Regulation of output from the plant circadian clock

REVIEW ARTICLE

Regulation of output from the plant circadian clockEsther Yakir, Dror Hilman, Yael Harir and Rachel M. Green

Department of Plant Sciences and the Environment, Institute for Life Sciences, Hebrew University, Jerusalem, Israel

What is a circadian system?2

Circadian systems are widespread endogenous mecha-

nisms that allow organisms to time their physiological

changes to predictable day ⁄night cycles. They have

evolved in a wide range of organisms, from cyano-

bacteria to mammals, indicating their importance in

life processes. Among an enormous variety of 24 h

rhythms that are controlled by the circadian system

are nitrogen-fixation in cyanobacteria, olfactory

responses in Drosophila and sleep patterns in humans

[1]. The basic oscillator mechanism that generates the

rhythms is being elucidated in several model organisms

[1] and consists of transcriptional–translational posit-

ive ⁄negative feedback loops involving a group of clock

genes. The oscillator can be set (entrained) by signals

from the environment, such as the daily changes in

light and temperature, transduced via input pathways.

Finally, output pathways link the oscillator to the var-

ious biological processes whose rhythms it controls.

The Arabidopsis circadian oscillator

Most of the work on the circadian oscillator in plants

has been carried out using the model plant Arabidopsis

thaliana. The plant oscillator appears to be comprised

Keywords

circadian; Arabidopsis; plant; output;

pathway; transcription; oscillator; hormone;

calcium

Correspondence

R. M. Green, Department of Plant Sciences

and the Environment, Institute for Life

Sciences, Hebrew University, Givat Ram,

Jerusalem 91904, Israel

Fax: +972 2 658 4425

Tel. +972 2 658 5391

E-mail: [email protected]

(Received 24 October 2006, accepted

23 November 2006)

doi:10.1111/j.1742-4658.2006.05616.x

Plants, like many other organisms, have endogenous biological clocks that

enable them to organize their physiological, metabolic and developmental

processes so that they occur at optimal times. The best studied of these biolo-

gical clocks are the circadian systems that regulate daily (� 24 h) rhythms.

At the core of the circadian system in every organism are oscillators respon-

sible for generating circadian rhythms. These oscillators can be entrained

(set) by cues from the environment, such as daily changes in light and tem-

perature. Completing the circadian clock model are the output pathways that

provide a link between the oscillator and the various biological processes

whose rhythms it controls. Over the past few years there has been a tremen-

dous increase in our understanding of the mechanisms of the oscillator and

entrainment pathways in plants and many useful reviews on the subject. In

this review we focus on the output pathways by which the oscillator regulates

rhythmic plant processes. In the first part of the review we describe the role of

the circadian system in regulation at all stages of a plant’s development, from

germination and growth to reproductive development as well as in multiple

cellular processes. Indeed, the importance of a circadian clock for plants can

be gauged by the fact that so many facets of plant development are under its

control. In the second part of the review we describe what is known about the

mechanisms by which the circadian system regulates these output processes.

Abbreviations

APRR7, ARABIDOPSIS PSEUDORESPONSE REGULATOR 7; APRR9, ARABIDOPSIS PSEUDORESPONSE REGULATOR 9; CAT3,

CATALASE 3; CBS, CCA1-binding site; CCA1, CIRCADIAN CLOCK ASSOCIATED 11 ; CCL, CCR-LIKE; CCR1, COLD CIRCADIAN RHYTHM

RNA BINDING 1; CCR2, COLD CIRCADIAN RHYTHM RNA BINDING 2; CK, cytokinin; CO, CONSTANS; DST, downstream element;

EE, evening element; FT, FLOWERING LOCUS T; GA, gibberellin; Hd1, heading date 1; Hd3A, heading date 3A; IAA, indole-3-acetic acid;

LHY, LATE ELONGATED HYPOCOTYLS; LUX, LUX ARRYTHMO; RCA, RUBISCO ACTIVASE; SEN1, SENESCENCE-ASSOCIATED GENE 1;

TOC1, TIMING OF CAB1.

FEBS Journal 274 (2007) 335–345 ª 2006 The Authors Journal compilation ª 2006 FEBS 335

of components analogous to those described in other

model organisms. Over the past decade, several puta-

tive Arabidopsis clock components have been identified

through mutational analysis and have been proposed

to form a positive ⁄negative feedback loop to generate

circadian rhythms. Towards the end of the night, the

positive element, TIMING OF CAB1 (TOC1), is

involved in inducing the expression of CIRCADIAN

CLOCK ASSOCIATED 1 (CCA1) and LATE ELON-

GATED HYPOCOTYL (LHY) [2]. CCA1 and LHY

are known to encode transcription factors that,

in vitro, can be phosphorylated [3,4] and can bind the

TOC1 promoter [2]. Thus, during the day, CCA1 and

LHY might directly repress the expression of TOC1.

Towards evening, following a drop in levels of CCA1

and LHY, TOC1 expression increases, completing the

feedback loop. More recently, additional genes, inclu-

ding EARLY FLOWERING 4 (ELF4), GIGANTEA

(GI) and LUX ARRYTHMO (LUX), and feedback

loops have been identified suggesting that the oscillator

is more complex and may be composed of several

interlocking feedback loops [2,5–9]. Such an arrange-

ment is likely to be important for conferring stability

to the oscillator and is part of the mechanism ensuring

that the circadian system is able to function accurately

under a range of environmental conditions [10–12].

Clearly, to be of use to an organism, an oscillator

needs to be entrained by environmental signals [13].

Light and temperature are the most important of such

signals. Phytochromes, cryptochromes and members of

the ZTL ⁄FKF1 ⁄LPK2 family of proteins [14–16] have

all been shown to be light receptors for entrainment

[17,18]. Several genes, including EARLY FLOWER-

ING 3 (ELF3) and TIME FOR COFFEE (TIC) have

also been implicated in the input signaling pathways

from light to the clock [19,20].

There is not always, however, a clear distinction

between oscillator and input elements in the circadian

system. For example, the TOC1 paralogs, ARABI-

DOPSIS PSEUDORESPONSE REGULATORS 7

and 9 (APRR7 and APRR9) both appear to function

as part of the oscillatory mechanism, possibly forming

an additional regulatory feedback loop similar to those

found in other organisms [21,22]. At the same time,

APRR7 and APRR9 also have a role in regulating

light and temperature input to the oscillator [13,21].

