Arabidopsis: Flower Development and Patterning

Abstract

The development of flowers and floral organs is directed by intricate genetic programmes, many aspects of which appear to be shared among angiosperms. Early acting genes establish floral meristem identity in flower primordia initiated at the periphery of the inflorescence 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). The ABCE model, supported by both molecular and genetic experiments in Arabidopsis, explains how a small number of regulatory genes (called floral homeotic genes or floral organ identity genes) act in different combinations to specify these different organ types. The floral organ identity genes encode transcription factors that form distinct higher order protein complexes in different regions of a flower primordium to control the expression of 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 and C genes are restricted to particular regions within a developing flower primarily, but not exclusively, through transcriptional regulation.
  • The MADS domain transcription factors encoded by the class A, B, C and E genes form unique tetrameric transcriptional regulatory complexes in cells of each floral whorl.
  • The transcriptional regulatory complexes formed by the A, B, C and E proteins regulate distinct sets of genes at different stages of flower development.
  • 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; floral organ identity genes; Arabidopsis; ABCE model; quartet 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 four 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 Arabidopsis flower. (b) Floral diagram of a wild‐type flower with sepals (se), petals (pe), stamens (st) and carpels (ca) indicated. (c) The ABCE model for the specification of floral organ identity showing how four classes of gene activities act in different combinations to specify four distinct floral organ identities. The boxes represent where the class A (red), B (yellow), C (blue) and E (grey) genes have activity. The floral homeotic genes associated with each class are indicated in the appropriate box and the identity of the organs present in each whorl (indicated by the numbers) is shown below the boxes. (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) sep1 sep2 sep3 ((se, se, se)n). (i) sep1 sep2 sep3 sep4 flower ((le, le, le)n). (j) Flower from a transgenic plant in which the B class genes are constitutively expressed (pe, pe, st, st). (k) 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 and x, organs absent.
Figure 4. Quartet model for the specification of floral organ identity. A unique tetrameric MADS domain protein regulatory complex forms in cells of each floral whorl. In first whorl cells, a tetrameric complex composed of two AP1‐SEP heterodimers regulates the expression of genes involved in sepal 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. In third whorl cells, a tetrameric complex composed of one AP3‐PI heterodimer and one AG‐SEP heterodimer regulates genes needed for stamen development. In fourth whorl cells, a tetrameric complex composed of two AG‐SEP heterodimers regulates genes required for carpel development. se, sepal; pe, petal; st, stamen and ca, carpel.
Figure 5. Gene regulatory interactions that control expression of the floral organ identity genes. Arrows indicate gene activation and bars indicate repression. The diagram was generated with BioTapestry (Longabaugh et al., ).
Figure 6. Schematic showing a few targets of AG regulation at different stages of flower development. AG promotes floral determinacy by activating expression of KNU (light blue) within fourth whorl cells. 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. se, sepal; pe, petal; st, stamen and ca, carpel.
close

References

Bowman JL, Smyth DR and Meyerowitz EM (1989) Genes directing flower development in Arabidopsis. Plant Cell 1: 37–52.

Chae E, Tan QK‐G, Hill TA and Irish VF (2008) An Arabidopsis F‐box protein acts as a transcriptional co‐factor to regulate floral development. Development 135: 1235–1245.

Chen X (2004) A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303: 2022–2025.

Conner J and Liu Z (2000) LEUNIG, a putative transcriptional corepressor that regulates AGAMOUS expression during flower development. Proceedings of the National Academy of Sciences of the United States of America 97: 12902–12907.

Daum G, Medzihradszky A, Suzaki T and Lohmann JU (2014) A mechanistic framework for noncell autonomous stem cell induction in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 111: 14619–14624.

Ditta G, Pinyopich A, Robles P, Pelaz S and Yanofsky MF (2004) The SEP4 gene of Arabidopsis thaliana functions in floral organ and meristem identity. Current Biology 14: 1935–1940.

Egea‐Cortines M, Saedler H and Sommer H (1999) Ternary complex formation between the MADS‐box proteins SQUAMOSA, DEFICIENS and GLOBOSA is involved in the control of floral architecture in Antirrhinum majus. EMBO Journal 18: 5370–5379.

Franks RG, Wang C, Levin JZ and Liu Z (2002) SEUSS, a member of a novel family of plant regulatory proteins, represses floral homeotic gene expression with LEUNIG. Development 129: 253–263.

