Analysis of clock-regulated genes in Neurospora reveals widespread posttranscriptional control of metabolic potential

Nov 2, 2014Proceedings of the National Academy of Sciences of the United States of America

Daily cycle controls on genes in Neurospora show extensive regulation after gene copying that affects metabolism

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Abstract

40% of the transcriptome in Neurospora crassa may be expressed under circadian control.

Circadian control of gene expression is crucial for understanding eukaryotic physiology, including that of fungi.
Isolation of clock-controlled genes (ccgs) in Neurospora crassa highlighted the role of the WCC transcription factor in regulating circadian rhythms.
High-resolution sampling using RNA sequencing over 48 hours revealed that 10% to 40% of the transcriptome is regulated by circadian rhythms.
Functional analysis showed that circadian genes are heavily involved in metabolism, protein synthesis, and stress responses.
Daytime gene expression is associated with energy production and catabolism, while nighttime expression favors biosynthesis and growth.
Posttranscriptional regulation significantly influences the rhythmicity of mRNA levels, despite the importance of circadian activation.

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Neurospora crassa has been for decades a principal model for filamentous fungal genetics and physiology as well as for understanding the mechanism of circadian clocks. Eukaryotic fungal and animal clocks comprise transcription-translation-based feedback loops that control rhythmic transcription of a substantial fraction of these transcriptomes, yielding the changes in protein abundance that mediate circadian regulation of physiology and metabolism: Understanding circadian control of gene expression is key to understanding eukaryotic, including fungal, physiology. Indeed, the isolation of clock-controlled genes (ccgs) was pioneered in Neurospora where circadian output begins with binding of the core circadian transcription factor WCC to a subset of ccg promoters, including those of many transcription factors. High temporal resolution (2-h) sampling over 48 h using RNA sequencing (RNA-Seq) identified circadianly expressed genes in Neurospora, revealing that from ∼10% to as much 40% of the transcriptome can be expressed under circadian control. Functional classifications of these genes revealed strong enrichment in pathways involving metabolism, protein synthesis, and stress responses; in broad terms, daytime metabolic potential favors catabolism, energy production, and precursor assembly, whereas night activities favor biosynthesis of cellular components and growth. Discriminative regular expression motif elicitation (DREME) identified key promoter motifs highly correlated with the temporal regulation of ccgs. Correlations between ccg abundance from RNA-Seq, the degree of ccg-promoter activation as reported by ccg-promoter-luciferase fusions, and binding of WCC as measured by ChIP-Seq, are not strong. Therefore, although circadian activation is critical to ccg rhythmicity, posttranscriptional regulation plays a major role in determining rhythmicity at the mRNA level.

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Analysis of clock-regulated genes in Neurospora reveals widespread posttranscriptional control of metabolic potential

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