Output processes regulated by thecircadian oscillator

Because there are already many excellent recent

reviews on the mechanism of the oscillator and its

entrainment [13,23,24], we focus on output from the

oscillator. We start with an overview of the multiple

roles that the circadian system has in regulation at all

stages of a plant’s life before describing what is known

about the mechanisms by which the circadian system

regulates these output processes.

The role of the circadian system during

development

The circadian clock controls many developmental pro-

cesses throughout the life cycle of the plant. Some of

these processes take place on a daily basis and are

directly regulated by the circadian clock. Others occur

annually and are controlled by changes in day-length

(photoperiod) that are detected by the circadian system.

Germination

At the earliest stage of development the circadian sys-

tem may regulate seed germination (Fig. 1A). In many

species, including downy birch (Betula pubescens), Lap-

land diapensia (Diapensia lapponica) and leatherleaf

(Chamaedaphne calyculata), germination is controlled

by day-length [25–28]. The existence of photoperiodic

control of germination suggests that, at least in some

plant species, the circadian system is functioning in

seeds. Consistent with this idea, imbibition (the absorb-

ance of water) by Arabidopsis seeds synchronizes circa-

dian-controlled gene expression [29]. Furthermore, in

dry (quiescent) onion (Allium cepa) seeds there is a

circadian rhythm in gas exchange that continues in con-

stant darkness [30], indicating that there may be a func-

tioning oscillator in seeds even before germination.

Growth

The circadian system continues to regulate many devel-

opmental processes that occur shortly after germina-

tion. For example, Arabidopsis hypocotyls elongate

with a circadian pattern immediately upon germination

(Fig. 1B). The rate of hypocotyl growth is greatest in

the evening and minimal in the morning, and can be

entrained by light even before the cotyledons emerge

from the seed coat [31]. A similar pattern of elongation

has also been found in adult plants such as tomato

(Lycopersicon esculentum) and red goosefoot (Chenopo-

dium rubrum) [32–34]. Cotyledon and leaf movements

are regulated by the circadian system in Arabidopsis

and other species like legumes (Fig. 1C) [31,35]. How-

ever, the mechanisms, for example, changes in cell

turgor and differential cell growth, controlling the

movements vary between species. The rate of Arabid-

opsis stem circumnutations is also under circadian

Circadian clock output in plants E. Yakir et al.

336 FEBS Journal 274 (2007) 335–345 ª 2006 The Authors Journal compilation ª 2006 FEBS

control (Fig. 1D), and is greatest at dawn [36]. During

the growth period, the circadian clock also regulates

shade-avoidance responses (Fig. 1E) that enable plants

to detect competition from other plants for light

energy and react by enhancing stem and petiole growth

[37].

Reproductive development

The best-characterized developmental phenomenon

regulated by the circadian clock is the transition from

vegetative to reproductive development via the photo-

periodic pathway (Fig. 1F). Some 70 years ago a

model was proposed for photoperiodic sensing [38].

According to this model, called the external coinci-

dence model, the circadian clock controls the expres-

sion of a light-sensitive component. When there is a

coincidence between light and sufficiently high levels of

the light-sensitive component in the leaves, flowering is

promoted. In recent years, research on Arabidopsis (a

plant that flowers earlier under conditions of long

days) has shown that the protein encoded by the CON-

STANS (CO) gene is the light-sensitive component

[39]. Briefly, the circadian clock controls CO mRNA

levels so that under long days CO transcript levels

start to rise well before sunset and stay high till the

next morning. Under short days CO mRNA accumu-

lates to significant levels only after sunset [40] and

although CO translation occurs rapidly the protein is

unstable in the dark. By contrast, during the day far-

red and blue light stabilize CO protein, and CO

accumulates in the nucleus [41]. CO then activates the

transcription of the floral regulator FLOWERING

LOCUS T (FT) [42]. FT mRNA, and possibly protein,

moves from the leaf to the shoot apex and promotes

flowering [43].

Interestingly, the components of the photoperiodic

flowering pathway appear to be conserved even in

plants that have a very different developmental

response to increasing day-length. Thus, in rice (Oryza

sativa), a plant that flowers early under short days, the

CONSTANS homolog Hd1 also acts as the component

integrating between the circadian clock and light sig-

nal, however, instead of activating the FT homolog

(Hd3a) under long days, Hd1 repress Hd3a under these

conditions [44,45].

Pollination

Following the transition to reproductive development,

the circadian clock continues to control physiological

events, such as pollination, that are important for suc-

cessful seed formation. Many plants rely on pollinators

that are active during a specific time of the day. In

some species, in order to maximize the possibility of

pollination and minimize the chances of damage, the

circadian system regulates flower opening so that it

occurs only during part of the day when potential poll-

inators are most active (Fig. 1G). Thus Arabidopsis

[46] petals open in the morning and close at midday,

whereas night-blooming cestrum (Cestrum nocturnum)

[47] petals open in the evening and close around dawn.

AB

C

F

M

N

G

H

I

J

K

L

D

E

Fig. 1. The circadian system has a regulatory role in nearly all aspects of a plant’s life. (A) Germination, (B) hypocotyl elongation, (C) leaf

movements, (D) circumnutations, (E) shade avoidance, (F) flowering time, (G) flower opening, (H) scent production, (I) tuberization, (J) winter

dormancy, (K) stomatal opening, (L) photosynthesis, (M) photoprotection, and (N) protection from temperature extremes.

E. Yakir et al. Circadian clock output in plants


Another important feature of the plant–pollinator

relationship is the plant’s signature scent, which is a

combination of volatile compounds unique for each

plant species. Some volatiles are regulated by the circa-

dian clock so that they are emitted in the correct phase

with the plant’s pollinator activity (Fig. 1H) [47]. For

example, in snapdragon (Antirrhinum majus) flowers

which are pollinated by bees, the emission of methyl

benzoate, myrcene and (E)-b-ocimene, is high during

the day [48,49]. By contrast, methyl benzoate, is emit-

ted at night by tobacco (Nicotiana suaveolens) and

petunia flowers (Petunia · hybrida) in order to attract

moths [49]. These rhythms are controlled by the clock

and are probably a result of circadian changes in

mRNA levels and enzyme activity in the biosynthesis

pathway and in the levels of available substrate [48–50].

Nectar secretion is a further factor affecting success-

ful pollination that may be timed to correspond with

pollinator activity. In some species of the family Com-

positae, nectar secretion is under diurnal control and

very possibly also under circadian control [51].

