Arabidopsis: Flower Development and Patterning

Beth A Krizek, University of South Carolina, Columbia, South Carolina, USA

Published online: September 2009

DOI: 10.1002/9780470015902.a0000734.pub2

The development of flowers and floral organs is directed by intricate genetic programmes, many aspects of which appear to be shared among all angiosperms. Early acting genes establish floral meristem identity in lateral organ primordia initiated at the periphery of the shoot apical meristem. Later, floral organ primordia arise at precise positions within these floral meristems and take on one of the four distinct identities (sepals, petals, stamens and carpels). A simple model (ABCE model), supported by both molecular and genetic experiments in Arabidopsis, explains how a small number of regulatory genes act in different combinations to specify these different organ types. These regulatory genes encode transcription factors that control the expression of many target genes responsible for organogenesis.

Key concepts

  • Lateral organs produced by the shoot apical meristem during reproductive development acquire their identity as flowers through the action of floral meristem identity genes such as LEAFY and APETALA1.
  • The identities of each of the four organ types of a flower (sepal, petal, stamen and carpel) is conferred by a unique combination of floral organ identity gene activities, referred to as class A, B, C and E in the ABCE model.
  • The activities of the class A, B, C and E genes are restricted to particular regions within a developing flower primarily, but not exclusively, through transcriptional regulation.
  • The proteins encoded by the class A, B, C and E genes encode transcription factors that form multimeric transcriptional regulatory complexes that control the expression of distinct sets of genes.
  • Many aspects of the genetic programmes conferring floral meristem identity and floral organ identity are conserved among all angiosperms.

Keywords: flower development; homeotic genes; floral meristem identity genes; Arabidopsis; ABCE model

