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Light signaling pathways and the circadian clock interact to help organisms synchronize physiological and developmental processes with periodic environmental cycles. The plant photoreceptors responsible for clock resetting have been characterized, but signaling components that link the photoreceptors to the clock remain to be identified. Here we describe a family of night lightinducible and clock-regulated genes (LNK) that play a key role linking light regulation of gene expression to the control of daily and seasonal rhythms in Arabidopsis thaliana. A genomewide transcriptome analysis revealed that most light-induced genes respond more strongly to light during the subjective day, which is consistent with the diurnal nature of most physiological processes in plants. However, a handful of genes, including the homologous genes LNK1 and LNK2, are more strongly induced by light in the middle of the night, when the clock is most responsive to this signal. Further analysis revealed that the morning phased LNK1 and LNK2 genes control circadian rhythms, photomorphogenic responses, and photoperiodic dependent flowering, most likely by regulating a subset of clock and flowering time genes in the afternoon. LNK1 and LNK2 themselves are directly repressed by members of the TIMING OF CAB1 EXPRESSION/PSEUDO RESPONSE REGULATOR family of core-clock genes in the afternoon and early night. Thus, LNK1 and LNK2 integrate early light signals with temporal information provided by core oscillator components to control the expression of afternoon genes, allowing plants to keep track of seasonal changes in day length.
The plant circadian clock allows organisms to anticipate the predictable changes in the environment by adjusting their developmental and physiological traits. In the last few years, it was determined that responses known to be regulated by the oscillator are also able to modulate clock performance. These feedback loops and their multilayer communications create a complex web, and confer on the clock network a role that exceeds the measurement of time. In this article, we discuss the current knowledge of the wiring of the clock, including the interplay with metabolism, hormone, and stress pathways in the model species Arabidopsis thaliana. We outline the importance of this system in crop agricultural traits, highlighting the identification of natural alleles that alter the pace of the timekeeper. We report evidence supporting the understanding of the circadian clock as a master regulator of plant life, and we hypothesize on its relevant role in the adaptability to the environment and the impact on the fitness of most organisms.
The mechanisms by which poikilothermic organisms ensure that biological processes are robust to temperature changes are largely unknown. Temperature compensation, the ability of circadian rhythms to maintain a relatively constant period over the broad range of temperatures resulting from seasonal fluctuations in environmental conditions, is a defining property of circadian networks. Temperature affects the alternative splicing (AS) of several clock genes in fungi, plants, and flies, but the splicing factors that modulate these effects to ensure clock accuracy throughout the year remain to be identified. Here we show that GEMIN2, a spliceosomal small nuclear ribonucleoprotein assembly factor conserved from yeast to humans, modulates low temperature effects on a large subset of pre-mRNA splicing events. In particular, GEMIN2 controls the AS of several clock genes and attenuates the effects of temperature on the circadian period in Arabidopsis thaliana. We conclude that GEMIN2 is a key component of a posttranscriptional regulatory mechanism that ensures the appropriate acclimation of plants to daily and seasonal changes in temperature conditions. spliceosome assembly | alternative splicing | circadian rhythms | Arabidopsis | GEMIN2 C ircadian clocks allow organisms to coordinate physiological processes with periodic environmental changes. The core of all circadian systems, in organisms ranging from cyanobacteria to humans, is a network of multiple interlocked feedback loops that operate at the transcriptional, translational, and posttranslational levels to sustain oscillations with a period of ∼24 h, even in the absence of environmental cues. An increasing body of evidence links alternative splicing (AS) with the regulation of circadian networks across eukaryotic organisms (1-3). The core clock genes period in Drosophila, frequency in Neurospora, and BMAL2 in humans undergo AS to give rise to different mRNA isoforms (1, 2, 4). In Arabidopsis, several core clock genes, including TIMING OF CAB EXPRESSION 1 (TOC1) and CIRCA-DIAN CLOCK ASSOCIATED 1 (CCA1), also undergo extensive AS (5-7).Interestingly, many of the alternative mRNA isoforms associated with the Arabidopsis core clock genes are abundant or alter their abundance upon changes in environmental conditions, suggesting that they have important physiological roles (5-7). For example, there is strong evidence that temperature regulation of CCA1 AS is critical for the proper functioning of circadian rhythms under cold conditions (8). Temperature also regulates the AS of frequency in Neurospora and period in Drosophila (1, 2), thereby promoting the proper functioning of circadian networks under the wide range of temperatures occurring throughout the seasons. Although our knowledge of the transcription factors that regulate clock function in different organisms has increased drastically over the last two decades, the splicing factors that modulate the AS patterns of core clock genes are only starting to be characterized (1). Splicing factors that mediate the effects...