Gomez‐Mena C, de Folter S, Costa MMR, Angenent GC and Sablowski R (2005) Transcriptional program controlled by the floral homeotic gene AGAMOUS during early organogenesis. Development 132: 429–438.

Goto K and Meyerowitz EM (1994) Function and regulation of the Arabidopsis floral homeotic gene PISTILLATA. Genes and Development 8: 1548–1560.

Honma T and Goto K (2001) Complexes of MADS‐box proteins are sufficient to convert leaves into floral organs. Nature 409: 525–529.

Ito T, Wellmer F, Yu H, et al. (2004) The homeotic protein AGAMOUS controls microsporogenesis by regulation of SPOROCYTELESS. Nature 430: 356–360.

Ito T, Ng K‐H, Lim T‐S, Yu H and Meyerowitz EM (2007) The homeotic protein AGAMOUS controls late stamen development by regulating a jasmonate biosynthetic gene in Arabidopsis. The Plant Cell 19: 3516–3529.

Jack T, Brockman LL and Meyerowitz EM (1992) The homeotic gene APETALA3 of Arabidopsis thaliana encodes a MADS box and is expressed in petals and stamens. Cell 68: 683–687.

Jofuku KD, den Boer BGW, Van Montagu M and Okamuro JK (1994) Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. The Plant Cell 6: 1211–1225.

Kanno A, Saeki H, Kameya T, Saedler H and Theissen G (2003) Heterotopic expression of class B floral homeotic genes supports a modified ABC model for tulip (Tulipa gesneriana). Plant Molecular Biology 52: 831–841.

Kaufmann K, Muino JM, Jauregui R, et al. (2009) Target genes of the MADS transcription factor SEPALLATA3: Integration of developmental and hormonal pathways in the Arabidopsis flower. PLoS Biology 2009: e1000090.

Kaufmann K, Wellmer F, Muino JM, et al. (2010) Orchestration of floral initiation by APETALA1. Science 328: 85–89.

Krizek BA and Meyerowitz EM (1996) The Arabidopsis genes APETALA3 and PISTILLATA are sufficient to specify the B class organ identity function. Development 122: 11–22.

Krogan NT, Hogan K and Long JA (2012) APETALA2 negatively regulates multiple floral organ identity genes in Arabidopsis by recruiting the co‐repressor TOPLESS and the histone deacetylase HDA19. Development 129: 4180–4190.

Lenhard M, Bohnert A, Jurgens G and Laux T (2001) Termination of stem cell maintenance in Arabidopsis floral meristems by interactions between WUSCHEL and AGAMOUS. Cell 105: 805–814.

Litt A (2007) An evaluation of A‐function: evidence from the APETALA1 and APETALA2 gene lineages. International Journal of Plant Science 168: 73–91.

Liu X, Kim YJ, Muller R, et al. (2011) AGAMOUS terminates floral stem cell maintenance in Arabidopsis by directly repressing WUSCHEL through recruitment of Polycomb Group proteins. The Plant Cell 23: 3654–3670.

Lohmann JU, Hong RL, Hobe M, et al. (2001) A molecular link between stem cell regulation and floral patterning in Arabidopsis. Cell 105: 793–803.

Longabaugh WJ, Davidson EH and Bolouri H (2005) Computational repression of developmental genetic regulatory networks. Developmental Biology 283: 1–16.

Ma H, Yanofsky MF and Meyerowitz EM (1991) AGL1‐AGL6, an Arabidopsis gene family with similarity to floral homeotic and transcription factor genes. Genes and Development 5: 484–495.

Mandel MA, Gustafson‐Brown C, Savidge B and Yanofsky MF (1992) Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature 360: 273–277.

Mandel MA and Yanofsky MY (1995) A gene triggering flower formation in Arabidopsis. Nature 377: 522–524.

Melzer R and Theissen G (2009) Reconstitution of 'floral quartets' in vitro involving class B and class E floral homeotic proteins. Nucleic Acids Research 37: 2723–2736.

Meyerowitz EM, Bowman JL, Brockman LL, et al. (1991) A genetic and molecular model for flower development in Arabidopsis thaliana. Development Supplement 1: 157–167.

Mizukami Y and Ma H (1992) Ectopic expression of the floral homeotic gene AGAMOUS in transgenic Arabidopsis plants alters floral organ identity. Cell 71: 119–131.

O'Maoleidigh DS, Wuest SE, Rae L, et al. (2013) Control of reproductive floral organ identity specification in Arabidopsis by the C function regulator AGAMOUS. The Plant Cell 25: 2482–2503.

