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Plant Cell Monogr (9) D.P.S. Verma and Z. Hong: Cell Division Control in Plants DOI 10.1007/7089_2007_119/Published online: 11 July 2007 © Springer-Verlag Berlin Heidelberg 2007 Circadian Regulation of Cell Division François-Yves Bouget () · Mickael Moulager · Florence Corellou UMR 7628 CNRS, Université Paris VI, Laboratoire Arago, Modèles en Biologie Cellulaire et Evolutive, BP44, 66651 Banyuls sur Mer, France [email protected] Abstract Plants are photosynthetic organisms, which use light, as main source of energy, for growth and development. Because sun-light is also mutagenic, many organisms, from most kingdoms, have evolved an internal time-tracking system, so-called the circadian, which restricts cell division to specific times of the day in when DNA is less exposed to UV damage (“escape from mutagenic light” theory). While the circadian regulation of cell division has been extensively characterized in animals and unicellular green algae, little is known about the photoperiodic regulation of cell division in land plants. Recent findings about the possible links between cell division, the circadian clock and the DNA damage checkpoint are discussed. 1 Introduction Biological clocks are pacemakers, which play an essential role in regulating the physiology and behavior of living organisms. Such clocks are the cell di- vision cycle (CDC) and the circadian clock, which coexist in many cells from organisms including plants, animals, fungi and cyanobacteria (Bell-Pedersen et al. 2005; McClung 2006; Naef 2005). Each day, living organisms are exposed to changes in light (photoperiod) and temperature due to the rotation of the earth. Furthermore the relative day to night lengths vary along the year. The circadian clock is an autonomous system, which gives the time and can be entrained by light or temperature cycles. This clock allows the organism to adapt to the predictable daily environmental changes by anticipating them. The first evidence of a circadian clock was first demonstrated in 1729 by de Mairan, who showed that a heliotrop plant still exhibits robust rhythms of leaf movement when placed in constant darkness. Since then, the circadian clock was shown to regulate a wide array of plant physiology processes including photosynthesis, metabolism, and at the molecular level, a significant propor- tion of gene expression (Gardner et al. 2006). The circadian clock is likely to confer an adaptive advantage to multicellular organisms since it is found in all kingdoms including animals, plants and fungi. Among unicellular free- living organisms circadian rhythms have been described almost exclusively in photosynthetic ones.

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Page 1: [Plant Cell Monographs] Cell Division Control in Plants Volume 9 || Circadian Regulation of Cell Division

Plant Cell Monogr (9)D.P.S. Verma and Z. Hong: Cell Division Control in PlantsDOI 10.1007/7089_2007_119/Published online: 11 July 2007© Springer-Verlag Berlin Heidelberg 2007

Circadian Regulation of Cell Division

François-Yves Bouget (�) · Mickael Moulager · Florence Corellou

UMR 7628 CNRS, Université Paris VI, Laboratoire Arago,Modèles en Biologie Cellulaire et Evolutive, BP44, 66651 Banyuls sur Mer, [email protected]

Abstract Plants are photosynthetic organisms, which use light, as main source of energy,for growth and development. Because sun-light is also mutagenic, many organisms, frommost kingdoms, have evolved an internal time-tracking system, so-called the circadian,which restricts cell division to specific times of the day in when DNA is less exposed toUV damage (“escape from mutagenic light” theory). While the circadian regulation of celldivision has been extensively characterized in animals and unicellular green algae, little isknown about the photoperiodic regulation of cell division in land plants. Recent findingsabout the possible links between cell division, the circadian clock and the DNA damagecheckpoint are discussed.

