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Circadian Clock-Controlled Translation of Specific mRNAs in Neurospora crassa Requires Rhythmic eIF2α Activity and P-body Sequestration

ABSTRACT: This SuperSeries is composed of the SubSeries listed below.

ORGANISM(S): Neurospora crassa

PROVIDER: GSE181566 | GEO | 2022/09/23

REPOSITORIES: GEO

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Circadian Clock-Controlled Translation of Specific mRNAs in Neurospora crassa Requires Rhythmic eIF2α Activity and P-body Sequestration [Ribo-seq]

Project description:We report the genome-wide impact of rhythmic P-eIF2α levels in vivo by performing ribosome profiling and RNA-seq in Neurospora crassa samples grown over a circadian time course. We identified candidate genes which showed rhyhmic ribosome occupancy in WT cells but lost rhythms in mRNA levels and ribosome occupancy in the clock mutant Dfrq, eIF2α kinase knockout Dcpc-3, and constitutively active kinase mutant cpc-3c cells. Select mRNAs harbor a P-body localization motif identified by MEME and MEME Suite's GOMo function. P-body localization of the target mRNAs provides an attractive mechanism for explaining translational rhythms from otherwise arrhythmic mRNAs.

2022-09-23 | GSE181565 | GEO

Circadian Clock-Controlled Translation of Specific mRNAs in Neurospora crassa Requires Rhythmic eIF2α Activity and P-body Sequestration [RNA-seq]

2022-09-23 | GSE181564 | GEO

Circadian Clock-Controlled Translation of Specific mRNAs in Neurospora crassa Requires Rhythmic eIF2α Activity and P-body Sequestration

Project description:Circadian Clock-Controlled Translation of Specific mRNAs in Neurospora crassa Requires Rhythmic eIF2α Activity and P-body Sequestration

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Circadian Clock-Controlled Translation of Specific mRNAs in Neurospora crassa Requires Rhythmic eIF2α Activity and P-body Sequestration [RNA-seq]

Project description:Circadian Clock-Controlled Translation of Specific mRNAs in Neurospora crassa Requires Rhythmic eIF2α Activity and P-body Sequestration [RNA-seq]

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Circadian Clock-Controlled Translation of Specific mRNAs in Neurospora crassa Requires Rhythmic eIF2α Activity and P-body Sequestration [Ribo-seq]

Project description:Circadian Clock-Controlled Translation of Specific mRNAs in Neurospora crassa Requires Rhythmic eIF2α Activity and P-body Sequestration [Ribo-seq]

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Circadian clock control of eIF2α phosphorylation is necessary for rhythmic translation initiation.

Project description:The circadian clock in eukaryotes controls transcriptional and posttranscriptional events, including regulation of the levels and phosphorylation state of translation factors. However, the mechanisms underlying clock control of translation initiation, and the impact of this potential regulation on rhythmic protein synthesis, were not known. We show that inhibitory phosphorylation of eIF2α (P-eIF2α), a conserved translation initiation factor, is clock controlled in Neurospora crassa, peaking during the subjective day. Cycling P-eIF2α levels required rhythmic activation of the eIF2α kinase CPC-3 (the homolog of yeast and mammalian GCN2), and rhythmic activation of CPC-3 was abolished under conditions in which the levels of charged tRNAs were altered. Clock-controlled accumulation of P-eIF2α led to reduced translation during the day in vitro and was necessary for the rhythmic synthesis of select proteins in vivo. Finally, loss of rhythmic P-eIF2α levels led to reduced linear growth rates, supporting the idea that partitioning translation to specific times of day provides a growth advantage to the organism. Together, these results reveal a fundamental mechanism by which the clock regulates rhythmic protein production, and provide key insights into how rhythmic translation, cellular energy, stress, and nutrient metabolism are linked through the levels of charged versus uncharged tRNAs.

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Isoform switching facilitates period control in the Neurospora crassa circadian clock.