Okamuro JK, Caster B, Villarroel R, Montagu MV and Jofuku KD (1997) The AP2 domain of APETALA2 defines a large new family of DNA binding proteins in Arabidopsis. Proceedings of the National Academy of Sciences 94: 7076–7081.

Pelaz S, Ditta GS, Baumann E, Wisman E and Yanofsky MF (2000) B and C floral organ identity functions require SEPALLATA MADS‐box genes. Nature 405: 200–203.

Pelaz S, Tapia‐Lopez R, Alvarez‐Buylla ER and Yanofsky MF (2001) Conversion of leaves into petals in Arabidopsis. Current Biology 11: 182–184.

Riechmann JL, Wang M and Meyerowitz EM (1996a) DNA‐binding properties of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA, and AGAMOUS. Nucleic Acids Research 24: 3134–3141.

Riechmann JL, Krizek BA and Meyerowitz EM (1996b) Dimerization specificity of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA, and AGAMOUS. Proceedings of the National Academy of Sciences of the United States of America 93: 4793–4798.

Smaczniak C, Immink RGH, Muino JM, et al. (2012) Characterization of MADS‐domain transcription factor complexes in Arabidopsis flower development. Proceedings of the National Academy of Sciences of the United States of America 109: 1560–1565.

Smyth DR, Bowman JL and Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2: 755–767.

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 Sciences 12: 358–367.

Sridhar VV, Surendrarao A and Liu Z (2006) APETALA1 and SEPALLATA3 interact with SEUSS to mediate transcription repression during flower development. Development 133: 3159–3166.

Sun B, Xu Y, Ng K‐H and Ito T (2009) A timing mechanism for stem cell maintenance and differentiation in the Arabidopsis floral meristem. Genes and Development 23: 1791–1804.

Theissen G (2001) Development of floral organ identity: stories from the MADS house. Current Opinion in Plant Biology 4: 75–85.

Wagner D, Sablowski RWM and Meyerowitz EM (1999) Transcriptional Activation of APETALA1 by LEAFY. Science 285: 582–584.

Weigel D and Nilsson O (1995) A developmental switch sufficient for flower initiation in diverse plants. Nature 377: 495–500.

William DA, Su Y, Smith MR, et al. (2004) Genomic identification of direct target genes of LEAFY. Proceedings of the National Academy of Sciences of the United States of America 101: 1775–1780.

Wollmann H, Mica E, Todesco M, Long JA and Weigel D (2010) On reconciling the interactions between APETALA2, miR172 and AGAMOUS with the ABC model of flower development. Development 137: 3633–3642.

Wuest SE, O'Maoleidigh DS, Rae L, et al. (2012) Molecular basis for the specification of floral organs by APETALA3 and PISTILLATA. Proceedings of the National Academy of Sciences of the United States of America 109: 13452–13457.

Yadav RK, Perales M, Gruel J, et al. (2011) WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex. Genes and Development 19: 2025–2030.

Yanofsky MF, Ma H, Bowman JL, et al. (1990) The protein encoded by the Arabidopsis homeotic gene AGAMOUS resembles transcription factors. Nature 346: 35–39.

Yant L, Mathieu J, Dinh TT, et al. (2010) Orchestration of the floral transition and floral development in Arabidopsis by the bifunctional transcription factor APETALA2. The Plant Cell 22: 2156–2170.

Further Reading

Causier B, Schwarz‐Sommer Z and Davies B (2010) Floral organ identity: 20 years of ABCs. Seminars in Cell & Developmental Biology 21: 73–79.

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.

Pajoro A, Biewers S, Dougali E, et al. (2014) The (r)evolution of gene regulatory networks controlling Arabidopsis plant reproduction: a two‐decade history. Journal of Experimental Botany 65: 4731–4745.

Prunet N and Jack TP (2014) Flower development in Arabidopsis: There is more to it than learning your ABCs. In: Methods in Molecular Biology: Flower Development, pp. 3–33. New York: Springer.

O'Maoileidigh DS, Graciet E and Wellmer F (2014) Gene Networks controlling Arabidopsis thaliana flower development. New Phytologist 201: 16–30.

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.

Wellmer F, Graciet E and Riechmann JL (2014) Specification of floral organs in Arabidopsis. Journal of Experimental Botany 65: 1–9.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Krizek, Beth A(May 2015) Arabidopsis: Flower Development and Patterning. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0000734.pub3]