Other photoperiod-regulated processes

In addition to the transition from vegetative to repro-

ductive development, several other processes in the

plant’s life circle are controlled, at least in part, by

photoperiod and thus, probably, the circadian system.

One of these processes is the development of storage

organs (Fig. 1I). In many cultivars of potatoes, inclu-

ding Solanum tuberosum ssp. Andigena, tuberization

depends on photoperiod and there is evidence that a

potato ortholog of CONSTANS might be involved

[52]. Another photoperiod-controlled process is the

winter dormancy of temperate-zone woody plants

(Fig. 1J). In chestnut (Castanea sativa) trees LHY and

TOC1 orthologs might play a part in regulating the

dormant state [53], and in aspen (Populus tremula) and

black cottonwood (Populus trichocarpa) trees short-

day-induced dormancy is controlled by CO and FT

[54].

The role of the circadian system in the regulation

of cellular processes

Stomatal opening

Circadian regulation can also be seen at the level of a

single cell. One important example is the circadian

rhythm observed in stomatal (leaf pore) opening

(Fig. 1K). In Arabidopsis, stomatal conductance is

higher during the day than at night [55], whereas in

crassulacean acid metabolism3 plants, stomatal opening

has an opposite phase [56]. In addition the circadian

clock gates sensitivity of stomata to extracellular sig-

nals, such as light [57].

Photosynthesis and carbon dioxide fixation

Photosynthesis and carbon fixation are two of the

many important cellular processes that take place at a

specific time of day (Fig. 1L). The expression of many

Arabidopsis genes participating in the light-harvesting

reactions of photosynthesis is under clock control

[58,59]. Among them are the LHCA and LHCB gene

families, which encode chlorophyll a ⁄b binding poly-

peptides for photosystems I and II, as well as genes

that are involved in the biosynthesis of chlorophyll

and RUBISCO SMALL SUBUNIT (RBCS) and

RUBISCO ACTIVASE (RCA) that participate in car-

bon fixation [58,60]. It is not yet clear whether the

circadian expression of mRNA in these pathways is

always matched by circadian regulation at the level of

protein synthesis. However, in some cases protein lev-

els are under circadian control, for example, the syn-

thesis of LHCB and RCA in tomato is regulated by

the circadian system [61]. The rhythm of expression of

photosynthesis genes appears to be correlated with the

circadian rhythms observed in stomatal opening and

CO2 assimilation [62]. The circadian system also regu-

lates post-translational modification of photosynthetic

components such as phosphorylation of the D1 protein

in duckweed (Spirodela oligorrhiza) [63].

Beside genes that encode proteins with a role in pho-

tosynthesis reactions, some genes encode proteins that

are involved in photorespiration, and sugar metabo-

lism and transport are also under circadian control

[58,64,65]. Furthermore, it has been suggested that

there is a clock-controlled correlation between the

energy-producing process of photosynthesis and the

expression of genes involved in energy-consuming pro-

cesses such as nitrogen assimilation [58].

Stress responses

The circadian system appears to have a role in regula-

ting responses to both abiotic and biotic stresses. For

example, although plants need sun in order to pro-

duce energy, high light levels can also be very dam-

aging. Thus, before sunrise plants express genes

encoding enzymes in the biosynthesis of photoprotect-

ing pigments [58] and this expression is under

circadian regulation (Fig. 1M). Similarly, the mRNA

levels of some genes involved in cold protection are

highest at dusk (Fig. 1N) [58]. Furthermore, the up-

regulation by cold of some major genes is gated by

the circadian clock to a specific time during the day



[66], as is sensitivity of the plants themselves to high

and low temperatures. Thus cotton (Gossypium hirsu-

tum) is most sensitive to cold at the beginning of the

day and to high temperatures in the evening [67]. It

has been suggested that this circadian-controlled gat-

ing of the timing of sensitivity to extreme tempera-

tures might be a way for the plant to distinguish

between changes in temperatures during the course of

the day and seasonal changes in temperature. In addi-

tion, the circadian clock also regulates mRNA levels

of some pathogen-related genes in Arabidopsis [59]. As

an indication of the importance of the circadian sys-

tem in regulating stress responses, microarray experi-

ments have shown that around 70% of the known

clock-controlled genes may also be regulated by cold,

salt or drought stresses [68].

Mechanisms for regulating output

In contrast with mammals, which have a central pace-

maker in the brain to regulate the other oscillators in

the body, plant circadian clocks appear to be auto-

nomous. Thus, different plant organs can maintain

rhythmic expression of genes with different phases [69].

Futhermore, genes can cycle with varying periods in

different cells [70]. These differences in phase and per-

iod may be a result either of tissue-specific changes in

input pathways and ⁄or of modifications in the oscilla-

tor mechanism itself, although the available evidence

suggests that the basic oscillator mechanism is funda-

mentally conserved [70]. It seems unlikely, however,

that tissue-specific differences in the oscillator mechan-

ism are sufficient to regulate a wide range of output

processes with different phases.

In general, despite extensive evidence, gathered over

the years, that the circadian system has a regulatory

role in nearly all aspects of a plant’s life, remarkably

little is known about the actual mechanisms by which

the oscillator regulates these outputs. Indeed, one of

the most intriguing, but least understood, questions is

how the oscillator can regulate so many different plant

processes, including gene expression, with a wide vari-

ety of phases throughout the day.

Transcriptional control

Transcriptional control is probably one of the

most important levels of regulation for controlling

developmental, physiological and metabolic outputs.

Research in mice, Drosophila and Neurospora has

shown that a large percentage of the genome in a vari-

ety of organisms is under clock control [71–73]. An

extreme case of transcription clock control was found

in the cyanobacterium Synechococcus elongates

PCC 7942 which has most of its genome under clock

control [74]. A two-component signaling system seems

to be one of the mechanisms by which the cyanobacte-

rial clock regulates transcription [75,76].

In Arabidopsis as much as 36% of the genome is

controlled by the circadian system [58,59,77,78] and

because at least two components of the circadian oscil-

lator are transcription factors (CCA1 and LHY), an

appealing idea is that plant oscillator components

directly control the expression of some genes. Several

motifs have been identified in the promoters of circa-

dian-regulated genes and have been suggested as tar-

gets for binding by CCA1 and LHY. One such motif,

AAATATCT, also known as the Evening Element

(EE), is over-represented in the promoters of circadian

clock-controlled genes that show a peak of expression

in the evening [58,77,78]. In vitro assays show that

CCA1 and LHY can bind directly to the EE element

[2,6,79]. Moreover, an artificial promoter containing

four tandem repeats of the EE separated by 16 ran-

dom nucleotides confer evening-phased gene expression

to a luciferase reporter, confirming that the EE may be

sufficient to determine the phase of gene expression

[79]. Furthermore, mutations in the EE alter circadian

rhythms of gene expression, demonstrating that this

motif is necessary for evening phase of these genes

[2,58,80]. By contrast, many of the circadian-regulated

genes with an evening phase do not contain EEs in

their promoters, whereas EEs have been found in the

promoters of morning genes.