Summary The Aux/IAA proteins are auxin-sensitive repressors that mediate diverse physiological and developmental processes in plants [1, 2]. There are 29 Aux/IAA genes in Arabidopsis that exhibit unique but partially overlapping patterns of expression [3] (Figure S1A). Although some studies have suggested that individual Aux/IAA genes have specialized function, genetic analyses of the family have been limited by the scarcity of loss-of-function phenotypes [4]. Further, with a few exceptions, our knowledge of the factors that regulate Aux/IAA expression is limited [1, 5]. We hypothesize that transcriptional control of Aux/IAA genes plays a central role in the establishment of the auxin-signaling pathways that regulate organogenesis, growth, and environmental response. Here we describe a screen for transcription factors (TFs) that regulate the Aux/IAA genes. We identify TFs from 38 families including 26 members of the DREB/CBF family. Several DREB/CBF TFs directly promote transcription of the IAA5 and IAA19 genes in response to abiotic stress. Recessive mutations in these IAA genes result in decreased tolerance to stress conditions demonstrating a role for auxin in abiotic stress. Our results demonstrate that stress pathways interact with the auxin gene regulatory network (GRN) through transcription of the Aux/IAA genes. We propose that the Aux/IAA genes function as hubs that integrate genetic and environmental information to achieve the appropriate developmental or physiological outcome.
Light modulates plant growth and development to a great extent by regulating gene expression programs. Here, we evaluated the effect of light on alternative splicing (AS) in light-grown Arabidopsis thaliana plants using high-throughput RNA sequencing (RNA-seq). We found that an acute light pulse given in the middle of the night, a treatment that simulates photoperiod lengthening, affected AS events corresponding to 382 genes. Some of these AS events were associated with genes involved in primary metabolism and stress responses, which may help to adjust metabolic and physiological responses to seasonal changes. We also found that several core clock genes showed changes in AS in response to the light treatment, suggesting that light regulation of AS may play a role in clock entrainment. Finally, we found that many light-regulated AS events were associated with genes encoding RNA processing proteins and splicing factors, supporting the idea that light regulates this posttranscriptional regulatory layer through AS regulation of splicing factors. Interestingly, the effect of a red-light pulse on AS of a gene encoding a splicing factor was not impaired in a quintuple phytochrome mutant, providing unequivocal evidence that nonphotosensory photoreceptors control AS in light-grown plants.
Optimizing the perception of external cues and regulating physiology accordingly help plants to cope with the constantly changing environmental conditions to which they are exposed. An array of photoreceptors and intricate signaling pathways allow plants to convey the surrounding light information and synchronize an endogenous timekeeping system known as the circadian clock. This biological clock integrates multiple cues to modulate a myriad of downstream responses, timing them to occur at the best moment of the day and the year. Notably, the mechanism underlying entrainment of the light-mediated clock is not clear. This review addresses known interactions between the light-signaling and circadian-clock networks, focusing on the role of light in clock entrainment and known molecular players in this process.
Summary Circadian clocks allow organisms to anticipate daily changes in the environment to enhance overall fitness. Transcription factors (TFs) play a prominent role in the molecular mechanism but are incompletely described possibly due to functional redundancy, gene family proliferation, and/or lack of context-specific assays. To overcome these, we performed a high-throughput yeast one-hybrid screen using the LUX ARRYHTHMO (LUX) gene promoter as bait against an Arabidopsis TF library. LUX is a unique gene because its mutation causes severe clock defects and transcript maintains high amplitude cycling in the cold. We report the well-characterized cold-inducible C-repeat (CRT)/drought-responsive element (DRE) binding factor CBF1/DREB1b is a transcriptional regulator of LUX. We show that CBF1 binds the CRT in the LUX promoter, and both genes overlap in temporal and spatial expression. CBF1 overexpression causes up-regulation of LUX and also alters other clock gene transcripts. LUX promoter regions including the CRT and Evening Element (EE) are sufficient for high amplitude transcriptional cycling in the cold, and cold-acclimated lux seedlings are sensitive to freezing stress. Our data show cold signaling is integrated into the clock by CBF-mediated regulation of LUX expression, thereby defining a new transcriptional mechanism for temperature input to the circadian clock.
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