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In plants, light receptors play a pivotal role in photoperiod sensing, enabling them to track seasonal progression. Photoperiod sensing arises from an interaction between the plant’s endogenous circadian oscillator and external light cues. Here, we characterize the role of phytochrome A (phyA) in photoperiod sensing. Our metaanalysis of functional genomic datasets identified phyA as a principal regulator of morning-activated genes, specifically in short photoperiods. We demonstrate that PHYA expression is under the direct control of the PHYTOCHROME INTERACTING FACTOR transcription factors, PIF4 and PIF5. As a result, phyA protein accumulates during the night, especially in short photoperiods. At dawn, phyA activation by light results in a burst of gene expression, with consequences for physiological processes such as anthocyanin accumulation. The combination of complex regulation of PHYA transcript and the unique molecular properties of phyA protein make this pathway a sensitive detector of both dawn and photoperiod.

In plants, light receptors play a pivotal role in photoperiod sensing, enabling them to track seasonal progression. Photoperiod sensing arises from an interaction between the plant's endogenous circadian oscillator and external light cues. Here, we characterise the role of phytochrome A (phyA) in photoperiod sensing. Our meta-analysis of functional genomic 15 datasets identified phyA as a principal transcriptional regulator of morning-activated genes, specifically in short photoperiods. We demonstrate that PHYA expression is under the direct control of the PHYTOCHROME INTERACTING FACTOR transcription factors, PIF4 and PIF5. As a result, phyA protein accumulates during the night, especially in short photoperiods. At dawn phyA activation by light results in a burst of gene expression, with consequences for 20 anthocyanin accumulation. The combination of complex regulation of PHYA transcript and the unique molecular properties of phyA protein make this pathway a sensitive detector of both dawn and photoperiod. Significance statementThe changing seasons subject plants to a variety of challenging environments. In order to deal 25 with this, many plants have mechanisms for inferring the season by measuring the duration of daylight in a day. A number of well-known seasonal responses such as flowering are responsive to daylength or photoperiod. Here, we describe how the photoreceptor protein phytochrome A senses short photoperiods. This arises from its accumulation during long nights, as happens during winter, and subsequent activation by light at dawn. As a result of this response, the 30 abundance of red anthocyanin pigments is increased in short photoperiods. Thus, we describe a mechanism underlying a novel seasonal phenotype in an important model plant species.

Damaged DNA Binding protein 1 (DDB1)–CULLIN4 E3 ubiquitin ligase complexes have been implicated in diverse biological processes in a range of organisms. Arabidopsis thaliana encodes two homologs of DDB1, DDB1A, and DDB1B. In this study we use a viable partial loss of function allele of DDB1B, ddb1b-2, to examine genetic interactions with DDB1A, DET1 and COP1. Although the ddb1b-2 ddb1a double mutant is lethal, ddb1a ddb1b-2/+ and ddb1b-2 ddb1a/+ heterozygotes exhibit few developmental phenotypes but do exhibit decreased tolerance of ultraviolet light. In addition, germination in ddb1a and ddb1a ddb1b-2/+ was found to be sensitive to salt and mannitol, and both DDB1 single mutants as well as the heterozygotes exhibited heat sensitivity. DE-ETIOLATED1 (DET1) and CONSTITUTIVE PHOTOMORPHOGENIC1 (COP1) are negative regulators of light development which interact with DDB1-CUL4 complexes. Although ddb1a strongly enhances det1 phenotypes in both dark- and light-grown seedlings, ddb1b-2 weakly enhanced the det1 short hypocotyl phenotype in the dark, as well as enhancing anthocyanin levels and suppressing the det1 low chlorophyll phenotype in light-grown seedlings. In adults, ddb1a suppresses det1 early flowering and enhances the det1 dwarf phenotype. A similar trend was observed in ddb1b-2 det1 double mutants, although the effects were smaller in magnitude. In cop1 mutants, ddb1b-2 enhanced the cop1-4 short hypocotyl phenotype in dark and light, enhanced anthocyanin levels in cop1-1 in the light, but had no effect in adults. Thus the requirement for DDB1B varies in the course of development, from COP1-specific effects in hypocotyls to DET1-specific in adults.

1 5 HEXOKINASE 1 (HXK1) is an evolutionarily conserved glycolytic enzyme that has a 1 6 separate nuclear glucose-sensor signalling function. In Arabidopsis, HXK1 mutant seedlings 1 7 have a stunted growth defect, yet how this relates to HXK1 function remains inconclusive. 1 8We show that the HXK1-glycolytic pathway performs a fundamental role in catabolising seed 1 9 reserves to fuel post-germinative cell division and expansion. This function is particularly 2 0 important in dim light which delays the switch to photoautotrophic growth. RNAseq analysis 2 1 reveals that HXK1 imposes strong repressive control on plastome gene expression, and 2 2 regulates nuclear-encoded genes that drive energy-consuming processes. Earlier studies 2 3 have implicated HXK1 sensor-signalling in the repression of CAB2 and CAA gene 2 4 expression by exogenous glucose. We show that over a wide range of irradiances this 2 5 pathway is not operative in seedlings. Our study therefore defines a new operational model 2 6for HXK1 action in catabolising carbon resources and tuning gene expression to optimize 2 7 seedling growth. 2 8 2 9

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