Within and between Whorls: Comparative Transcriptional Profiling of Aquilegia and Arabidopsis

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.

Comparative transcriptomics among floral organs of the basal eudicot Eschscholzia californica as reference for floral evolutionary developmental studies

“…Our comparison of the gene expression patterns in E. californica , Aquilegia , Persea and Arabidopsis showed that the E. californica results support a 'sharp border' model, similar to that for core eudicots such as Arabidopsis , rather than the 'fading border' model in other basal angiosperms [29,62]. This is consistent with the clear morphological distinction of sepals and petals, and the lack of intermediate floral organs such as staminodes in E. californica flowers.…”

Conservation and canalization of gene expression during angiosperm diversification accompany the origin and evolution of the flower

“…17) and support the inference that this model is the ancestral regulatory program for flowers. A shared transcriptional program across the perianth organs and stamens of Aquilegia (Ranunculales) (33) suggests that some form of "fading borders" operates in some basal members of the eudicot clade as well. Moreover, extrapolating the trajectory of floral transcriptome evolution to its likely origin leads to an ancestrally uniform program in which separate components (if any) overlap fully, resembling the genetic program operating in unisexual gymnosperm cones (Fig.…”

Predictable transcriptome evolution in the convergent and complex bioluminescent organs of squid

“…Although previous transcriptomic comparisons from long-diverged species indicate that largely conserved gene expression profiles characterize homologous traits (6,7), the potentially labile nature of gene expression suggests that widespread changes in gene expression could readily produce similar phenotypic outcomes over short evolutionary times (8)(9)(10), especially if natural selection acts on a clearly optimal phenotype. In contrast, if gene expression patterns are evolutionarily conserved, perhaps by historical or developmental constraints, then homologous traits should have highly correlated expression, whereas convergent traits should be less correlated because of their different evolutionary origins (11)(12)(13)(14). Depending on the extent to which genes are recruited and/or modulated in parallel, expression levels of genes in convergent traits may be more correlated than expression levels of genes in two dissimilar, nonhomologous traits.…”

“…S1). In addition to using elaborate, eye-like optical devices such as concave reflectors and large crystallin lenses to project emitted light (8)(9)(10)20), these photophores enable E. scolopes to control the intensity of ventrally directed light and to distort the silhouette produced from down-welling light (11,12,21,22). The photophore interior in E. scolopes comprises epithelial crypts capable of mediating bacterial growth and detecting light (15,16,19,23,24).…”