Abstract

BackgroundThe genus Aquilegia is an emerging model system in plant evolutionary biology predominantly because of its wide variation in floral traits and associated floral ecology. The anatomy of the Aquilegia flower is also very distinct. There are two whorls of petaloid organs, the outer whorl of sepals and the second whorl of petals that form nectar spurs, as well as a recently evolved fifth whorl of staminodia inserted between stamens and carpels.Methodology/Principal FindingsWe designed an oligonucleotide microarray based on EST sequences from a mixed tissue, normalized cDNA library of an A. formosa x A. pubescens F2 population representing 17,246 unigenes. We then used this array to analyze floral gene expression in late pre-anthesis stage floral organs from a natural A. formosa population. In particular, we tested for gene expression patterns specific to each floral whorl and to combinations of whorls that correspond to traditional and modified ABC model groupings. Similar analyses were performed on gene expression data of Arabidopsis thaliana whorls previously obtained using the Ath1 gene chips (data available through The Arabidopsis Information Resource).Conclusions/SignificanceOur comparative gene expression analyses suggest that 1) petaloid sepals and petals of A. formosa share gene expression patterns more than either have organ-specific patterns, 2) petals of A. formosa and A. thaliana may be independently derived, 3) staminodia express B and C genes similar to stamens but the staminodium genetic program has also converged on aspects of the carpel program and 4) staminodia have unique up-regulation of regulatory genes and genes that have been implicated with defense against microbial infection and herbivory. Our study also highlights the value of comparative gene expression profiling and the Aquilegia microarray in particular for the study of floral evolution and ecology.

Highlights

  • Flowers intrigue us because of their great diversity of form, colour and smell

  • With contrast 7 we tested if the B domain is extended to petaloid sepals; with contrasts 9 and 11 we tested if the B and C domains are extended to staminodia and with contrasts 10 and 7 we tested the extent to which stamens and staminodia or carpels and staminodia were similar in gene expression, respectively

  • We analysed whorl- and domain-specific gene expression patterns in two publically available datasets of Arabidopsis thaliana. These data are comprised of triplicate measurements of global gene expression in pre- and postanthesis A. thaliana flowers obtained with Affymetrix Ath1 microarrays

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Summary

Introduction

Flowers intrigue us because of their great diversity of form, colour and smell. This diversity is largely thought to be the result of co-evolution between flowering plants and pollinators, which dates to the Cretaceous when flowering plants first arose [1]. For one aspect of floral form, the identity of floral organs, the ABC model has been developed. It states that combinations of three classes of regulatory genes specify the development of sepals (A genes), petals (A + B genes), stamens (B+C genes) and carpels (C genes) [2]. B genes are expressed throughout the sterile whorls of monocots and many magnoliid dicots [3,4,5] and, as predicted by the ABC model, the entire perianths of these taxa have similar appearances as opposed to clearly distinct sepals and petals. There are two whorls of petaloid organs, the outer whorl of sepals and the second whorl of petals that form nectar spurs, as well as a recently evolved fifth whorl of staminodia inserted between stamens and carpels

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