Studies in Drosophila circadian neurons reveal a bifurcation in the Pigment Dispersing Factor (PDF) neuropeptide signaling pathway, independently synchronizing circadian clocks via PKA or acutely controlling neuronal excitability via cAMP.

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 which 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).

Summary Circadian clocks in the brain are organized as coupled oscillators that integrate seasonal cues to time daily behaviors. In Drosophila, the PIGMENT DISPERSING FACTOR (PDF) neuropeptide expressing morning (M) and non-PDF evening (E) cells are coupled cell groups important for morning and evening behavior, respectively. Depending on day length, either M- (short days) or E-cells (long days) dictate both morning and evening phase, a phenomenon we term network hierarchy. To examine the role of PDF in light-dark conditions, we examined flies lacking both the PDF receptor (PDFR) and the circadian photoreceptor CRYPTOCHROME (CRY). We found that subsets of E-cells exhibit molecular oscillations antiphase to those of wild-type flies, single cry mutants, or single Pdfr mutants, demonstrating a potent role for PDF in light-mediated entrainment specifically in the absence of CRY. Moreover, evening behavioral phase is more strongly reset by PDF(+) M-cells in the absence of CRY. Based on our findings, we propose that CRY can gate PDF signaling to determine behavioral phase and network hierarchy.

Daily cycles of light and dark provide an organizing principle and temporal constraints under which life on Earth evolved. While light is often the focus of plant studies, it is only half the story. Plants continuously adjust to their surroundings, taking both dawn and dusk as cues to organize their growth, development and metabolism to appropriate times of day. In this review, we examine the effects of darkness on plant physiology and growth. We describe the similarities and differences between seedlings grown in the dark versus those grown in light–dark cycles, and the evolution of etiolated growth. We discuss the integration of the circadian clock into other processes, looking carefully at the points of contact between clock genes and growth-promoting gene-regulatory networks in temporal gating of growth. We also examine daily starch accumulation and degradation, and the possible contribution of dark-specific metabolic controls in regulating energy and growth. Examining these studies together reveals a complex and continuous balancing act, with many signals, dark included, contributing information and guiding the plant through its life cycle. The extraordinary interconnection between light and dark is manifest during cycles of day and night and during seedling emergence above versus below the soil surface.

The size of plant organs is highly responsive to environmental conditions. The plant’s embryonic stem, or hypocotyl, displays phenotypic plasticity, in response to light and temperature. The hypocotyl of shade avoiding species elongates to outcompete neighboring plants and secure access to sunlight. Similar elongation occurs in high temperature. However, it is poorly understood how environmental light and temperature cues interact to effect plant growth. We found that shade combined with warm temperature produces a synergistic hypocotyl growth response that dependent on PHYTOCHROME-INTERACTING FACTOR 7 (PIF7) and auxin. This unique but agriculturally relevant scenario was almost totally independent on PIF4 activity. We show that warm temperature is sufficient to promote PIF7 DNA binding but not transcriptional activation and we demonstrate that additional, unknown factor/s must be working downstream of the phyB-PIF-auxin module. Our findings will improve the predictions of how plants will respond to increased ambient temperatures when grown at high density.

Plants optimize their growth in fluctuating environments using information acquired by different organs. This information is then transmitted through the rest of the plant using both short- and long-distance signals, including hormones and mobile proteins. Although a few of these signals have been characterized, long-distance signaling is not well understood in plants. Recently, the light-regulated transcription factor HY5 was reported to move from the shoot to the root to regulate root growth. We generated a cell-type specifically expressed HY5 fusion protein that could not be detected outside the tissue in which it was targeted. By expressing this DOF-HY5 protein in specific cell types of the hypocotyl, we showed that its local activity was sufficient to regulate hypocotyl growth. We also found that, although DOF-HY5 was expressed specifically in the shoot and not detected in the roots, it could rescue hy5 growth defects in primary roots but not in lateral roots. We therefore conclude that HY5 protein mobility is not required in the hypocotyl or for shoot-to-root communication. Our results indicate that a signal downstream of, or in parallel with, HY5 in the shoot is mobile and links shoot and root growth.