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 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...
Growing evidence suggests that core spliceosomal components differentially affect RNA processing of specific genes; however, whether changes in the levels or activities of these factors control specific signaling pathways is largely unknown. Here we show that some SM-like (LSM) genes, which encode core components of the spliceosomal U6 small nuclear ribonucleoprotein complex, regulate circadian rhythms in plants and mammals. We found that the circadian clock regulates the expression of LSM5 in Arabidopsis plants and several LSM genes in mouse suprachiasmatic nucleus. Further, mutations in LSM5 or LSM4 in Arabidopsis, or down-regulation of LSM3, LSM5, or LSM7 expression in human cells, lengthens the circadian period. Although we identified changes in the expression and alternative splicing of some core clock genes in Arabidopsis lsm5 mutants, the precise molecular mechanism causing period lengthening remains to be identified. Genome-wide expression analysis of either a weak lsm5 or a strong lsm4 mutant allele in Arabidopsis revealed larger effects on alternative splicing than on constitutive splicing. Remarkably, large splicing defects were not observed in most of the introns evaluated using RNA-seq in the strong lsm4 mutant allele used in this study. These findings support the idea that some LSM genes play both regulatory and constitutive roles in RNA processing, contributing to the fine-tuning of specific signaling pathways.posttranscriptional | alternative splicing | circadian clock | Arabidopsis | mammals C ircadian rhythms are persistent 24-h oscillations in biological processes that occur under constant environmental conditions. They allow organisms to coordinate multiple physiological processes with periodic or seasonal changes that occur in the environment. At the heart of the eukaryotic circadian system lies a complex set of interconnected transcriptional and translational feedback loops, in which a group of core clock genes regulate each other to ensure that their mRNA levels oscillate with a period of ∼24 h (1). The core oscillator in Arabidopsis thaliana involves two MYB domain-containing transcription factors, CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) and LATE ELONGATED HYPOCOTYL (LHY), that repress the expression of TIMING OF CAB2 EXPRESSION 1 (TOC1) at the beginning of the day. In turn, TOC1, a member of the PSEUDO-RESPONSE REGULATOR (PRR) family, represses CCA1/LHY expression at the end of the day (2). Other clock components expressed throughout the day form multiple interconnected transcriptional feedback loops (2).Mounting evidence indicates that alternative splicing (AS), the process by which pre-mRNA molecules are differentially spliced to yield multiple mRNA isoforms from a single gene, plays a key role in the regulation of circadian networks in a variety of organisms, including Drosophila melanogaster (3), Neurospora crassa (4-6), and Arabidopsis (7-11). For example, the core clock genes period in Drosophila and frequency in Neurospora give rise to different mRNA isoforms through AS, which helps t...
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