress W J and Sytsma K J 1977 Angiosperm phylogeny inferred from 18S ribosomal DNA sequences;Ann. Mo. Bot. Gard. 84 1–49

    Article  Google Scholar 

  • Tandre K, Albert V A, Sundas A and Engstrom P 1995 Conifer homologues to genes that control floral development in angiosperms;Plant Mol. Biol. 27 69–78

    Article  CAS  Google Scholar 

  • Theissen G, Kim J T and Saedler H 1996 Classification and phylogeny of the MADS-box multigene family suggest defined roles of MADS-box gene subfamilies in the morphological evolution of eukaryotes;J. Mol. Evol. 43 484–516

    Article  CAS  Google Scholar 

  • van der Krol A R and Chua N -H 1993 Flower development in petunia;Plant Cell 5 1195–1203

    Article  Google Scholar 

  • van Tunen A J, Eikelboom W and Angenent G C 1993 Floral organogenesis inTulipa;Flowering Newsl. 16 33–37

    Google Scholar 

  • Veit B, Schmidt R J, Hake S and Yanofsky M F 1993 Maize floral development: new genes and old mutants;Plant Cell 5 1205–1215.

    Article  Google Scholar 

  • Vergara F S and Alvarez-Buyela E 1977 Developmental genetic basis of the origin and evolution of the homeotic phenotype ofLacandonia schismatica: an endemic angiosperm from Chiapas (Mexico) with inverted reproductive whorls;Keystone Symposium: Evolution of Plant Development, Taos, NM, p 28

  • Weigel D and Meyerowitz E M 1994 The ABCs of floral homeotic genes;Cell 78 203–209

    Article  CAS  Google Scholar 

  • Yanofsky M F, Ma H, Bowman J L, Drews G N, Feldmann K A and Meyerowitz E M 1990 The protein encoded by theArabidopsis homeotic geneagamous resembles transcription factors;Nature (London) 346 35–40

    Article  CAS  Google Scholar 

  • Yu D, Kotilained P, Elomaa P, Mehto M, Helariutta Albert V and Teeri T H 1977 Inflorescence development in Asteraceae: B-function MADS-box genes are required for congenital fusion in corolla and stamen and the DEFICIENS ortholog has differential radial effects within capitulum;Keystone Symposium: Evol-ution of Plant Development, Taos, NM p 28.

Download references

Author information

Authors and Affiliations

  1. Section of Plant Biology, University of California, 95616, Davis, Davis California, USA

    John L. Bowman

Authors
  1. John L. Bowman
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bowman, J.L. Evolutionary conservation of angiosperm flower development at the molecular and genetic levels. J. Biosci. 22, 515–527 (1997). https://doi.org/10.1007/BF02703197

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02703197

Keywords

Search

Navigation