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

Matsushika, Akinori; Makino, Seiya; Kojima, Masaru; Mizuno, Takeshi

doi:10.1093/pcp/pcd043

Cited by 381 publications

(359 citation statements)

References 53 publications

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“…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).…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2017

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Seasonal reproduction in many organisms requires detection of day length. This is achieved by integrating information on the light environment with an internal photoperiodic time‐keeping mechanism. Arabidopsis thaliana promotes flowering in response to long days (LDs), and CONSTANS (CO) transcription factor represents a photoperiodic timer whose stability is higher when plants are exposed to light under LDs. Here, we show that PSEUDO RESPONSE REGULATOR (PRR) proteins directly mediate this stabilization. PRRs interact with and stabilize CO at specific times during the day, thereby mediating its accumulation under LDs. PRR‐mediated stabilization increases binding of CO to the promoter of FLOWERING LOCUS T (FT), leading to enhanced FT transcription and early flowering under these conditions. PRRs were previously reported to contribute to timekeeping by regulating CO transcription through their roles in the circadian clock. We propose an additional role for PRRs in which they act upon CO protein to promote flowering, directly coupling information on light exposure to the timekeeper and allowing recognition of LDs.

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Section: Introductionmentioning

confidence: 99%

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

et al. 2017

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“…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).…”

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

Jones

Litthauer

et al. 2015

Plant Physiology

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The sensitivity of the circadian system to light allows entrainment of the clock, permitting coordination of plant metabolic function and flowering time across seasons. Light affects the circadian system via both photoreceptors, such as phytochromes and cryptochromes, and sugar production by photosynthesis. In the present study, we introduce a constitutively active version of phytochrome B-Y276H (YHB) into both wild-type and phytochrome null backgrounds of Arabidopsis (Arabidopsis thaliana) to distinguish the effects of photoreceptor signaling on clock function from those of photosynthesis. We find that the YHB mutation is sufficient to phenocopy red light input into the circadian mechanism and to sustain robust rhythms in steady-state mRNA levels even in plants grown without light or exogenous sugars. The pace of the clock is insensitive to light intensity in YHB plants, indicating that light input to the clock is constitutively activated by this allele. Mutation of YHB so that it is retained in the cytoplasm abrogates its effects on clock function, indicating that nuclear localization of phytochrome is necessary for its clock regulatory activity. We also demonstrate a role for phytochrome C as part of the red light sensing network that modulates phytochrome B signaling input into the circadian system. Our findings indicate that phytochrome signaling in the nucleus plays a critical role in sustaining robust clock function under red light, even in the absence of photosynthesis or exogenous sources of energy.

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“…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).…”

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confidence: 99%

Phase-Specific Circadian Clock Regulatory Elements in Arabidopsis

2002

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We have defined a minimal Arabidopsis CATALASE 3 (CAT3) promoter sufficient to drive evening-specific circadian transcription of a LUCIFERASE reporter gene. Deletion analysis and site-directed mutagenesis reveal a circadian response element, the evening element (EE: AAAATATCT), that is necessary for evening-specific transcription. The EE differs only by a single base pair from the CIRCADIAN CLOCK ASSOCIATED 1-binding site (CBS: AAAAAATCT), which is important for morning-specific transcription. We tested the hypothesis that the EE and the CBS specify circadian phase by site-directed mutagenesis to convert the CAT3 EE into a CBS. Changing the CAT3 EE to a CBS changes the phase of peak transcription from the evening to the morning in continuous dark and in light-dark cycles, consistent with the specification of phase by the single base pair that distinguishes these elements. However, rhythmicity of the CBS-containing CAT3 promoter is dramatically compromised in continuous light. Thus, we conclude that additional information normally provided in the context of a morning-specific promoter is necessary for full circadian activity of the CBS.The circadian clock enables an organism to specifically partition aspects of its biology to precise times over the day (Dunlap, 1999). Although the circadian clock is, by definition, endogenous and continues to run in the absence of external time cues, environmental stimuli such as light and temperature act to entrain the internal processes of an organism both to the exact external daily period and in a defined relationship, or phase angle, to the diurnal cycle. For example, in Arabidopsis, light and temperature information are integrated to partition physiological activities such as circadian-regulated leaf movement, stomatal opening, and gene expression to distinct times of day or phases (McClung et al., 2002).A central theme that has emerged in circadian biology is that the core oscillator is composed of a negative feedback loop grounded in positive and negative transcriptional regulation (Dunlap, 1999). It has recently been demonstrated that the Arabidopsis circadian clock entails such a transcriptional feedback loop (Alabadí et al., 2001) that includes at least three components: TIMING OF CAB EXPRESSION 1 (TOC1; also called Arabidopsis PSEUDO-RESPONSE REGULATOR 1, APRR1; Millar et al., 1995;, CIRCADIAN CLOCK ASSOCIATED 1 (CCA1; Wang and Tobin, 1998), and LATE ELON-GATED HYPOCOTYL (LHY; Schaffer et al., 1998).CCA1 and LHY are single-Myb domain transcription factors, and DNA-binding activity of CCA1 to a CCA1-binding site (CBS: AAAAATCT) has been characterized (Wang et al., 1997). The hypothesized role of TOC1 as a transcription factor is based on similarity to CONSTANS, although DNA binding by TOC1 has not been experimentally established (Strayer et al., 2000). 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 o...

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

Cited by 381 publications

References 53 publications

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

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

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

Phase-Specific Circadian Clock Regulatory Elements in Arabidopsis

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