Floral developmental genetics of Aquilegia and the Ranunculales
Members of the family Ranunculaceae offer the opportunity to test the “sliding boundary” hypothesis and study the evolution of novel perianth morphologies. This is due to the coexistence of two distinctly different types of petaloid organs in many genera of the family. In the first whorl of these flowers, the organs are petaloid but have many of the developmental hallmarks of sepals, which is how botanists refer to them. We will refer to these organs as whorl one-type petaloid organs. Many genera of the family exhibit an additional form of petaloid organ, which although sterile and petaloid, bears a striking likeness to stamens in all aspects of its development and even, in many cases, its final appearance. Botanists simply refer to these organs as petals, but here we will distinguish them as whorl two-type petaloid organs. Across the family, a wide variety of perianth forms are observed as a result of different combinations and elaborations of these two petal types (see above). In some genera, such as Anemonella, only whorl one-type petaloid organs are produced. In other cases, as with Aquilegia, both types are almost always present. Some genera have species representing both these morphologies, as exemplified by Clematis. In still other cases, the first whorl organs resemble leaf-like sepals and the whorl two-type petaloid organs are much less staminoid. Although this last type of perianth, found most notably in Ranunculus, resembles that of the core eudicots, these second whorl petals are thought to share an ancestry with the staminoid, nectiferous whorl two-type petals found in species like Xanthorhiza. It should be noted that the phylogeny of the family is well established and is consistent with a single evolution of whorl two-type petaloid organs, followed by several losses. Alternatively, these petals may have arisen many times in parallel, as has been suggested by botanists. Thus, the Ranunculaceae affords us the opportunity to study simple versions of the sliding boundary hypothesis, where the first whorl organs are petaloid, as well as more complex modifications, such as in genera where two distinct types of petaloid organs are present.
We began this study by examining the evolution of the AP3 and PI gene lineages across the family Ranunculaceae (Kramer et al., 2003). This work demonstrated that two ancient duplications in the AP3 lineage gave rise to three paralogous lineages which have been retained in many members of the family. In contrast, the multiple PI paralogs that we detected are the products of comparatively recent duplications. We are currently expanding this study across the Ranunculales and similar analyses of the AG and AP1 lineages are underway.
In order to understand the functional implications of these duplications events and whether they relate to the multiple types of petaloid organs produced across the family, we have decided to focus on the genus Aquilegia as a model for floral genetics in the Ranunculaceae. We are currently studying the floral expression patterns of homologs of all the Arabidopsis floral organ identity genes in Aquilegia. Functional studies of the PI homolog demonstrate that the B class genes are involved in the identity of the petals, stamens and novel staminodia (a fifth organ type observed in this genus, Kramer et al., 2007). Further experiments are targeting each of the three Aquilegia AP3 paralogs to help us understand how they have experienced sub- and neofunctionalization. The availability of floral homeotic mutants in Aquilegia (see Flower Gallery), as well as the development of a wide array of genomic and genetic tools, will allow us to directly assess the functions of these genes in vivo and discover new candidate genes for the development of novel structures such as the nectar spur and the staminodia. Long term, we hope to conduct comparative gene expression studies across additional representatives of the Ranunculaceae and Ranunculales in order to determine whether shifts in the expression patterns of the floral organ identity genes are associated with radical changes in perianth structure. This work is supported by a grant from the Developmental Systems Program of NSF.
Kramer, E.M., Di Stilio, V.S., and Schlüter, P. (2003). Complex patterns of gene duplication in the APETALA3 and PISTILLATA lineages of the Ranunculaceae. International Journal of Plant Science 164, 1-11.
Kramer, E. M., L. Holappa, B. Gould, M. A. Jaramillo, D. Setnikov, and P. Santiago. (2007)
Elaboration of B gene function to include the identity of novel floral organs in the lower
eudicot Aquilegia (Ranunculaceae). Plant Cell, 19:750-766.
