Evolutionary dynamics of genes controlling floral development
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.
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