Abstract
The first exposure to light marks a crucial transition in plant development. This transition relies on the transcription factor HY5 controlling a complex downstream growth program. Despite its importance, its function in transcription remains unclear. Previous studies have generated lists of thousands of potential target genes and competing models of HY5 transcription regulation. In this work, we carry out detailed phenotypic and molecular analysis of constitutive activator and repressor HY5 fusion proteins. Using this strategy, we were able to filter out large numbers of genes that are unlikely to be direct targets, allowing us to eliminate several proposed models of HY5's mechanism of action. We demonstrate that the primary activity of HY5 is promoting transcription and that this function relies on other, likely light-regulated, factors. In addition, this approach reveals a molecular feedback loop via the COP1/SPA E3 ubiquitin ligase complex, suggesting a mechanism that maintains low HY5 in the dark, primed for rapid accumulation to reprogram growth upon light exposure. Our strategy is broadly adaptable to the study of transcription factor activity. Lastly, we show that modulating this feedback loop can generate significant phenotypic diversity in both Arabidopsis (Arabidopsis thaliana) and tomato (Solanum lycopersicum).
Highlights
Plants continuously monitor the environment to tune development and optimize performance
We reasoned that the fusion proteins would repress (HY5-SRDX) or activate (HY5-VP16) the transcription of HYPOCOTYL 5 (HY5) direct targets
We identified in our list of 297 HY5regulated genes the E3 ubiquitin ligase complex components SPA1, SPA4, and CONSTITUTIVELY PHOTOMORPHOGENIC1 (COP1), which promote HY5 degradation (Figure 3D; Supplemental Data Set 2)
Summary
Plants continuously monitor the environment to tune development and optimize performance They sense changes in factors such as temperature, water availability, gravity, nutrients, and many aspects of light, the latter of which are sensed by a diverse array of photoreceptors and feed into a variety of growth programs (Chen et al, 2004). When light is a limiting factor, the seedling will use etiolated growth, characterized by an elongated embryonic stem (hypocotyl) with the apical hook and tightly closed embryonic leaves (cotyledons) protecting the meristematic tissue. Rapid elongation during this stage allows the plant to quickly emerge from the soil and gain access to light.
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