The EE differs in only one base pair from another

important circadian motif, the CCA1-binding site

(CBS) sequence, AAAAATCT. Wang et al. [81] first

characterized the CBS as the site for CCA1 binding in

CAB1 promoter. However, the CBS does not appear

to be over-represented in circadian gene promoters

[78]. Furthermore, there is contradictory evidence

regarding the role of the CBS in phase determination.

Harmer and Kay [79] found that changing the EE to a

CBS in a synthetic promoter based on the COLD

CIRCADIAN RHYTHM RNA BINDING 2 (CCR2)

promoter did not alter the peak expression phase of

the gene. By contrast, Michael and McClung [80]

showed that altering the EE motif in CATALASE 3

(CAT3)4 promoter to a CBS could change the peak

expression phase of the gene from evening to morning.

Together, the results from these two groups suggest

that other elements in CAT3 promoter are required for

phase determination and that the context of the motif

is important.

Clearly, therefore, the EE and CBS are insufficient

to explain circadian expression of all the clock-



controlled genes and combinations of known and

unknown motifs are necessary for the correct phasing

of circadian genes. Recently, Harmer and Kay [79]

have identified a morning element (AACCACGA

AAAT) sequence that might have a role in determining

circadian expression and phase by binding of a yet

unknown transcription activator. Other motifs might

include the light-activation sequence G-box (CAC

GTG) and the related Hex element, but these have not

yet been tested experimentally [77,78,82].

Post-transcriptional control

The oscillator also regulates post-transcriptional con-

trol. For example, CCR2 mRNA accumulation is a

result of both transcriptional and post-transcriptional

regulation. CCR2 regulates the splicing of its own

transcript and that of the closely related COLD CIR-

CADIAN RHYTHM RNA BINDING 1 (CCR1), thus

circadian-regulated changes in the levels of CCR2 pro-

tein affect CCR1 and CCR2 mRNA accumulation [83–

86]. Another example is circadian control of the half-

life of some transcripts. CCR-LIKE5 (CCL) and

SENESCENCE ASSOCIATED GENE 1 (SEN1) have

a longer half-life in the morning than in the afternoon

even under conditions of constant light and tempera-

ture [87]. CCL and SEN1 have in their 3¢-UTRs a

downstream element (DST) that can mediate transcript

stability [88]. Furthermore, CCL and SEN1 mRNA

decay is altered in a mutant that affects the DST decay

pathway [87]. Thus, DST may be involved in circadian

regulation of transcript stability.

Included in the cohort of plant genes controlled by

the circadian system are many genes that encode regu-

latory proteins such as kinases and phosphatases.

These proteins may act as secondary regulators of cir-

cadian output pathways. For example, the circadian

system controls expression of the gene encoding phos-

phoenolpyruvate carboxylase kinase that regulates

phosophorylation of phosphoenolpyruvate carboxylase

to catalyse fixation of CO2 in crassulacean acid meta-

bolism plants [89].

The role of hormones in regulating circadian

output

Hormones affect most of the known circadian-con-

trolled processes in plants and it is likely that, at least

in some cases, the clock operates through changes in

hormone levels or hormone perception. However, to

date, there is only limited evidence for the role of

hormones in delivering information from the clock to

output processes.

In many plant species, including Arabidopsis, barley

(Hordeum distychum), wheat (Triticum aestivum), rye

(Secale cereale), red goosefoot and cotton, ethylene

production is under circadian control [90,91]. In Ara-

bidopsis, ethylene levels peak in the middle of the sub-

jective day. This pattern of ethylene accumulation is

correlated with the circadian regulation of expression

of ACC SYNTHASE which encodes the enzyme

responsible for the synthesis of the ethylene precursor,

1-amino-cyclopropane-1-carboxilic acid. The fact that

ethylene production is regulated by the circadian oscil-

lator might suggest that ethylene has a role in regula-

ting output processes. However, mutant plants that are

affected in ethylene biosynthesis and signaling show no

differences in rhythmic hypocotyl elongation or leaf

movement, two rhythmic growth processes that circa-

dian-controlled oscillations of ethylene might be expec-

ted to regulate [92]. Thus the biological significance of

rhythmic ethylene production is still unclear.

Greater success has been achieved in connecting

auxin to circadian regulation of growth. The levels of

free indole-3-acetic acid (IAA) and its conjugated form,

IAA–aspartate, were shown to cycle in continuous light

both in floral stems and in rosette leaves of Arabidopsis

[93]. There is also a circadian control of the expression

of genes involved in auxin transport and auxin

response [58,59]. More interestingly, the abolition of

rhythmic stem elongation following removal of the

floral stem, the endogenous source of auxin, can be res-

cued by the application of exogenous auxin [93].

The relationship between the circadian clock and

gibberellins (GAs) is more complicated. Both the

clock, via the photoperiod pathway, and GAs affect

flowering time in Arabidopsis, but most evidence

reveals genetic differences between the photoperiod

pathway and the GA pathway [94]. However in other

plants, such as darnel ryegrass (Lolium temulentum),

GAs may have a role in regulating photoperiodic

flowering [95–98]. Thus, it is possible that GAs have a

role in regulating circadian output.

There is some circumstantial evidence that other

hormones may be involved in regulating circadian out-

put. In carrot (Daucus carota), the levels of cytokinins

(CKs) are under circadian control [99]. While in

tobacco, CKs, as well as IAA and abscisic acid, are

rhythmic under diurnal condition [100]. It has been

suggested that CKs may also be a part of an input

pathway to the Arabidopsis clock [101,102].

