Circadian Waves of Expression of the APRR1/TOC1 Family of Pseudo-Response Regulators in Arabidopsis thaliana : Insight into the Plant Circadian Clock

Abstract

The Arabidopsis pseudo-response regulator, APRR1, has a unique structural design containing a pseudo-receiver domain and a C-terminal CONSTANS motif. This protein was originally characterized as a presumed component of the His-to-Asp phosphorelay systems in Arabidopsis thaliana. Recently, it was reported that APRR1 is identical to the TOC1 gene product, a mutational lesion of which affects the periods of many circadian rhythms in Arabidopsis plants. TOC1 is believed to be a component of the presumed circadian clock (or central oscillator). Based on these facts, in this study four more genes, each encoding a member of the APRR1/TOC1 family of pseudo-response regulators were identified and characterized with special reference to circadian rhythms. It was found that all these members of the APRR1/TOC1 family (APRR1, APRR3, APRR5, APRR7, and APRR9) are subjected to a circadian rhythm at the level of transcription. Furthermore, in a given 24 h period, the APRR-mRNAs started accumulating sequentially after dawn with 2-3 h intervals in the order of APRR9-->APRR7-->APRR5-->APRR3-->APRR1. These sequential events of transcription, termed 'circadian waves of APRR1/TOCI', were not significantly affected by the photoperiod conditions, if any (e.g. both long and short days), and the expression of APRR9 was first boosted always after dawn. Among these APRRs, in fact, only the expression of APRR9 was rapidly and transiently induced also by white light, whereas such light responses of others were very dull, if any. These results collectively support the view that these members of the APRR1/TOC1 family are together all involved in an as yet unknown mechanism underlying the Arabidopsis circadian clock. Here we propose that the circadian waves of the APRR1/TOC1 family members are most likely a molecular basis of such a biological clock in higher plants.

PSEUDO RESPONSE REGULATORs stabilize CONSTANS protein to promote flowering in response to day length

“…In A. thaliana, PRR proteins are encoded by a family of five genes and are defined as central components of the circadian clock ( TIMING OF CAB EXPRESSION 1 ( TOC1 ), PRR3 , PRR5 , PRR7, and PRR9 ) (Strayer et al , 2000; Ito et al , 2003; Yamamoto et al , 2003; Murakami et al , 2004; Para et al , 2007). The abundance of their transcripts and proteins exhibit circadian rhythms, and under diurnal conditions, they peak in expression sequentially at 2–3 h intervals during the light period in the order PRR9 , PRR7 , PRR5 , PRR3 , and TOC1 (Matsushika et al , 2000; Fujiwara et al , 2008). PRR9, PRR7, PRR5, and TOC1 proteins are degraded during the night, so they mainly accumulate during the day when they repress transcription of genes encoding other clock components such as LATE ELONGATED HYPOCOTYL (LHY) and CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) (Mas et al , 2003b; Farré & Kay, 2007; Ito et al , 2007; Kiba et al , 2007; Nakamichi et al , 2010; Huang et al , 2012).…”

A Constitutively Active Allele of Phytochrome B Maintains Circadian Robustness in the Absence of Light

“…CIRCADIAN CLOCK ASSOCIATED1 (CCA1) and LATE ELON-GATED HYPOCOTYL (LHY) are morning-phased, light-inducible transcription factors that induce expression of PSEUDO-RESPONSE REGULATOR9 (PRR9; Schaffer et al, 1998;Wang and Tobin, 1998;Farré et al, 2005). PRR9, whose transcription is itself light induced (Ito et al, 2003;Jones et al, 2012), represses expression of CCA1 and LHY in partnership with the later-phased PRR7, PRR5, and TIMING OF CAB1 (TOC1; Matsushika et al, 2000;Nakamichi et al, 2010). Later in the subjective day, TOC1 and REVEILLE8 act as negative and positive transcription factors, respectively, that act to reinforce the robust oscillations of circadian genes (Farinas and Más, 2011;Gendron et al, 2012;Huang et al, 2012;Hsu et al, 2013).…”

Phase-Specific Circadian Clock Regulatory Elements in Arabidopsis

“…However, TOC1 (APRR1) has been shown to bind to PHYTOCHROME-INTERACTING FACTOR 3 (PIF3), a Myc-related basic helix-loop-helix transcription factor, and to the related PIF3-LIKE 1 (PIL1; Makino et al, 2002). Expression of each of the three clock components, TOC1, CCA1, and LHY, is circadian regulated (Schaffer et al, 1998;Wang and Tobin, 1998;Matsushika et al, 2000;Strayer et al, 2000). TOC1 (APRR1) and CCA1/LHY make up a feedback loop in which TOC1 acts as a positive regulator of CCA1 and LHY, which in turn are negative regulators of TOC1 (Alabadí et al., 2001).…”