1Introduction

Biological clocks are pacemakers, which play an essential role in regulatingthe physiology and behavior of living organisms. Such clocks are the cell di-vision cycle (CDC) and the circadian clock, which coexist in many cells fromorganisms including plants, animals, fungi and cyanobacteria (Bell-Pedersenet al. 2005; McClung 2006; Naef 2005). Each day, living organisms are exposedto changes in light (photoperiod) and temperature due to the rotation of theearth. Furthermore the relative day to night lengths vary along the year. Thecircadian clock is an autonomous system, which gives the time and can beentrained by light or temperature cycles. This clock allows the organism toadapt to the predictable daily environmental changes by anticipating them.The first evidence of a circadian clock was first demonstrated in 1729 by deMairan, who showed that a heliotrop plant still exhibits robust rhythms of leafmovement when placed in constant darkness. Since then, the circadian clockwas shown to regulate a wide array of plant physiology processes includingphotosynthesis, metabolism, and at the molecular level, a significant propor-tion of gene expression (Gardner et al. 2006). The circadian clock is likelyto confer an adaptive advantage to multicellular organisms since it is foundin all kingdoms including animals, plants and fungi. Among unicellular free-living organisms circadian rhythms have been described almost exclusively inphotosynthetic ones.

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Cells often divide with a period of 24 hours, leading sometimes to a con-fusion between the circadian clock and the CDC. The rhythmicity of celldivision has been known for a long time in unicellular algae such as theflagellate Euglena (Edmunds et al. 1982), the green alga Chlamydomonas(Bruce 1972; Goto and Johnson 1995) or the marine dinoflagellate Gonyaulax(Sweeney 1958). These cells usually divide once per day or with a multiple of24 hours. However, when they are allowed to divide more than once per day,the rhythmicity of cell division is lost in Euglena or in Gonyaulax. It was con-cluded, according to the “circadian/infradian” rule that circadian rhythms ofdivision exist only in cells dividing in a circadian or infradian way, that is,once per day or less. According to this rule, both the circadian clock and theCDC are tightly interconnected and cell division might even be controlled byan autonomous clock that is completely independent of a circadian clock. Ex-periments in the prokaryotic cyanobacteria Synechococcus contradicted thisrule, since cells dividing more than once per day still exhibit robust circadianrhythms of cell division and gene expression (Kondo et al. 1997).

Plants are photosynthetic organisms, which heavily rely on light as a sourceof energy and it is sometime difficult to discriminate between the effect of lightas a signal through activating specific signalization pathways and as a source ofenergy that is a required for a cell to grow and divide when it reaches a criticalsize. The molecular basis of both the cell cycle core machinery (Inze 2005) andthe circadian clock are well understood in plants (McClung 2006). However,neither a direct regulation of cell division by light nor a circadian regulationof the CDC have been demonstrated in higher plants. Recent results from ourgroup, using the firefly luciferase reporter protein fused to Arabidopsis spe-cific promoters indicate that the expression of cell cycle regulated genes suchas histone H4 and of central CDC genes such as cyclinB occurs at the end ofthe day and is under circadian control in the Arabidopsis shoot apical meris-tem (unpublished data). However, direct studies of the CDC remain difficultto perform in planta because only a limited number of cells divide in grow-ing plants and cell division is restricted to meristems. Cell division studiesare much easier to perform in unicellular organisms, such as unicellular algae,which can be naturally synchronized by the light/dark cycle. Circadian regu-lation of cell division has been known for over 30 years in green algae such asChlorophyta chlamydomonas. Chlorophyta belong to the green lineage and area sister group to Streptophyta which encompasses higher plants.

Recently, several important findings have started to unravel the molecularbasis of circadian regulation of cell division in animals (Fu et al. 2002; Matsuoet al. 2003). In this review we will first focus on the circadian regulation of celldivision in unicellular photosynthetic eukaryotes, especially those evolution-arily related to higher plants, that is green algae. We will also summarize theactual knowledge of molecular basis of circadian regulation of the CDC basedon recent work in animals. Finally, we will speculate on what we can expectfrom plants.