Project description:A striking and defining feature of circadian clocks is the small variation in period over a physiological range of temperatures. This is referred to as temperature compensation, although recent work has suggested that the variation observed is a specific, adaptive control of period. Moreover, given that many biological rate constants have a Q(10) of around 2, it is remarkable that such clocks remain rhythmic under significant temperature changes. We introduce a new mathematical model for the Neurospora crassa circadian network incorporating experimental work showing that temperature alters the balance of translation between a short and long form of the FREQUENCY (FRQ) protein. This is used to discuss period control and functionality for the Neurospora system. The model reproduces a broad range of key experimental data on temperature dependence and rhythmicity, both in wild-type and mutant strains. We present a simple mechanism utilising the presence of the FRQ isoforms (isoform switching) by which period control could have evolved, and argue that this regulatory structure may also increase the temperature range where the clock is robustly rhythmic.

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Circadian clock regulation of the glycogen synthase (<i>gsn</i>) gene by WCC is critical for rhythmic glycogen metabolism in <i>Neurospora crassa</i>.

Project description:Circadian clocks generate rhythms in cellular functions, including metabolism, to align biological processes with the 24-hour environment. Disruption of this alignment by shift work alters glucose homeostasis. Glucose homeostasis depends on signaling and allosteric control; however, the molecular mechanisms linking the clock to glucose homeostasis remain largely unknown. We investigated the molecular links between the clock and glycogen metabolism, a conserved glucose homeostatic process, in Neurospora crassa We find that glycogen synthase (gsn) mRNA, glycogen phosphorylase (gpn) mRNA, and glycogen levels, accumulate with a daily rhythm controlled by the circadian clock. Because the synthase and phosphorylase are critical to homeostasis, their roles in generating glycogen rhythms were investigated. We demonstrate that while gsn was necessary for glycogen production, constitutive gsn expression resulted in high and arrhythmic glycogen levels, and deletion of gpn abolished gsn mRNA rhythms and rhythmic glycogen accumulation. Furthermore, we show that gsn promoter activity is rhythmic and is directly controlled by core clock component white collar complex (WCC). We also discovered that WCC-regulated transcription factors, VOS-1 and CSP-1, modulate the phase and amplitude of rhythmic gsn mRNA, and these changes are similarly reflected in glycogen oscillations. Together, these data indicate the importance of clock-regulated gsn transcription over signaling or allosteric control of glycogen rhythms, a mechanism that is potentially conserved in mammals and critical to metabolic homeostasis.

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Circadian activation of the mitogen-activated protein kinase MAK-1 facilitates rhythms in clock-controlled genes in Neurospora crassa.

Project description:The circadian clock regulates the expression of many genes involved in a wide range of biological functions through output pathways such as mitogen-activated protein kinase (MAPK) pathways. We demonstrate here that the clock regulates the phosphorylation, and thus activation, of the MAPKs MAK-1 and MAK-2 in the filamentous fungus Neurospora crassa. In this study, we identified genetic targets of the MAK-1 pathway, which is homologous to the cell wall integrity pathway in Saccharomyces cerevisiae and the extracellular signal-regulated kinase 1/2 (ERK1/2) pathway in mammals. When MAK-1 was deleted from Neurospora cells, vegetative growth was reduced and the transcript levels for over 500 genes were affected, with significant enrichment for genes involved in protein synthesis, biogenesis of cellular components, metabolism, energy production, and transcription. Additionally, of the ~500 genes affected by the disruption of MAK-1, more than 25% were previously identified as putative clock-controlled genes. We show that MAK-1 is necessary for robust rhythms of two morning-specific genes, i.e., ccg-1 and the mitochondrial phosphate carrier protein gene NCU07465. Additionally, we show clock regulation of a predicted chitin synthase gene, NCU04352, whose rhythmic accumulation is also dependent upon MAK-1. Together, these data establish a role for the MAK-1 pathway as an output pathway of the circadian clock and suggest a link between rhythmic MAK-1 activity and circadian control of cellular growth.

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