The role of calcium in regulating circadian output

Calcium (Ca2+) is a second messenger in many differ-

ent processes in the plant cell and there is evidence



that it may play this role in the regulation of output

pathways from the circadian clock. Consistent with a

potential role in regulating circadian output, circadian

oscillations in free Ca2+ have been demonstrated in

the cytosol and chloroplast of tobacco (Nicotiana

plumbaginifolia) and in the cytosol of Arabidopsis

[103,104]. However, there are differences in the circa-

dian oscillations of Ca2+; cytosolic oscillations of

Ca2+ continue in constant light, whereas chloroplastic

oscillations of Ca2+ continue only in constant dark

[103]. Furthermore, circadian oscillations of cytosolic

Ca2+ in tobacco seedlings have different phases in dif-

ferent tissues and in Arabidopsis the phase of circadian

oscillations of cytosolic Ca2+ is modulated by the

entraining photoperiod [104,105]. These results may

reflect a possible role for calcium in mediating different

clock controlled processes, including photoperiodism, in

different cells. Finally there is evidence that Ca2+ has

a role in the circadian regulation of leaf movement in

legumes, and in stomatal opening and photoperiod-

controlled flowering in morning glory (Pharbitis nil)

[35,106]. Together these results strongly suggest that

Ca2+ is part of the output signaling from the clock.

As yet, however, no molecular decoders of the circa-

dian Ca2+ oscillations, such as calcium-binding pro-

teins, have been experimentally proven in plants

although a number of potential Ca2+ decoders have

been identified [106].

Conclusions

The circadian system clearly plays an extremely

important role in the life of plants, and indeed other

organisms. However, despite this significance, and in

spite of the considerable advances in our understand-

ing of how the oscillator and input pathways func-

tion, there is still much we do not understand of how

the circadian system is able to accurately regulate so

many output processes. Deciphering the mechanisms

by which these output processes are controlled may

allow us to modify specific pathways that are regula-

ted by the circadian system. It will also give us a bet-

ter understanding of this important aspect of the lives

of plants.

Acknowledgements

The authors would like to thank Miri Hassidim, Shai

Yerushalmi, Ido Kron and David Greenberg for their

critical reading of the manuscript. Our apologies to the

many researchers whose work was not cited due to

limitation of space. This work was supported by ISF

grants (0397232 and 0397386).

References

1 Young MW & Kay SA (2001) Time zones: a compara-

tive genetics of circadian clocks. Nat Rev Genet 2, 702–

715.

2 Alabadi D, Oyama T, Yanovsky MJ, Harmon FG,

Mas P & Kay SA (2001) Reciprocal regulation

between TOC1 and LHY ⁄CCA1 within the Arabidopsis

circadian clock. Science 293, 880–883.

3 Sugano S, Andronis C, Green RM, Wang Z-Y &

Tobin EM (1998) Protein kinase CK2 interacts with

and phosphorylates the Arabidopsis circadian clock-

associated 1 protein. Proc Natl Acad Sci USA 95,

11020–11025.

4 Sugano S, Andronis C, Ong MS, Green RM & Tobin

EM (1999) The protein kinase CK2 is involved in regu-

lation of circadian rhythms in Arabidopsis. Proc Natl

Acad Sci USA 96, 12362–12366.

5 Doyle MR, Davis SJ, Bastow RM, McWatters HG,

Kozma-Bognar L, Nagy F, Millar AJ & Amasino RM

(2002) The ELF4 gene controls circadian rhythms and

flowering time in Arabidopsis thaliana. Nature 419,

74–77.

6 Hazen SP, Schultz TF, Pruneda-Paz JL, Borevitz JO,

Ecker JR & Kay SA (2005) LUX ARRHYTHMO

encodes a Myb domain protein essential for circadian

rhythms. Proc Natl Acad Sci USA 102, 10387–

10392.

7 Kikis EA, Khanna R & Quail PH (2005) ELF4 is a

phytochrome-regulated component of a negative-feed-

back loop involving the central oscillator components

CCA1 and LHY. Plant J 44, 300–313.

8 Mizoguchi T, Wright L, Fujiwara S, Cremer F, Lee K,

Onouchi H, Mouradov A, Fowler S, Kamada H,

Putterill J et al. (2005) Distinct roles of GIGANTEA

in promoting flowering and regulating circadian

rhythms in Arabidopsis. Plant Cell 17, 2255–2270.

9 Paltiel J, Amin R, Gover A, Ori N & Samach A

(2006) Novel roles for GIGANTEA revealed under

environmental conditions that modify its expression in

Arabidopsis and Medicago truncatula. Planta 224,

1255–1268.6

10 Locke JC, Millar AJ & Turner MS (2005) Modelling

genetic networks with noisy and varied

experimental data: the circadian clock in Arabidopsis

thaliana. J Theoret Biol 234, 383–393.

11 Edwards KD, Lynn JR, Gyula P, Nagy F & Millar AJ

(2005) Natural allelic variation in the temperature-

compensation mechanisms of the Arabidopsis thaliana

circadian clock. Genetics 170, 387–400.

12 Gould PD, Locke JC, Larue C, Southern MM, Davis

SJ, Hanano S, Moyle R, Milich R, Putterill J, Millar

AJ et al. (2006) The molecular basis of temperature

compensation in the Arabidopsis circadian clock. Plant

Cell 18, 1177–1187.



13 Salom AP & McClung CR (2005) What makes the

Arabidopsis clock tick on time? A review on entrain-

ment. Plant, Cell Environ 28, 21–38.

14 Nelson DC, Lasswell J, Rogg LE, Cohen MA & Bartel

B (2000) FKF1, a clock-controlled gene that regulates

the transition to flowering in Arabidopsis. Cell 101,

331–340.

15 Schultz TF, Kiyosue T, Yanovsky M, Wada M & Kay

SA (2001) A role for LKP2 in the circadian clock of

Arabidopsis. Plant Cell 13, 2659–2670.

16 Somers DE, Schultz TF, Milnamow M & Kay SA

(2000) ZEITLUPE encodes a novel clock-associated

PAS protein from Arabidopsis. Cell 101, 319–329.

17 Devlin PF & Kay SA (2001) Circadian photopercep-

tion. Annu Rev Physiol 63, 677–694.

18 Imaizumi T, Tran HG, Swartz TE, Briggs WR & Kay

SA (2003) FKF1 is essential for photoperiodic-specific

light signalling in Arabidopsis. Nature 426, 302–306.

19 Hall A, Bastow RM, Davis SJ, Hanano S, McWatters

HG, Hibberd V, Doyle MR, Sung S, Halliday KJ,

Amasino RM et al. (2003) The TIME FOR COFFEE

gene maintains the amplitude and timing of Arabidop-

sis circadian clocks. Plant Cell 15, 2719–2729.