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2Circadian Gating of Cell Division

In Chlamydomonas, the question whether or not the CDC is under circa-dian control, has been a never-ending story. When Chlamydomonas cellsentrained by light/dark cycles are placed under constant light, cell divi-sion persists with a period of 24 hours, suggesting that cell division isunder control of a circadian clock (Bruce 1972). Subsequent studies chal-lenged the former studies suggesting that the CDC is directly regulated bylight, being dependent on energy available though photosynthesis (Spudichand Sager 1980). The proposed model is that cell division is dependent ona timer and a sizer (Donnan and John 1983). Cells divide only when theyhave reached a critical size at a specific phase relative to the synchroniz-ing light/dark cycle but the timer is not a circadian oscillator. Twenty fiveyears later Goto and Johnson clearly demonstrated that cell division is undercircadian control, fulfilling the three criteria of a circadian regulation: (1) en-trainment by different photoperiods, (2) persistence under constant condi-tions, (3) temperature compensation (Goto and Johnson 1995). The currentview is that the circadian clock gates cell division. Every day a circadian-regulated gate is opened only during a limited time, allowing cell division.Chlamydomonas divides by multiple fission, i.e. a cell is able to divide sev-eral times in a row, when it has reached a critical size. As a result, whenthe gate is opened in the middle of the night cells can divide several timesin a row, if they were large enough. Similar gating of cell division has beendescribed in Euglena, Synechococcus, or in animal cells suggesting that gat-ing of cell division, which restricts cell division to specific phases of theday, is widely distributed in living organisms (Cardone and Sassone-Corsi2003). What is the meaning of the circadian gating of cell division? A se-ducing hypothesis is that the circadian clock prevents cells from dividingwhen DNA is the most exposed to mutations. In agreement with this hy-pothesis, Chlamydomonas cells exposed to UV exhibit a circadian-regulatedrhythm of survival, the most sensitive phases corresponding to the time ofnuclear division (Nikaido and Johnson 2000). The importance of circadiangating of cell division in tumor suppression has been established in mousewhere the central clock gene Period2 is required to arrest the CDC pro-gression in animals exposed to γ -radiation (Fu et al. 2002). Finally, a tightconnection between the cell cycle control and the circadian clock was recentlyreported in the fungus Neurospora (Pregueiro et al. 2006). In this organism,the clock protein Period4 is a checkpoint kinase2 homolog, which is involvedin both the DNA damage checkpoint and cell cycle progression, suggestingthat the cell cycle can feedback to the clock though activation of a commoncheckpoint.

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3Evidence for Different Types of Circadian Checkpoints

The CDC core cell cycle machinery is well conserved in eukaryotes, relyingmainly on Cyclin-dependent-kinases (CDKs) which are required for the mainstages of CDC progression including DNA replication during the S phase andsegregation of chromosomes at mitosis (Inze 2005). CDKs are positively reg-ulated by association to cyclins and negatively regulated by small inhibitors(CKI). CDKs are also strongly regulated by phosphorylation and dephos-phorylation. For example, in G2 the WEE1 kinase down-regulates mitoticCDKs by phosphorylation whereas the antagonistic CDC25 phosphatase ac-tivates CDK at the G2/M transition. CDKs are the main targets of the variouscheckpoints, which ensure that CDC progression arrests if something wronghappens such as incomplete DNA replication, DNA damage or spindle de-fect (Millband et al. 2002; Weinert 1998). Another critical checkpoint is thecell-size checkpoint also called “sizer” (Kellogg 2003). During development,cell growth and division must be tightly coordinated to maintain a specificsize. This size control is well known in yeasts. In budding yeast, a criticalrestriction point START or (R) has been defined in G1, when cells becomeirreversibly engaged in cell division when they reach a critical size. In con-trast fission yeast grow mainly in G2 and the control of CDC progressionis exerted at the G2/M transition (Kellogg 2003). Photosynthetic organismsrely on light as the source of energy, to reach a critical size for cell divi-sion. The regulation of cell division by light was dissected in Chlamydomonas.Two points were defined: in early G1, a restriction point called primary arrest(A) when cells become light-dependent; in late G1, a “transition point” (T)when cell division becomes independent of light (Spudich and Sager 1980).Though it remains to be demonstrated clearly that gating of cell division oc-curs before entry into the S phase in Chlamydomonas, it is likely to be so,since arrests outside of the G1 phase are never observed when cells are movedfrom light to darkness (Fig. 1). In contrast, light-dependent restriction mech-anisms were shown to exist both in G1, S and G2 phases of the cell cycle inEuglena cells transferred from light to darkness (Hagiwara et al. 2002) anda circadian gating of CDC progression has been observed from G2 to mito-sis but also at the S/G2 and G1/S transitions in this organism (Bolige et al.2005). The targets of the circadian checkpoints remain elusive in Euglena orChlamydomonas. The only demonstration of a direct regulation of cell divi-sion by the circadian clock come from animals. In hepatocytes re-enteringcell cycle upon hepatectomy, the circadian clock gates cell cycle progression atthe G2/M transition, through a direct transcriptional regulation of the WEE1kinase (Matsuo 2003). A negative regulation of cell cycle by the circadianclock at the G1/S transition was demonstrated in osteoblasts where the clockinhibits the G1 cyclin D1 (Fu et al. 2002). In summary, the circadian clock ap-

