Skip to main content
SpringerLink
Log in

Inflorescence architecture: A developmental genetics approach

  • Interpreting Botanical Progress
  • Published:
The Botanical Review Aims and scope Submit manuscript

Abstract

We are characterizing a suiteof Pisum sativum mutants that alter inflorescence architecture to construct a model for the genetic regulation of inflorescence development in a plant with a compound raceme. Such a model, when compared with those created forAntirrhinum majus andArabidopsis thaliana, both of which have simple racemes, should provide insight into the evolution of the development of inflorescence architecture. The highly conserved nature of cloned genes that regulate reproductive development in plants and the morphological similarities among our mutants and those identified inA. majus andA. thaliana enhance the probability that a developmental genetics approach will be fruitful. Here we describe sixP. sativum mutants that affect morphologically and architecturally distinct aspects of the inflorescence, and we analyze interactions among these genes. Both vegetative and inflorescence growth of the primary axis is affected byUNIFOLIA TA, which is necessary for the function ofDETERMINATE (DET).DET maintains indeterminacy in the first-order axis. In its absence, the meristem differentiates as a stub covered with epidermal hairs.DET interacts withVEGETATIVE1 (VEG1).VEG1 appears essential for second-order inflorescence (I2) development.veg1 mutants fail to flower or differentiate the I2 meristem into a rudimentary stub,det veg1 double mutants produce true terminal flowers with no stubs, indicating that two genes must be eliminated for terminal flower formation inP. sativum, whereas elimination of a single gene accomplishes this inA. thaliana andA. majus. NEPTUNE also affects I2 development by limiting to two the number of flowers produced prior to stub formation. Its role is independent ofDET, as indicated by the additive nature of the double mutantdet nep. UNI, BROC, and PIM all play roles in assigning floral meristem identity to the third-order branch.pim mutants continue to produce inflorescence branches, resulting in a highly complex architecture and aberrant flowers.uni mutants initiate a whorl of sepals, but floral organogenesis is aberrant beyond that developmental point, and the double mutantuni pim lacks identifiable floral organs. A wild-type phenotype is observed inbroc plants, butbroc enhancesthe pim phenotype in the double mutant, producing inflorescences that resemble broccoli. Collectively these genes ensure that only the third-order meristem, not higher- or lower-order meristems, generates floral organs, thus precisely regulating the overall architecture of the plant.

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

Literature Cited

  • Alvarez, J., C. L. Guli, X-H. Yu &D. R. Smyth. 1992.TERMINAL FLOWER: A gene affecting inflorescence development inArabidopsis thaliana. Pl. J. 2: 103–116.

    Article  Google Scholar 

  • Amasino, R. 1996. Control of flowering time in plants. Curr. Opinion in Genet. & Developm. 6: 480–187.

    Article  CAS  Google Scholar 

  • Bassiri, A., E. E. Irish &R. S. Poethig. 1992. Heterochronic effects ofTeopod2 on the growth and photosensitivity of the maize shoot. Pl. Cell 4: 497–504.

    Google Scholar 

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

    CAS  Google Scholar 

  • Bradley, D., R. Carpenter, L. Copsey, C. Vincent, S. Rothstein &E. Coen. 1996. Control of inflorescence architecture in Antirrhinum. Nature 379: 791–797.

    Article  PubMed  CAS  Google Scholar 

  • —,O. Ratcliffe, C. Vincent, R. Carpenter &E. Coen. 1997. Inflorescence commitment and architecture inArabidopsis. Science 275: 80–83.

    Article  PubMed  CAS  Google Scholar 

  • Chappill, J. A. 1995. Cladistic analysis of the Fabaceae: The development of an explicit phylogenetic hypothesis. Pp. 1–9in M. D. Crisp & J. J. Doyle (eds.), Advances in legume systematics. Pt. 7. Phylogeny. Royal Botanic Gardens, Kew.

    Google Scholar 

  • Coen, E. S. & J. M. Nugent. 1994. Evolution of flowers and inflorescences. Development (suppl.): 107–116.

  • Diggle, P. K. 1992. Development and the evolution of plant reproductive characters. Pp. 326–355in R. Wyatt (ed.), Ecology and evolution of plant reproduction: New approaches. Chapman and Hall, New York.

    Google Scholar 

  • Doebley, J. &L. Lukens. 1998. Transcriptional regulators and the evolution of plant form. Pl. Cell 10: 1075–1082.

    CAS  Google Scholar 

  • Donoghue, M. J., R. H. Ree &D. A. Baum. 1998. Phylogeny and the evolution of flower symmetry in the Asteridae. Trends Pl. Sci. 3: 311–317.

    Article  Google Scholar 

  • Doyle, J. J. 1997. A phylogeny of the chloroplast gene rbcL in the Fabaceae: Taxonomic correlations and insights into the evolution of nodulation. Amer. J. Bot. 84: 541–554.

    Article  CAS  Google Scholar 

  • Endress, P. K. 1994. Diversity and evolutionary biology of tropical flowers. Cambridge University Press, Cambridge.

