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Review
. 2015 Jan 20;54(2):157-70.
doi: 10.1021/bi500922q. Epub 2014 Dec 30.

Circadian clock and photoperiodic response in Arabidopsis: from seasonal flowering to redox homeostasis

Jae Sung Shim  1 , Takato Imaizumi
Affiliations
Review

Circadian clock and photoperiodic response in Arabidopsis: from seasonal flowering to redox homeostasis

Jae Sung Shim et al. Biochemistry. .

Abstract

Many of the developmental responses and behaviors in plants that occur throughout the year are controlled by photoperiod; among these, seasonal flowering is the most characterized. Molecular genetic and biochemical analyses have revealed the mechanisms by which plants sense changes in day length to regulate seasonal flowering. In Arabidopsis thaliana, induction of the expression of a florigen, FLOWERING LOCUS T (FT) protein, is a major output of the photoperiodic flowering pathway. The circadian clock coordinates the expression profiles and activities of the components in this pathway. Light-dependent control of CONSTANS (CO) transcription factor activity is a crucial part of the induction of the photoperiodic expression of FT. CO protein is stabilized only in the long day afternoon, which is when FT is induced. In this review, we summarize recent progress in the determination of the molecular architecture of the circadian clock and mechanisms underlying photoperiodic flowering. In addition, we introduce the molecular mechanisms of other biological processes, such as hypocotyl growth and reactive oxygen species production, which are also controlled by alterations in photoperiod.

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Figures

Figure 1
Figure 1
Expression of circadian clock proteins and the architecture of the clock in Arabidopsis thaliana. (A) Daily protein expression profiles of circadian clock components. The expression profiles of the clock proteins are based on the following: CCA1, RVE8, PRR9, PRR7,ZTL, PRR5, Evening Complex (ELF4–ELF3–LUX), and TOC1. The peak expression levels of these proteins were set to 100%, and the rest of the expression levels were calculated against the peak levels. The levels of expression are plotted at 2 h intervals throughout the day. (B) Molecular events occurring from morning to afternoon in the circadian clock. The interactions of clock components and their transcriptional targets, which mainly happen from morning to afternoon, are depicted. In the morning, CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) and LATE ELONGATED HYPOCOTYL (LHY) activate the expression of PSEUDO-RESPONSE REGULATOR 9 (PRR9) and PRR7 and suppress the expression of most evening phase genes such as PRR5, TIMING OF CAB EXPRESSION 1 (TOC1), LUX ARRHYTHMO (LUX), and EARLY FLOWERING 4 (ELF4). CCA1 and LHY form a repressor complex with the CONSTITUTIVE PHOTOMORPHOGENIC 10 (COP10)–DE-ETIOLATED 1 (DET1)–DAMAGED DNA BINDING 1 (DDB1) complex (CDD) to suppress the expression of the evening genes. CCA1 and LHY also suppress their own expression. In the early afternoon, PRR9 and PRR7 suppress the expression of CCA1 and LHY using TOPLESS (TPL) as a corepressor. Downregulation of CCA1 and LHY expression results in derepression of evening phase genes. RVE8, together with NIGHT LIGHT-INDUCIBLE AND CLOCK-REGULATED GENES 1 and 2 (LNK1/2) as coactivators, directly activates expression of evening phase genes, such as PRR5, TOC1, ELF4, and LUX. (C) Molecular events occurring from evening to night in the circadian clock. The interactions of clock components and their transcriptional targets, which mainly happen from evening to the end of the night, are depicted. PRR5 protein continuously suppresses the expression of CCA1 and LHY. PRR5 also represses its own expression. TOC1 suppresses the expression of CCA1 and LHY by itself or interacting with CCA1 HIKING EXPEDITION (CHE). TOC1 also suppresses the expression of other clock components, PRR9, PRR7, TOC1, GI, LUX, and ELF4. ZTL interacts with PRR5 and TOC1 to degrade them in the dark. The Evening Complex (ELF4–ELF3–LUX) suppresses the expression of PRR9 to complete the cycle by induction of CCA1 and LHY. The positions of the circles in panels B and C indicate the timing of peak protein accumulation (based on panel A) of each component.
Figure 2
Figure 2
Photoperiodic regulation of FLOWERING LOCUS T (FT) expression. In LD, FLAVIN-BINDING, KELCH REPEAT, F-BOX1 (FKF1), and GIGANTEA (GI) form a complex, when their expression patterns coincide and FKF1 absorbs blue light. The FKF1–GI complex degrades CYCLING DOF FACTOR (CDF) proteins on the CONSTANS (CO) promoter in the afternoon. FKF1–GI-dependent degradation of CDFs results in derepression of CONSTANS (CO) expression. The same mechanism of degradation of CDFs by the FKF1–GI complex also exists on the FT promoter. FKF1 physically interacts with CO protein to stabilize it. Far-red light-absorbed PHYTOCHROME A (PHYA) also stabilizes CO protein. Stabilized CO protein binds to the FT promoter to activate FT expression. The NUCLEAR FACTOR-Y (NF-Y) complex enhances the binding of CO protein to the FT promoter. CO protein antagonizes the function of the EMBRYONIC FLOWERING 1 complex (EMF1c) and the FLOWERING LOCUS C (FLC) complex that suppresses the expression of FT. CRYPTOCHROME-INTERACTING BASIC HELIX–LOOP–HELIX 1 (CIB1) is activated by blue light absorbed by CRYPTOCHROME 2 (CRY2) and stabilized by blue light absorbed by ZEITLUPE (ZTL). CIB1 directly activates the expression of FT in the afternoon. In the morning, PHYB that has absorbed red light and HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENE 1 (HOS1) degrade CO protein. At night, the CONSTITUTIVE PHOTOMORPHOGENIC 1 (COP1)–SUPPRESSOR OF PHYA-105s (SPAs) complex degrades CO protein. They prevent flowering under unfavorable conditions, such as SD. In SD, the expression peaks of FKF1 and GI do not coincide. Without the FKF–GI complex, CO expression is continuously suppressed by CDF proteins during the daytime.
Figure 3
Figure 3
Photoperiodic regulation of hypocotyl elongation. The hypocotyl elongation rate of plants is determined by a combination of the internal circadian clock and external photoperiodic information. Expression of PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) is controlled by the circadian clock. The Evening Complex (ELF4–ELF3–LUX) directly suppresses the expression of PIF4. Under LD conditions, both transcription and translation of PIF4 occur during the day. PIF4 that accumulates during the daytime is inactivated by PHYB and DELLA protein. PHYB interacts with PIF4 to degrade it, and DELLAs interact with residual PIF4 to inactivate it by interrupting its DNA binding activity. Under SD conditions, PIF4 transcription and translation occur during day and night. PIF4 that accumulates during the nighttime activates its downstream target genes, which regulate hormonal responses that trigger hypocotyl elongation. We used the experimental data of DELLA protein expression under SD conditions to illustrate DELLA protein expression in both LD and SD.
Figure 4
Figure 4
Circadian regulation of ROS homeostasis. (A) Circadian regulation of ROS homeostasis. The circadian clock regulates the daily expression patterns of three catalase genes (CAT1–CAT3) and their activities to maintain cellular hydrogen peroxide (H2O2) levels. (B) Day length-dependent phenotype of the cat2 mutant. The cat2 mutant shows the lesion (cell death) phenotype when it is grown only under LD conditions.
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