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Fig. 1 Circadian gating of cell division in different cell types. In Chlamydomonas or os-teoblasts the clock gates cell division at the G1/S transition. In contrast, in hepatocytes,a circadian regulation of cell division is observed at the G2/M transition through the reg-ulation of the CDK inhibitor WEE1. In Euglena, the clock can arrest the CDC at all majortransitions

pears to gate the CDC at various stages of cell cycle progression, includingG1/S, S/G2 and G2/M (Fig. 1).

Finally, it should be mentioned that while the molecular link between thecircadian clock and the CDC has been characterized in cells re-entering orexiting the CDC and upon checkpoint activation, the molecular basis of cir-cadian gating of cell division in cycling cells, remains to be established.

4What about Plants?

Direct evidences for a circadian regulation of cell division in higher plantsare still lacking. However, based on the ubiquitous nature of circadian reg-ulation of cell division in multicellular organisms, the essential role of thecircadian clock in regulating plant physiology, it is likely that such a con-trol will also exist in plants. On the other hand “green” organisms such asChlamydomonas, which belong to the green lineage, are potentially valuable

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systems to study circadian regulation of cell cycle in plants, however, the mo-lecular mechanisms of the circadian clock are not known in Chlamydomonas.

Except for cryptochromes and casein kinase II, the molecular actors of thecircadian clock are not conserved between kingdoms suggesting that clockshave emerged independently during evolution of plant, animals and fungi(Gardner et al. 2006). Nevertheless, the principles of the clock organization ishighly conserved between organisms. Coupled oscillators, which rely on in-terconnected feedback loops produce robust oscillations. These oscillators areentrained by environmental cycles such as light cycles but also gate input tothe clock by regulating the expression of photoreceptors (Fig. 2). Most of ourknowledge about the plant circadian oscillator comes from Arabidopsis. Thispacemaker consists of two interlocked oscillators. The first transcriptionalfeedback loop consists of the pseudo-response regulator TOC1 (Time of CABexpression1) and the two MYB transcription factors of the REVEILLE family,CCA1 (Circadian Clock Associated 1)/LHY (Late Elongated Hypocotyl) (Al-abadi et al. 2001). The transcription of CCA1/LHY is induced by light in themorning. CCA1/LHY bind to an evening element (EE) found in the promoterof TOC1 and other genes expressed in the evening (Harmer et al. 2000), re-

Fig. 2 A speculative model of CDC control by the circadian clock in plants. The clock con-sists of two interconnected loops. CCA1/LHY and GI are transcribed in response to lightin the morning. CCA1/LHY and GI have opposite inhibiting and activating roles in theregulation of TOC1 expression. CCA1/LHY may regulate the transcription of CDC genessuch as cyclins, CDK or CDK inhibitors (KRP) through a binding to specific circadianelements in their promoters

