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A key innovation of flowering plants is the female reproductive organ, the carpel. Here, we show that a mechanism that regulates carpel margin development in the model flowering plant Arabidopsis thaliana was recruited from light-regulated processes. This recruitment followed the loss from the basic helix-loop-helix transcription factor SPATULA (SPT) of a domain previously responsible for its negative regulation by phytochrome. We propose that the loss of this domain was a prerequisite for the light-independent expression in female reproductive tissues of a genetic module that also promotes shade avoidance responses in vegetative organs. Striking evidence for this proposition is provided by the restoration of wild-type carpel development to spt mutants by low red/far-red light ratios, simulating vegetation shade, which we show to occur via phytochrome B, PHYTOCHROME INTERACTING FACTOR4 (PIF4), and PIF5. Our data illustrate the potential of modular evolutionary events to generate rapid morphological change and thereby provide a molecular basis for neo-Darwinian theories that describe this nongradualist phenomenon. Furthermore, the effects shown here of light quality perception on carpel development lead us to speculate on the potential role of light-regulated mechanisms in plant organs that, like the carpel, form within the shade of surrounding tissues.
INTRODUCTION
The flowering plants, or angiosperms, arose suddenly from an unknown ancestor in the early Cretaceous and rapidly became the dominant form of terrestrial vegetation. Angiosperms reproduce by means of the flower, whose principal defining feature is the carpel. This novel female reproductive organ encloses the ovules, providing numerous benefits in reproductive efficiency over the naked ovules typically present in the remaining seed plants or gymnosperms (Scutt et al., 2006). A number of genes are known to regulate the development of the two fused carpels that make up the gynoecium, or female floral whorl, in the model angiosperm Arabidopsis thaliana. Among these, the basic helix-loop-helix (bHLH) transcription factor SPATULA (SPT) (Heisler et al., 2001) plays a key role in regulating the development of the stigma, style, and septum, which emerge from the carpel margins to close the gynoecium and provide a route for pollen tube growth (Alvarez and Smyth, 1999). In spt mutants, these tissues show reduced cell elongation and lack extracellular matrix-secreting cells, which make up the pollen transmitting tissue of the style and septum (Alvarez and...