20 McWatters HG, Bastow RM, Hall A & Millar AJ

(2000) The ELF3 zeitnehmer regulates light signalling

to the circadian clock. Nature 408, 716–720.

21 Farre EM, Harmer SL, Harmon FG, Yanovsky MJ &

Kay SA (2005) Overlapping and distinct roles of PRR7

and PRR9 in the Arabidopsis circadian clock. Curr Biol

15, 47–54.

22 Yamamoto Y, Sato E, Shimizu T, Nakamich N, Sato

S, Kato T, Tabata S, Nagatani A, Yamashino T &

Mizuno T (2003) Comparative genetic studies on the

APRR5 and APRR7 genes belonging to the APRR1 ⁄TOC1 quintet implicated in circadian rhythm, control

of flowering time, and early photomorphogenesis.

Plant Cell Physiol 44, 1119–1130.

23 Gardner MJ, Hubbard KE, Hotta CT, Dodd AN &

Webb AAR (2006) How plants tell the time. Biochem

J 397, 15–24.

24 McClung CR (2006) Plant circadian rhythms. Plant

Cell 18, 792–803.

25 Baskin JM & Baskin CC (1976) Effect of photoperiod

on germination of Cyperus inflexus seeds. Bot Gaz 137,

269–273.

26 Black M & Wareing PF (1954) Photoperiodic control

of germination in seed of birch (Betula pubescens

Ehrh.). Nature 174, 705–706.

27 Black M & Wareing PF (1955) Growth studies in

woody species VII. Photoperiodic control of germina-

tion in Betula pudescens Ehrh. Physiologia Plantarum

8, 300–316.

28 Densmore RV (1997) Effect of day length on germina-

tion of seeds collected in Alaska. Am J Bot 84, 274–

278.

29 Zhong HH, Painter JE, Salome PA, Straume M &

McClung CR (1998) Imbibition, but not release from

stratification, sets the circadian clock in Arabidopsis

seedlings. Plant Cell 10, 2005–2018.

30 Bryant TR (1972) Gas exchange in dry seeds: circadian

rhythmicity in the absence of DNA replication, tran-

scription, and translation. Science 178, 634–636.

31 Dowson-Day MJ & Millar AJ (1999) Circadian dys-

function causes aberrant hypocotyl elongation patterns

in Arabidopsis. Plant J 17, 63–71.

32 Fernandez SR & Wagner E (1994) New method of

measurement and analysis of the stem extension

growth rate to demonstrate complete synchronisation

of Chenopodium rubrum plants by environmental con-

ditions. J Plant Physiol 144, 362–369.

33 Lecharny A & Wagner E (1984) Stem extension rate in

light-grown plants. Evidence for an endogenous circa-

dian rhythm in Chenopodium rubrum. Physiologia Plan-

tarum 60, 437–443.

34 Tukey HB & Ketellapper HJ Jr (1963) Length of the

light–dark cycle and plant growth. Am J Bot 50, 110–

115.

35 Webb AAR (2003) The physiology of circadian

rhythms in plants. New Phytologist 160, 281–303.

36 Niinuma K, Someya N, Kimura M, Yamaguchi I &

Hamamoto H (2005) Circadian rhythm of circumnuta-

tion in inflorescence stems of Arabidopsis. Plant Cell

Physiol 46, 1423–1427.

37 Salter MG, Franklin KA & Whitelam GC (2003) Gat-

ing of the rapid shade-avoidance response by the circa-

dian clock in plants. Nature 426, 680–683.

38 Bunning E (1936) Die endogene tagesrhythmik als

grundlage der photoperiodischen reaktion. Ber Dtsch

Bot Ges 54, 590–607.

39 Searle I & Coupland G (2004) Induction of flowering

by seasonal changes in photoperiod. EMBO J 23,

1217–1222.

40 Suarez-Lopez P, Wheatley K, Robson F, Onouchi H,

Valverde F & Coupland G (2001) CONSTANS med-

iates between the circadian clock and the control of

flowering in Arabidopsis. Nature 410, 1116–1120.

41 Valverde F, Mouradov A, Soppe W, Ravenscroft D,

Samach A & Coupland G (2004) Photoreceptor regula-

tion of CONSTANS protein in photoperiodic flower-

ing. Science 303, 1003–1006.

42 Samach A, Onouchi H, Gold SE, Ditta GS, Schwarz-

Sommer Z, Yanofsky MF & Coupland G (2000) Dis-

tinct roles of CONSTANS target genes in reproductive

development of Arabidopsis. Science 288, 1613–1616.

43 Huang T, Bohlenius H, Eriksson S, Parcy F &

Nilsson O (2005) The mRNA of the Arabidopsis gene

FT moves from leaf to shoot apex and induces flower-

ing. Science 309, 1694–1696.

44 Hayama R, Yokoi S, Tamaki S, Yano M & Shima-

moto K (2003) Adaptation of photoperiodic control



pathways produces short-day flowering in rice. Nature

422, 719–722.

45 Kojima S, Takahashi Y, Kobayashi Y, Monna L,

Sasaki T, Araki T & Yano M (2002) Hd3a, a rice

ortholog of the Arabidopsis FT gene, promotes transi-

tion to flowering downstream of Hd1 under short-day

conditions. Plant Cell Physiol 43, 1096–1105.

46 van Doorn WG & van Meeteren U (2003) Flower open-

ing and closure: a review. J Exp Bot 54, 1801–1812.

47 Overland L (1960) Endogenous rhythm in opening and

odor of flowers of Cestrum nocturnm. Am J Bot 47,

378–382.

48 Dudareva N, Martin D, Kish CM, Kolosova N,

Gorenstein N, Faldt J, Miller B & Bohlmann J (2003)

(E)-a-Ocimene and myrcene synthase genes of floral

scent biosynthesis in snapdragon: function and expres-

sion of three terpene synthase genes of a new terpene

synthase subfamily. Plant Cell 15, 1227–1241.

49 Kolosova N, Gorenstein N, Kish CM & Dudareva N

(2001) Regulation of circadian methyl benzoate emis-

sion in diurnally and nocturnally emitting plants. Plant

Cell 13, 2333–2347.

50 Verdonk JC, Ric de Vos CH, Verhoeven HA, Haring

MA, van Tunen AJ & Schuurink RC (2003) Regula-

tion of floral scent production in petunia revealed by

targeted metabolomics. Phytochemistry 62, 997–1008.

51 Pesti J (1976) Daily fluctuations in the sugar content of

nectar and periodicity of secretion in the Compositae.

Acta Agron Acad Sci Hung 25, 5–17.

