Epidermal GIGANTEA adjusts the response to shade at dusk by directly impinging on PHYTOCHROME INTERACTING FACTOR 7 function

ABSTRACT For plants adapted to bright light, a decrease in the amount of light received can be detrimental to their growth and survival. Consequently, in response to shade from surrounding vegetation, they initiate a suite of molecular and morphological changes known as the shade avoidance response (SAR) through which stems and petioles elongate in search for light. Under sunlight-night cycles, the plant’s responsiveness to shade varies across the day, being maximal at dusk time. While a role for the circadian clock in this regulation has long been proposed, mechanistic understanding of how it is achieved is incomplete. Here we show that the clock component GIGANTEA (GI) directly interacts with the transcriptional regulator PHYTOCHROME INTERACTING FACTOR 7 (PIF7), a key player in the response to shade. GI represses PIF7 transcriptional activity and the expression of its target genes in response to shade, thereby fine-tuning the magnitude of the response to limiting light conditions. We find that, under light/dark cycles, this function of GI is required to adequately modulate the gating of the response to shade at dusk. Importantly, we also show that GI expression in epidermal cells is sufficient for proper SAR regulation. SIGNIFICANCE Plants have a remarkable capacity to adapt to and cope with changes in environmental conditions. Because of the importance of light to their survival, plants have evolved sophisticated mechanisms to optimize responses to light. An outstanding adaptive response in terms of plant plasticity in dynamic light environments is the shade avoidance response which sun-loving plants deploy to escape canopy and grow towards the light. This response is the result of a complex signaling network in which cues from different pathways are integrated, including light, hormone, and circadian signaling. Within this framework, our study provides a mechanistic model of how the circadian clock contributes to this complex response by temporalizing the sensitivity to shade signals towards the end of the light period. In light of evolution and local adaptation, this work gives insights into a mechanism through which plants may have optimized resource allocation in fluctuating environments.