Circadian Control of Messenger RNA Stability. Association with a Sequence-Specific Messenger RNA Decay Pathway

Abstract

New Hampshire 03755 (P.A.S., C.R.M.)Transcriptional and posttranscriptional regulation are well-established mechanisms for circadian gene expression. Among the latter, differential messenger RNA (mRNA) stability has been hypothesized to control gene expression in response to the clock. However, direct proof that the rate of mRNA turnover can be regulated by the clock is lacking. Previous microarray expression data for unstable mRNAs in Arabidopsis (Arabidopsis thaliana) revealed that mRNA instability is associated with a group of genes controlled by the circadian clock. Here, we show that CCR-LIKE (CCL) and SENESCENCE ASSOCIATED GENE 1 transcripts are differentially regulated at the level of mRNA stability at different times of day. In addition, the changes in CCL mRNA stability continue under free-running conditions, indicating that it is controlled by the Arabidopsis circadian clock. Furthermore, we show that these mRNAs are targets of the mRNA degradation pathway mediated by the downstream (DST) instability determinant. Disruption of the DST-mediated decay pathway in the dst1 mutant leads to aberrant circadian mRNA oscillations that correlate with alterations of the half-life of CCL mRNA relative to parental plants in the morning and afternoon. That this is due to an effect on the circadian control is evidenced by mRNA decay experiments carried out in continuous light. Finally, we show that the defects exhibited by dst mutants are reflected by an impact on circadian regulation at the whole plant level. Together, these results demonstrate that regulation of mRNA stability is important for clock-controlled expression of specific genes in Arabidopsis. Moreover, these data uncover a connection between circadian rhythms and a sequence-specific mRNA decay pathway.Plants, like many other organisms, have internal clocks that command biological rhythms with a period close to 24 h. These rhythms provide selective advantages because they allow anticipation of the daily changes in environmental conditions (Ouyang et al., 1998;Green et al., 2002). Examples of processes that can exhibit circadian rhythms in plants are leaf movement, hypocotyl elongation, stomatal opening, and floral induction (for review, see McClung, 2001). At the molecular level, DNA microarray experiments have shown that 2% to 6% of Arabidopsis (Arabidopsis thaliana) mRNAs can oscillate (Harmer et al., 2000;Schaffer et al., 2001). For Arabidopsis and other circadian clocks studied to date, the core circadian oscillator is comprised of transcriptional feedback loops. The underlying master oscillator in Arabidopsis is believed to include the LATE ELONGATED HYPO-COTYL (LHY; Schaffer et al., 1998), the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1; Wang and Tobin, 1998), and the TIMING OF CAB EXPRESSION 1 (TOC1; Millar et al., 1995;Strayer et al., 2000) genes. Similar to what is observed in other systems (Glossop et al., 1999), the clock components form a regulatory loop in which TOC1 positively regulates LHY and CCA1 gene expression, and LHY and CCA1 proteins in turn...

Posttranscriptional Control of Photosynthetic mRNA Decay under Stress Conditions Requires 3′ and 5′ Untranslated Regions and Correlates with Differential Polysome Association in Rice

“…1C). Cordycepin treatments were effective in rice in blocking transcription, as evidenced by the reduced half-lives of EXPL2 (AK068088) and SEN1 (AK120910), rice homologs of Arabidopsis genes that produce very unstable mRNAs (Gutierrez et al, 2002;Lidder et al, 2005;Xu and Chua, 2009), under normal growth conditions (Supplemental Fig. S5).…”

“…Measurements of mRNA Half-Lives mRNA half-lives were determined as described previously by Lidder et al (2005). Briefly, 2-week-old rice seedlings were transferred to tap water and grown for 2 d. Cordycepin (39-deoxyadenosine) was added to a final concentration of 1 mM.…”

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Loss of Nocturnin, a circadian deadenylase, confers resistance to hepatic steatosis and diet-induced obesity

“…There are several examples of rhythmic posttranscriptional regulation in which the mRNA half-life or adenylation state changes over the course of the day (16)(17)(18)(19), but very little is known about the mechanisms responsible. A likely contributor is Nocturnin (Ccrn4l, Noc), which has been implicated in the posttranscriptional regulation of mRNA stability and/or translatability by the circadian clock (20).…”

Biological Clocks and the Coordination Theory of RNA Operons and Regulons

“…Among the distilled data in these studies were cyclic changes in mRNAs that encode both transcription factors and RBPs. For example, transcription factors Zfp36 and Sox3 show circadian expression in mammalian organs, and the RNA regulators nocturnin (Ccr4 deadenylase) and butyrate response factor (BRF1) show cyclic circadian expression as well (Panda et al 2002;Storch et al 2002;Lidder et al 2005). In addition, the RBP, LARK also cycles with circadian rhythms and was found to activate translation of the mRNA encoding the Period protein in the suprachiasmatic nucleus in the mouse brain (Kojima et al 2007).…”