52 Martinez-Garcia JF, Virgos-Soler A & Prat S (2002)

Control of photoperiod-regulated tuberization in

potato by the Arabidopsis flowering-time gene CON-

STANS. Proc Natl Acad Sci USA 99, 15211–15216.

53 Ramos A, Perez-Solis E, Ibanez C, Casado R, Collada

C, Gomez L, Aragoncillo C & Allona I (2005) Winter

disruption of the circadian clock in chestnut. Proc Natl

Acad Sci USA 102, 7037–7042.

54 Bohlenius H, Huang T, Charbonnel-Campaa L, Brun-

ner AM, Jansson S, Strauss SH & Nilsson O (2006)

CO ⁄FT regulatory module controls timing of flowering

and seasonal growth cessation in trees. Science 312,

1040–1043.

55 Somers DE, Webb AAR, Pearson M & Kay SA (1998)

The short-period mutant, toc1-1, alters circadian clock

regulation of multiple outputs throughout development

in Arabidopsis thaliana. Development 125, 485–494.

56 Thimann KV, Tan Z-Y & Park J (1992) Cycling of

stomatal aperture in leaves of plants with crassulacean

acid metabolism under constant conditions. Am J Bot

79, 23–27.

57 Gorton HL, Williams WE & Assmann SM (1993) Cir-

cadian rhythms in stomatal responsiveness to red and

blue light. Plant Physiol 103, 399–406.

58 Harmer SL, Hogenesch JB, Straume M, Chang H-S,

Han B, Zhu T, Wang X, Kreps JA & Kay SA (2000)

Orchestrated transcription of key pathways in Arabi-

dopsis by the circadian clock. Science 290, 2110–2113.

59 Schaffer R, Landgraf J, Accerbi M, Simon V, Larson

M & Wisman E (2001) Microarray analysis of diurnal

and circadian-regulated genes in Arabidopsis. Plant Cell

13, 113–123.

60 Pilgrim ML & McClung CR (1993) Differential invol-

vement of the circadian clock in the expression of

genes required for ribulose-1,5-bisphosphate

carboxylase ⁄ oxygenase synthesis, assembly, and activa-

tion in Arabidopsis thaliana. Plant Physiol 103, 553–

564.

61 Martino-Catt S & Ort DR (1992) Low temperature

interrupts circadian regulation of transcriptional activ-

ity in chilling-sensitive plants. Proc Natl Acad Sci USA

89, 3731–3735.

62 Salome PA, Michael TP, Kearns EV, Fett-Neto AG,

Sharrock RA & McClung CR (2002) The out of phase

1 mutant defines a role for PHYB in circadian phase

control in Arabidopsis. Plant Physiol 129, 1674–1685.

63 Booij-James IS, Swegle WM, Edelman M & Mattoo

AK (2002) Phosphorylation of the D1 photosystem II

reaction center protein is controlled by an endogenous

circadian rhythm. Plant Physiol 130, 2069–2075.

64 Lu Y, Gehan JP & Sharkey TD (2005) Daylength and

circadian effects on starch degradation and maltose

metabolism. Plant Physiol 138, 2280–2291.

65 McClung CR, Hsu M, Painter JE, Gagne JM, Karls-

berg SD & Salome PA (2000) Integrated temporal reg-

ulation of the photorespiratory pathway. Circadian

regulation of two Arabidopsis genes encoding serine

hydroxymethyltransferase. Plant Physiol 123, 381–392.

66 Fowler SG, Cook D & Thomashow MF (2005) Low

temperature induction of Arabidopsis CBF1, 2, and 3 is

gated by the circadian clock. Plant Physiol 137, 961–

968.

67 Rikin A, Dillwith JW & Bergman DK (1993) Correla-

tion between the circadian rhythm of resistance to

extreme temperatures and changes in fatty acid compo-

sition in cotton seedlings. Plant Physiol 101, 31–36.

68 Kreps JA, Wu Y, Chang H-S, Zhu T, Wang X & Har-

per JF (2002) Transcriptome changes for Arabidopsis

in response to salt, osmotic, and cold stress. Plant

Physiol 130, 2129–2141.

69 Thain SC, Hall A & Millar AJ (2000) Functional inde-

pendence of circadian clocks that regulate plant gene

expression. Curr Biol 10, 951–956.

70 Thain SC, Murtas G, Lynn JR, McGrath RB & Millar

AJ (2002) The circadian clock that controls gene

expression in Arabidopsis is tissue specific. Plant Phy-

siol 130, 102–110.

71 Ceriani MF, Hogenesch JB, Yanovsky M, Panda S,

Straume M & Kay SA (2002) Genome-wide expression

analysis in Drosophila reveals genes controlling circa-

dian behavior. J Neurosci 22, 9305–9319.



72 Nowrousian M, Duffield GE, Loros JJ & Dunlap JC

(2003) The frequency gene is required for temperature-

dependent regulation of many clock-controlled genes

in Neurospora crassa. Genetics 164, 923–933.

73 Panda S, Antoch MP, Miller BH, Su AI, Schook AB,

Straume M, Schultz PG, Kay SA, Takahashi JS &

Hogenesch JB (2002) Coordinated Transcription of key

pathways in the mouse by the circadian clock. Cell

109, 307–320.

74 Liu Y, Tsinoremas NF, Johnson CH, Lebedeva NV,

Golden SS, Ishiura M & Kondo T (1995) Circadian

orchestration of gene expression in cyanobacteria.

Genes Dev 9, 1469–1478.

75 McClung CR (2006) Two-component signaling pro-

vides the major output from the cyanobacterial circa-

dian clock. Proc Natl Acad Sci USA 103, 11819–11820.

76 Takai N, Nakajima M, Oyama T, Kito R, Sugita C,

Sugita M, Kondo T & Iwasaki H (2006) A KaiC-asso-

ciating SasA–RpaA two-component regulatory system

as a major circadian timing mediator in cyanobacteria.

Proc Natl Acad Sci USA 103, 12109–12114.

77 Edwards KD, Anderson PE, Hall A, Salathia NS,

Locke JCW, Lynn JR, Straume M, Smith JQ &

Millar AJ (2006) FLOWERING LOCUS C mediates

natural variation in the high-temperature response of

the Arabidopsis circadian clock. Plant Cell 18, 639–

650.

78 Michael TP & McClung CR (2003) Enhancer trapping

reveals widespread circadian clock transcriptional con-

trol in Arabidopsis. Plant Physiol 132, 629–639.