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pressing the expression of TOC1. On the other hand, TOC1 is responsible forthe activation of CCA1/LHY, though probably indirectly, since there is a de-lay between the peak of TOC1 expression and the transcription of CCA1/LHY.This picture of the plant circadian clock is far from being complete, since thissimple loop does not account for several experimental observations (Lockeet al. 2005). In particular TOC1 overexpression led to an unpredicted de-crease in CCA1 (Hayama and Coupland 2003). Furthermore, cca1/lhy doublemutants still exhibit rhythmicity (Mizoguchi et al. 2002). A second loop wasrecently identified by a mathematical modelization approach. A predictedcandidate Gigantea (GI) is also induced by light leading to the activation ofTOC1 and is transcriptionally repressed by CCA1 (Locke et al. 2005). Thoughthe molecular roles of the respective actors remain to be precisely assessed,this two-loop model accounts much better for experimental data, than theone-loop model does.

The question then is, how does the circadian clock regulate cell divisionin plants? In hepatocytes, the central CLOCK-BMAL1 complex binds the Ebox response element (CACGTG) resulting in a direct activation of WEE1transcription (Matsuo 2003). In Arabidopsis, cis-acting elements mediatinggene expression have been identified in the promoters of circadian-regulatedgenes (ref). The EE (AAAATATCT), mediates the transcriptional repression ofTOC1 by CCA1 at the heart of the clock. A single mutation in the EE to theAAAAATCT CBS sequence (CCA1 binding site element) switches the phase ofcatalase expression from evening to morning (Michael and McClung 2002).We have performed a genome-wide analysis of the main core cell cycle genepromoters in Arabidopsis (Table 1). Both EE and CBS sequences were iden-

Table 1 In silico identification of potential circadian elements (EE and CBS) in Arabidopsiscore cell cycle genes

Gene Accession Motif Location Functionnumber

CDKA,1 At3g48750 AAATATCT (EE) – 1130 G1/S G2/MCDKB1,2 At2g38620 AAATATCT (EE) – 200 G2/M

AAAAATCT (CBS) – 300CDKD,2 At1g66750 AAAATATCT (EE) – 570 G2/Mcyclin D3,1 At4g34160 AATATCT (EE) – 280 G1/ScyclinA3,1 At5g43080 AAAATATCT (EE) – 1000 S/M?

AAAAATCT (CBS) – 1800 SDEL2 At5g14960 AAAATATCT (EE) – 20 G1/SRetinoblastoma At1g22803 AAATATCT (EE) – 500

AAAATCT (CBS) – 500KRP2 At3g50630 AATATCT (EE) – 1600 G2/MKRP3 At5g48820 AAATATCT (EE) – 2200 G1/S G2/M?

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tified in cell cycle genes involved at various stages of cell cycle progression(Table 1), suggesting that the transcription of several cell cycle genes may beregulated by circadian clock components such as CCA1/LHY. A highly specu-lative view of how such a regulation of the clock may regulate cell division isrepresented in Fig. 2.

5Conclusion: A Future for Unicellular Algae in Circadian Studies of Cell Cycle?

The circadian regulation of cell division has been known for a long time inunicellular algae of the green lineage. Recently, the genomes of two greenalgae, the Prasinophyta Ostreococcus tauri and the Chlorophyta Chlamy-domonas, have been sequenced (Derelle et al. 2006). Genetic tools are avail-able in both species and luciferase reporter allows automated monitoring ofin vivo expression of circadian clock and CDC genes in Ostreococcus (ourunpublished results). Both organisms display a minimum set of cell cyclegenes, most cyclins, CDK and regulating kinases and phosphatases beingpresent as a single copy (Bisova et al. 2005; Robbens et al. 2005). Thesegenes are regulated by light/dark cycles in Chlamydomonas. Interestingly,both Chlamydomonas and Ostreococcus contain plant-specific CDC proteinssuch as a B-type CDK, which plays a major role in the control of mitosis inOstreococcus (Corellou et al. 2005). In silico analysis, has revealed the pres-ence of CCA1/LHY and TOC1-like protein homologues in Chlamydomonasand Ostreococcus (Breton and Kay 2006, our unpublished data).

These unique features of green algae may promote them as models ofchoice to study circadian regulation of cell division.

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