A CYC-RAD-DIV-DRIF interaction likely pre-dates the origin of floral monosymmetry in Lamiales.

BACKGROUND: An outstanding question in evolutionary biology is how genetic interactions defining novel traits evolve. They may evolve either by de novo assembly of previously non-interacting genes or by en bloc co-option of interactions from other functions. We tested these hypotheses in the context of a novel phenotype-Lamiales flower monosymmetry-defined by a developmental program that relies on regulatory interaction among CYCLOIDEA, RADIALIS, DIVARICATA, and DRIF gene products. In Antirrhinum majus (snapdragon), representing Lamiales, we tested whether components of this program likely function beyond their previously known role in petal and stamen development. In Solanum lycopersicum (tomato), representing Solanales which diverged from Lamiales before the origin of Lamiales floral monosymmetry, we additionally tested for regulatory interactions in this program. RESULTS: We found that RADIALIS, DIVARICATA, and DRIF are expressed in snapdragon ovaries and developing fruit, similar to their homologs during tomato fruit development. In addition, we found that a tomato CYCLOIDEA ortholog positively regulates a tomato RADIALIS ortholog. CONCLUSION: Our results provide preliminary support to the hypothesis that the developmental program defining floral monosymmetry in Lamiales was co-opted en bloc from a function in carpel development. This expands our understanding of novel trait evolution facilitated by co-option of existing regulatory interactions.

Novel Traits, Flower Symmetry, and Transcriptional Autoregulation: New Hypotheses From Bioinformatic and Experimental Data.

A common feature in developmental networks is the autoregulation of transcription factors which, in turn, positively or negatively regulate additional genes critical for developmental patterning. When a transcription factor regulates its own expression by binding to cis-regulatory sites in its gene, the regulation is direct transcriptional autoregulation (DTA). Indirect transcriptional autoregulation (ITA) involves regulation by proteins expressed downstream of the target transcription factor. We review evidence for a hypothesized role of DTA in the evolution and development of novel flowering plant phenotypes. We additionally provide new bioinformatic and experimental analyses that support a role for transcriptional autoregulation in the evolution of flower symmetry. We find that 5' upstream non-coding regions are significantly enriched for predicted autoregulatory sites in Lamiales CYCLOIDEA genes-an upstream regulator of flower monosymmetry. This suggests a possible correlation between autoregulation of CYCLOIDEA and the origin of monosymmetric flowers near the base of Lamiales, a pattern that may be correlated with independently derived monosymmetry across eudicot lineages. We find additional evidence for transcriptional autoregulation in the flower symmetry program, and report that Antirrhinum DRIF2 may undergo ITA. In light of existing data and new data presented here, we hypothesize how cis-acting autoregulatory sites originate, and find evidence that such sites (and DTA) can arise subsequent to the evolution of a novel phenotype.