79 Harmer SL & Kay SA (2005) Positive and negative

factors confer phase-specific circadian regulation of

transcription in Arabidopsis. Plant Cell 17, 1926–1940.

80 Michael TP & McClung CR (2002) Phase-specific cir-

cadian clock regulatory elements in Arabidopsis. Plant

Physiol 130, 627–638.

81 Wang ZY, Kenigsbuch D, Sun L, Harel E, Ong MS &

Tobin EM (1997) A Myb-related transcription factor is

involved in the phytochrome regulation of an Arabi-

dopsis Lhcb gene. Plant Cell 9, 491–507.

82 Hudson ME & Quail PH (2003) Identification of pro-

moter motifs involved in the network of phytochrome

A-regulated gene expression by combined analysis of

genomic sequence and microarray data. Plant Physiol

133, 1605–1616.

83 Heintzen C, Nater M, Apel K & Staiger D (1997)

AtGRP7, a nuclear RNA-binding protein as a compo-

nent of a circadian-regulated negative feedback loop in

Arabidopsis thaliana. Proc Natl Acad Sci USA 94,

8515–8520.

84 Schoning JC & Staiger D (2005) At the pulse of time:

protein interactions determine the pace of circadian

clocks. FEBS Lett 579, 3246–3252.

85 Staiger D, Apel K & Trepp G (1999) The Atger3 pro-

moter confers circadian clock-regulated transcription

with peak expression at the beginning of the night.

Plant Mol Biol 40, 873–882.

86 Staiger D, Zecca L, Kirk DAW, Apel K & Eckstein L

(2003) The circadian clock regulated RNA-binding

protein AtGRP7 autoregulates its expression by influ-

encing alternative splicing of its own pre-mRNA. Plant

J 33, 361–371.

87 Lidder P, Gutierrez RA, Salome PA, McClung CR &

Green PJ (2005) Circadian control of messenger RNA

stability. Association with a sequence-specific messenger

RNA decay pathway. Plant Physiol 138, 2374–2385.

88 Newman TC, Ohme-Takagi M, Taylor CB & Green PJ

(1993) DST sequences, highly conserved among plant

SAUR genes, target reporter transcripts for rapid

decay in tobacco. Plant Cell 5, 701–714.

89 Hartwell J, Gill A, Nimmo GA, Wilkins MB, Jenkins

GI & Nimmo HG (1999) Phosphoenolpyruvate car-

boxylase kinase is a novel protein kinase regulated at

the level of expression. Plant J 20, 333–342.

90 Jasoni RL, Cothren T, Morgan PW & Sohan DE

(2004) Circadian ethylene production in cotton. Plant

Growth Regulation 36, 127–133.

91 McClung CR (2000) Circadian rhythms in plants: a

millennial view. Physiologia Plantarum 109, 359–371.

92 Thain SC, Vandenbussche F, Laarhoven LJJ, Dowson-

Day MJ, Wang Z-Y, Tobin EM, Harren FJM, Millar

AJ & Van Der Straeten D (2004) Circadian rhythms of

ethylene emission in Arabidopsis. Plant Physiol 136,

3751–3761.

93 Jouve L, Gaspar T, Kevers C, Greppin H & Degli

Agosti R (1999) Involvement of indole-3-acetic acid in

the circadian growth of the first internode of Arabidop-

sis. Planta 209, 136–142.

94 Boss PK, Bastow RM, Mylne JS & Dean C (2004)

Multiple pathways in the decision to flower: enabling,

promoting, and resetting. Plant Cell 16, S18–S31.

95 King RW & Evans LT (2003) GIBBERELLINS and

FLOWERING OF GRASSES and CEREALS: prizing

open the lid of the ‘florigen’ black box. Annu Rev Plant

Biol 54, 307–328.

96 King RW, Evans LT, Mander LN, Moritz T, Pharis R

& Twitchin B (2003) Synthesis of gibberellin GA6 and

its role in flowering of Lolium temulentum. Phytochem-

istry 62, 77–82.

97 King RW, Moritz T, Evans LT, Martin J, Andersen

CH, Blundell C, Kardailsky I & Chandler PM (2006)

Regulation of flowering in the long-day grass Lolium

temulentum by gibberellins and the FLOWERING

LOCUS T cene. Plant Physiol 141, 498–507.

98 MacMillan CP, Blundell CA & King RW (2005) Flow-

ering of the grass Lolium perenne. Effects of vernaliza-

tion and long days on gibberellin biosynthesis and

signaling. Plant Physiol 138, 1794–1806.

99 Stiebeling B & Neumann K-H (1986) Identification

and concentation of endogenous cytokinins in carrots



(Daucus carota L.) as influenced by development and a

circadian rhythm. J Plant Physiol 127, 111–121.

100 Novakova M, Motyka V, Dobrev PI, Malbeck J,

Gaudinova A & Vankova R (2005) Diurnal variation

of cytokinin, auxin and abscisic acid levels in tobacco

leaves. J Exp Bot 56, 2877–2883.

101 Salome PA, To JPC, Kieber JJ & McClung CR (2006)

Arabidopsis response regulators ARR3 and ARR4 play

cytokinin-independent roles in the control of circadian

period. Plant Cell 18, 55–69.

102 Zheng B, Deng Y, Mu J, Ji Z, Xiang T, Niu Q-W,

Chua N-H & Zuo J (2006) Cytokinin affects circadian-

clock oscillation in a phytochrome B- and Arabidopsis

response regulator 4-dependent manner. Physiologia

Plantarum 127, 277–292.

103 Johnson CH, Knight MR, Kondo T, Masson P, Sed-

brook J, Haley A & Trewavas A (1995) Circadian

oscillations of cytosolic and chloroplastic free calcium

in plants. Science 269, 1863–1865.

104 Wood NT, Haley A, Viry-Moussaid M, Johnson CH,

van der Luit AH & Trewavas AJ (2001) The calcium

rhythms of different cell types oscillate with different

circadian phases. Plant Physiol 125, 787–796.

105 Love J, Dodd AN & Webb AAR (2004) Circadian and

diurnal calcium oscillations encode photoperiodic

information in Arabidopsis. Plant Cell 16, 956–966.

106 Dodd AN, Love J & Webb AAR (2005) The plant

clock shows its metal: circadian regulation of cytosolic

free Ca2+. Trends Plant Sci 10, 15–21.



Regulation of output from the plant circadian clock

Documents

Transcript of Regulation of output from the plant circadian clock