Figure 1. Establishment of the floral meristem. (a) Wild-type inflorescence meristem (im) and young floral meristems (fm). Four sepal primordia (se) have arised in the older flowers and are indicated on one flower. (b) ap1 cal inflorescence apex. (c) ap1 lfy inflorescence apex.
Figure 2. Expression patterns of the floral meristem identity and floral organ identity genes. (a) LFY (purple) is expressed in floral meristem anlagen (1, 2), flower meristems (3–7) and young developing flowers (8–11). The number 8 marks a stage 3 flower in which the 4 sepal primordia are first visible. (b) The A class gene AP1 (red) is expressed in floral meristems, developing sepals and petals in whorls one and two of the flower, and the floral pedicel. (c) The B class genes AP3 and PI (yellow) are expressed in whorls two and three, which develop into petals and stamens. (d) The C class gene AG (blue) is expressed in whorls three and four, which develop into stamens and carpels and (e) Composite of B, C and D; in whorl one A class genes are expressed (red), in whorl two both A and B class genes are expressed (orange), in whorl three both B and C class genes are expressed (green) and in whorl four C class genes are expressed (blue).
Figure 3. Specification of floral organ identity. (a) Wild-type flower. (b) Floral diagram of the wild-type flower. (c) The ABCE model of the specification of floral organ identity showing how four classes of gene activities act in different combinations to specify four distinct floral organ identities. A section through a floral primordium is represented as a set of boxes, with the regions representing each floral whorl shown at the bottom. In the top set of boxes, the A (red), B (yellow), C (blue) and E (grey) fields are shown and the floral homeotic gene products present in each field listed. The identity of the organs present in each whorl is shown in the lower set of boxes: sepal (red), petal (orange), stamen (green) and carpel (blue). (d) ap1 flower (le, x, st, ca). (e) ap2 flower (ca, st, st, ca). (f) pi flower (se, se, ca, ca). (g) ag flower ((se, pe, pe)n). (h) pi ag flower ((se, se, se)n). (i) ap2 pi flower (ca, ca, ca, ca). (j) ap2 ag flower ((le-ca, pe-st, pe-st)n). (k) ap2 pi ag flower ((le-ca, le-ca, le-ca)n). (l) sep1 sep2 sep3 ((se, se, se)n). (m) sep1 sep2 sep3 sep4 ((le, le, le)n). (n) Flower from a transgenic plant in which the B class genes are constitutively expressed (pe, pe, st, st). (o) ap2 flower in which the B class genes are constitutively expressed (st, st, st, st). se, sepal; pe, petal; st, stamen; ca, carpel; le, leaf-like; le-ca, leaf-like carpel; pe-st, petaloid stamen and x, organs absent.
Figure 4. Quartet model for the specification of floral organ identity. A unique tetrameric MADS domain protein regulatory complex is proposed to form in cells of each floral whorl. In first whorl cells, a tetrameric complex composed of two AP1-SEP heterodimers is proposed to regulate the expression of genes involved in sepal (red) development. In second whorl cells, a tetrameric complex composed of one AP1-SEP heterodimer and one AP3-PI heterodimer regulates genes required to make a petal (orange). In third whorl cells, a tetrameric complex composed of one AP3-PI heterodimer and one AG-SEP heterodimer regulates genes needed for stamen (green) development. In fourth whorl cells, a tetrameric complex composed of two AG-SEP heterodimers regulates genes required for carpel (blue) development.
Figure 5. Transcriptional network showing regulatory interactions involving AG during different stages of flower development. LFY (purple) acts with WUS (pink) in stage 1 and 2 flowers to activate expression of AG (blue) in the two inner whorls of a stage 3 flower. AG later acts to repress WUS expression in the centre of developing flowers. LFY activates AP1 (red) expression throughout a young floral meristem but AP1 expression becomes restricted to the outer two floral whorls in a stage 3 flower due to repression of AP1 expression by AG. AG binds directly to its own promoter and that of AP3 (yellow) and SEP3 (grey) to maintain their expression in developing flowers. AG promotes stamen and carpel identity through early and late activation of target genes. An early target of AG regulation in stamen primordia is SPL (light green). A later target of AG regulation in developing stamens is DAD1 (dark green). Solid arrows indicate direct regulation. Bars shown in dashes indicate interactions that have not yet been shown to be direct. se, sepal; pe, petal; st, stamen and ca, carpel.
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 Further Reading
    Coen ES and Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353: 31–37.
    Jack T (2004) Molecular and genetic mechanisms of floral control. Plant Cell 16: S1–S17.
    Krizek BA and Fletcher JC (2005) Molecular mechanisms of flower development: an armchair guide. Nature Review. Genetics 6: 688–698.
    Litt A (2007) An evaluation of A-function: evidence from the APETALA1 and APETALA2 gene lineages. International Journal of Plant Science 168: 73–91.
    Lohman JU and Weigel D (2002) Building beauty: the genetic control of floral patterning. Developmental Cell 2: 135–142.
    Meyerowitz EM, Smyth DR and Bowman JL (1989) Abnormal flowers and pattern formation in floral development. Development 106: 209–217.
    Robles P and Pelaz S (2005) Flower and fruit development in Arabidopsis thaliana. International Journal of Developmental Biology 49: 633–643.
    Schwarz-Sommer Z, Huijser P, Nacken W, Saedler H and Sommer H (1990) Genetic control of flower development: homeotic genes of Antirrhinum majus. Science 250: 931–936.
    Soltis DE, Ma H, Frohlich MW et al. (2007) The floral genome: an evolutionary history of gene duplication and shifting patterns of gene expression. Trends in Plant Science 12: 358–367.
    Theissen G (2001) Development of floral organ identity: stories from the MADS house. Current Opinion in Plant Biology 4: 75–85.

Related Sub-Topics:

Genes, Molecules and Cellular Processes | Organogenesis | Flowers | Plant Development
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Article Title: Arabidopsis: Flower Development and Patterning
 
How to Cite close
Krizek, Beth A(Sep 2009) Arabidopsis: Flower Development and Patterning. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0000734.pub2]