    Google Scholar 

  • Evans, M. M. S. &R. S. Poethig. 1997. Theviviparous8 mutation delays vegetative phase change and accelerates the rate of seedling growth in maize. Pl. J. 12: 769–779.

    Article  Google Scholar 

  • Ferguson, C. J., S. C. Huber, P. H. Hong &S. R. Singer. 1991. Determination for inflorescence development is a stable state, separable from determination for flower development inPisum sativum L.. Planta 185: 518–522.

    Article  Google Scholar 

  • Frohlich, M. W. &E. M. Meyerowitz. 1997. The search for flower homeotic gene homologs in basai angiosperms and gnetales: A potential new source of data on the evolutionary origin of flowers. Int. J. Pl. Sci. 158: S131-S142.

    Article  CAS  Google Scholar 

  • Grimes, J. 1996. Branch apices, heterochrony, and inflorescence morphology in some mimosoid legumes (Leguminosae: Mimosoidea). Telopea 6: 729–748.

    Google Scholar 

  • Hempel, F. D., P. C. Zambryski &L. J. Feldman. 1998. Photoinduction of flower identity in vegetatively biased primordia. Pl. Cell 10: 1663–1675.

    CAS  Google Scholar 

  • Hilu, K. W. 1983. The role of single-gene mutations in the evolution of flowering plants. Pp. 97–128in M. K. Hecht, B. Wallace & G. T. Prance (eds.), Evolutionary biology. Plenum Press, New York.

    Google Scholar 

  • Hofer, J., L. Turner, R. Hellens, M. Ambrose, P. Matthews, A. Michael &N. Ellis. 1997.UNIFOLIATA regulates leaf and flower morphogenesis in pea. Curr. Biol. 7: 581–587.

    Article  PubMed  CAS  Google Scholar 

  • Hole, C. C. &R. C. Hardwick. 1976. Development and control of the number of flowers per node inPisum sativum. London Ann. Bot. 40: 707–722.

    Google Scholar 

  • Kelly, A. J., M. B. Bonnlander &D. R. Meeks-Wagner. 1995. NF the tobacco homolog ofFLORICAULA andLEAFY, is transcriptionally expressed in both vegetative and floral meristems. Pl. Cell 7: 225–234.

    CAS  Google Scholar 

  • Kempin, S., B. Savidge &M. Yanofsky. 1995. Molecular basis of the cauliflower phenotype inArabidopsis. Science 267: 522–525.

    Article  PubMed  CAS  Google Scholar 

  • Luo, D., R. Carpenter, C. Vincent, L. Copsey &E. Coen. 1996. Origin of floral symmetry inAntirrhinum. Nature 383: 794–799.

    Article  PubMed  CAS  Google Scholar 

  • Mandel, M. A., C. Gustafson-Brown, B. Savidge &M. Yanofsky. 1992. Molecular characterization of theArabidopsis floral homeotic geneAPETALA1. Nature 360: 273–277.

    Article  PubMed  CAS  Google Scholar 

  • Marx, G. A. 1987. A suite of mutants that modify pattern formation in pea leaves. Pl. Molec. Biol. Reporter 5: 311–335.

    Article  Google Scholar 

  • McDaniel, C. N., S. R. Singer &S. M. E. Smith. 1992. Developmental states associated with the floral transition. Developm. Biol. 153: 59–69.

    Article  CAS  Google Scholar 

  • Millonig, G. 1961. Advantage of a phosphate buffer for OsO4 solutions in fixation. J. Appl. Physics 32: 1637.

    Google Scholar 

  • Munster, T. J. Pahnke, A. Di Rosa, J. Kim, W. Martin, H. Saedler &G. Theissen. 1997. Floral homeotic genes were recruited from homologous MADS-box genes preexisting in the common ancestor of ferns and seed plants. Proc. Natl. Acad. USA 94: 2415–2420.

    Article  CAS  Google Scholar 

  • Murfet, I. C. 1989. Flowering genes inPisum. Pp. 10–18in E. Lord & G. Bernier (eds.), Plant reproduction: From floral induction to pollination. American Society of Plant Physiologists, Rockville, MD.

    Google Scholar 

  • Parcy, F., O. Nilsson, M. A. Busch, I. Lee &D. Weigel. 1998. A genetic framework for floral patterning. Science 395: 561–566.

    CAS  Google Scholar 

  • Poethig, R. S. 1990. Phase change and the regulation of shoot morphogenesis in plants. Science 250: 923–930.

    Article  PubMed  Google Scholar 

  • Poteau, S., D. Nichols, F. Tooke, E. Coen &N. Batty. 1997. The induction and maintenance of flowering inImpatiens. Development 124: 3343–3351.

    Google Scholar 

  • Purugganan, M. D. 1997. The MADS-box floral homeotic gene lineages predate the origin of seed plants: Phylogenetic and molecular clock estimates. J. Molec. Evol. 45: 392–396.

    Article  PubMed  CAS  Google Scholar 

  • Ratcliffe, O. J., I. Amaya, C. A. Vincent, S. Rothstein, R. Carpenter, E. S. Coen &D. J. Bradley. 1998. A common mechanism controls the life cycle and architecture of plants. Development 125: 1609–1615.

