Evolutionary dynamics of genes controlling floral development

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Advances in the understanding of floral developmental genetics in model species such as Arabidopsis continue to provide an important foundation for comparative studies in other flowering plants. In particular, floral organ identity genes are the focus of many projects that are addressing both ancient and recent evolutionary questions. Expanded analyses of the evolution of these gene lineages have highlighted the dynamic nature of the gene birth-and-death process, and may have significant implications for the evolution of genetic pathways. Crucial functional studies of floral organ identity genes in diverse taxa are allowing the first real insight into the conservation of gene function, while findings on the genetic control of organ elaboration offer to open up new avenues for investigation. Taken together, these trends show that the field of floral developmental evolution continues to make significant progress towards elucidating the processes that have shaped the evolution of flower development and morphology.

Introduction

The beauty and complexity of flowers have held the fascination of scientists for centuries, from Linnaeus, to Goethe, to Darwin, through to the present. Given the enormous degree of morphological diversity present in angiosperm flowers, it is not surprising that the genes that control floral development have become an important focus of the plant ‘evo-devo’ field. In particular, considerable attention has been given to the evolution of the floral organ identity genes, most of which are MIKC-type MADS-box-containing transcription factors (see [1] for review). As a result, this plant-specific group is among the most thoroughly studied gene families, especially in terms of the evolution of gene lineage [2]. MADS-box genes are not the only players in floral development, however, and several other crucial loci have been drawn into the spotlight. In this review, we outline recent progress in the field of floral developmental evolution and discuss the broader implications of these findings.

Section snippets

Floral organ identity genes and the ABC model

For well over a decade, the ABC model (Figure 1a) has formed the foundation of our understanding of floral development [3]. This program, which is based on work done with homeotic mutants of Arabidopsis and Antirrhinum, has also led to an emphasis on the MADS-box gene family, which includes all but one of the loci traditionally associated with the model (Figure 1b; [1]). Recently, reverse genetic studies of other MADS-box genes have led to the proposal of two additional groups, the D- and

Sorting out A function

In Arabidopsis, there are two genes that are formally assigned to the A class, APETALA1 (AP1) and AP2 [1]. It is interesting to note, however, that the MADS-box gene AP1 was not considered an organ identity gene in the original versions of the model; rather it was described solely in terms of its role in floral meristem identity 3., 6., 7.. AP1 was added as an A-class gene after its expression was found to be restricted to the outer two whorls by the repressive activity of the C-function gene

Elaboration of B-function genes

Of all the organ identity gene lineages, perhaps the best understood from an evolutionary standpoint are the B-class genes, represented in Arabidopsis by the MADS-box genes APETALA3 (AP3) and PISTILLATA (PI) (Figure 1b). These two closely related lineages were produced by a gene duplication that apparently predated the angiosperm radiation but occurred after the last common ancestor of seed plants [16]. Recent studies of B-gene homologs in basal angiosperms have confirmed this, but show that

Conservation and diversity in C- and E-function genes

As with the AP1 and AP3 gene lineages, understanding the evolution of function in the AG lineage begins with acquiring a better picture of the evolutionary history of this C-class gene. A first step in the process has recently been taken, revealing now familiar patterns of gene duplication [21]. This study shows that an ancestral AG-like MADS-box gene underwent duplication before the radiation of the angiosperms to produce two paralogous lineages, termed C and D. The former lineage includes

Beyond organ identity: organ elaboration and inflorescence architecture

Until recently, most of what we knew about floral development was limited to the stage at which organ identity was established, and few direct targets of the ABC genes were identified. This has changed significantly, however, because of the application of a combination of forward-genetic and whole-genome approaches. Using microarray-based techniques, several groups have been able to identify large sets of genes that are expressed in developing floral organs 28., 29.. These findings have the

Conclusions and perspectives

Several broad themes emerge from the disparate lines of research described in this review. Perhaps the most striking is the mercurial nature of MADS-box genes, which seem to have an almost bothersome tendency to retain paralogs. Although this predilection may cause frustration when seeking to make functional comparisons across distantly related taxa, it represents a unique opportunity to study many cases in which evolution has acted on independent duplicates of a common gene lineage. Among the

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

We thank Liam Dolan and Michael Freeling for the opportunity to contribute to this issue and apologize to authors whose work we did not have room to discuss. Our laboratory receives funding from the National Science Foundation (IBN-0319103) and JCH is supported by a Mercer Fellowship from the Arnold Arboretum of Harvard University.

References (47)

  • E.M. Meyerowitz et al.

    A genetic and molecular model for floral development in Arabidopsis thaliana

    Dev Suppl

    (1991)
  • C. Gustafson-Brown et al.

    Regulation of the Arabidopsis floral homeotic gene APETALA1

    Cell

    (1994)
  • V.F. Irish et al.

    Function of the apetela-1 gene during Arabidopsis floral development

    Plant Cell

    (1990)
  • P. Huijser et al.

    Bractomania, an inflorescence anomaly, is caused by the loss of function of the MADS-box gene squamosa in Antirrhinum majus

    EMBO J

    (1992)
  • H. Yu et al.

    AGAMOUS-LIKE 24, a dosage-dependent mediator of the flowering signals

    Proc Natl Acad Sci USA

    (2002)
  • H. Yu et al.

    Repression of AGAMOUS-LIKE 24 is a crucial step in promoting flower development

    Nat Genet

    (2004)
  • A. Litt et al.

    Duplication and diversification in the APETALA1/FRUITFULL floral homeotic gene lineage: implications for the evolution of floral development

    Genetics

    (2003)
  • M. Vandenbussche et al.

    Structural diversification and neo-functionalization during floral MADS-box gene evolution by C-terminal frameshift mutations

    Nucleic Acids Res

    (2003)
  • A. Becker et al.

    A novel MADS-box gene subfamily with a sister-group relationship to class B floral homeotic genes

    Mol Genet Genomics

    (2002)
  • S. Aoki et al.

    Phylogeny and divergence of basal angiosperms inferred from APETALA3- and PISTILLATA-like MADS-box genes

    J Plant Res

    (2004)
  • G.M. Stellari et al.

    Evolution of the APETALA3 and PISTILLATA lineages of MADS-box containing genes in basal angiosperms

    Mol Biol Evol

    (2004)
  • E.M. Kramer et al.

    Molecular evolution of genes controlling petal and stamen development: duplication and divergence within the APETALA3 and PISTILLATA MADS-box gene lineages

    Genetics

    (1998)
  • M. Vandenbussche et al.

    The duplicated B-class heterodimer model: whorl-specific effects and complex genetic interactions in Petunia hybrida flower development

    Plant Cell

    (2004)
  • Cited by (0)

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