    PubMed  CAS  Google Scholar 

  • Reid, J. B. &I. C. Murfet. 1984. Flowering inPisum: A fifth locus,veg. Ann. Bot. 53: 369–382.

    Google Scholar 

  • ——,S. R. Singer, J. L. Weiler &S. A. Taylor. 1996. Physiological-genetics of flowering inPisum. Seminars Cell & Developm. Biol. 7: 455–463.

    Article  CAS  Google Scholar 

  • Shannon, S. &D. R. Meeks-Wagner. 1991. A mutation in theArabidopsis TFL1 gene affects inflorescence meristem development. Pl. Cell 3: 877–892.

    CAS  Google Scholar 

  • ——. 1993. Genetic interactions that regulate inflorescence development inArabidopsis. Pl. Cell 5: 639–655.

    Google Scholar 

  • Singer, S. R., L. P. Hsiung &S. C. Huber. 1990. Determinate (det) mutant ofPisum sativum (Fabaceae: Papilionoideae) exhibits an indeterminate growth pattern. Amer. J. Bot. 77: 1330–1335.

    Article  Google Scholar 

  • Souer, E., A. van der Krol, D. Kloos, C. Spelt, M. Bliek, J. Mol &R. Koes. 1998. Genetic control of branching pattern and floral identity duringPetunia inflorescence development. Development 125: 733–742.

    PubMed  CAS  Google Scholar 

  • Stebbins, G. L. 1974. Flowering plants: Evolution above the species level. Harvard University Press, Cambridge, MA.

    Google Scholar 

  • Tucker, S. C. 1987. Pseudoracemes in papilionoid legumes: Their nature, development and variation. J. Linn. Soc., Bot. 95: 181–206.

    Article  Google Scholar 

  • —. 1989. Overlapping organ initiation and common primordia in flowersof Pisum sativum (Fabaceae: Papilionoideae). Amer. J. Bot. 76: 714–729.

    Article  Google Scholar 

  • —. 1997. Floral evolution, development, and convergence: The hierarchical-significance hypothesis. Int. J. Plant Sci. 158: S143-S161.

    Article  Google Scholar 

  • —. 1998. Floral ontogeny in legume generaPetalostylis, Labichea, andDialium (Caesalpinoideae: Cassieae), a series in floral reduction. Amer. J. Bot. 85: 184–208.

    Article  Google Scholar 

  • — &A. W. Douglas. 1994. Ontogenetic evidence and phylogenetic relationships among basal taxa of legumes. Pp. 11–32in I. K. Ferguson & S. C. Tucker (eds.), Advances in legume systematics. Pt. 6. Structural botany. Royal Botanic Gardens, Kew.

    Google Scholar 

  • Weberling, F. 1989. Morphology of flowers and inflorescences. Cambridge University Press, Cambridge.

    Google Scholar 

  • Weigel, D. 1995. The genetics of flower development: From floral induction to ovule morphogenesis. Annual Rev. Genet. 29: 19–39.

    Article  CAS  Google Scholar 

  • Weigel, D., J. Alvarez, D. R. Smyth, M. F. Yanofsky &E. M. Meyerowitz. 1992.LEAFY controls floral meristem identity inArabidopsis. Cell 69: 843–860.

    Article  PubMed  CAS  Google Scholar 

  • Weiler, J. L., J. B. Reid, S. A. Taylor &I. C. Murfet. 1997. The genetic control of flowering in pea. Trends Pl. Sci. 2:1360–1385.

    Google Scholar 

  • Wray, G. A. 1994. Developmental evolution: New paradigms and paradoxes. Developm. Genetics 15: 1–6.

    Article  CAS  Google Scholar 

  • Yanofsky, M. F., 1995. Floral meristems to floral organs: Genes controlling early events inArabidopsis flower development. Annual Rev. Pl. Physiol. & Pl. Molec. Biol. 46: 167–188.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biology, Carleton College, 55057, Northfleld, MN, USA

    Susan Singer, John Sollinger, Jason Fishbach, Brad Short, Catherine Reinke, Jennifer Fick, Laura Cox, Andrew McCall & Heidi Mullen

  2. Department of Horticulture, Clemson University, 29634, Clemson, SC, USA

    Sonja Maki

Authors
  1. Susan Singer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. John Sollinger
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sonja Maki
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jason Fishbach
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Brad Short
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Catherine Reinke
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jennifer Fick
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Laura Cox
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Andrew McCall
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Heidi Mullen
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Gene symbols used in this article: For clarity a common symbolization is used for genes of all species discussed in this article. Genes are symbolized with italicized capital letters. Mutant alleles are represented by lowercase, italicized letters. In both cases, the number immediately following the gene symbol differentiates among genes with the same symbol. If there are multiple alleles, a hyphen followed by a number is used to distinguish alleles. Protein products are represented by capital letters without italics.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Singer, S., Sollinger, J., Maki, S. et al. Inflorescence architecture: A developmental genetics approach. Bot. Rev 65, 385–410 (1999). https://doi.org/10.1007/BF02857756

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02857756

Keywords

Search

Navigation