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<h3><font style="color:#006400;">The Arabidopsis Circadian Clock</font></h3>
<h3><font style="color:#006400;">Circadian clocks</font></h3>




Circadian clocks have evolved to provide an adaptive advantage to most organisms that live under alternating cycles of light and darkness (Ouyang et al., 1998; Woelfle et al., 2004; Dodd et al., 2005). The clock provides a mechanism whereby physiological and behavioral processes can be performed at the appropriate times of day or night. Furthermore, the evolution of a true oscillator, rather than just a light-responsive sand-timer, enables organisms to predict the alterations that occur in relative proportion to day and night throughout the year in most clines. In mammals, many aspects of behavior and physiology are regulated by endogenous circadian clocks and are subject to daily oscillations (Hastings et al., 2003). In higher plants, the circadian clock regulates many key physiological processes, ranging from flowering time (Yanovsky and Kay, 2003; Imaizumi and Kay, 2006) and growth (Dowson-Day and Millar, 1999) to stomatal opening and CO2 assimilation (Hennessey and Field, 1991). Moreover, in Arabidopsis thaliana the expression of at least 6% of the transcriptome is regulated by the circadian clock (Harmer et al., 2000; Schaffer et al., 2001; Michael and McClung, 2003), and recent findings show that the matching of internal and external cycles optimizes growth and survival (Dodd et al., 2005).  
Circadian clocks have evolved to provide an adaptive advantage to most organisms that live under alternating cycles of light and darkness (Dodd et al., 2005; Ouyang et al., 1998; Woelfle et al., 2004). The clock provides a mechanism whereby physiological and behavioral processes can be performed at the appropriate times of day or night. Furthermore, the evolution of a true oscillator, rather than just a light-responsive sand-timer, enables organisms to predict the alterations that occur in relative proportion to day and night throughout the year in most clines. In mammals, many aspects of behavior and physiology are regulated by endogenous circadian clocks and are subject to daily oscillations (Hastings et al., 2003). In higher plants, the circadian clock regulates many key physiological processes, ranging from flowering time (Imaizumi and Kay, 2006; Yanovsky and Kay, 2003) and growth (Dowson-Day and Millar, 1999; Farre, 2012) to stomatal opening and CO2 assimilation (Farre and Weise, 2012). Moreover, in Arabidopsis thaliana the expression of at least 6% of the transcriptome is regulated by the circadian clock (Harmer et al., 2000; Michael and McClung, 2003; Schaffer et al., 2001), and recent findings show that the matching of internal and external cycles optimizes growth and survival (Dodd et al., 2005).  


[[Image:BasicClock.jpg | center | Figure 1]]
[[Image:BasicClock.jpg | center | Figure 1]]
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Circadian systems can be thought of consisting of 3 parts (Figure 1). The imput pathways are involved in the entrainment or reprograming of the central oscillator which is the core of the circadian system. In turn this molecular self-sustained oscillator regulates the different physiological processes by regulating output pathways.  
Circadian systems can be thought of consisting of 3 parts (Figure 1). The imput pathways are involved in the entrainment or reprograming of the central oscillator which is the core of the circadian system. In turn this molecular self-sustained oscillator regulates the different physiological processes by regulating output pathways.  


'''The mechanisms regulating the circadian oscillator'''


Although circadian clocks in different species utilize distinct proteins, they appear to maintain the same overall pattern of regulation based on the combination of transcriptional regulatory loops with post-translational regulation. Therefore, the elucidation of the molecular mechanisms regulating the clock in plants will help understand the general principles governing circadian oscillators. Circadian systems can be thought of consisting of 3 parts (Figure 1). The imput pathways are involved in the entrainment or reprograming of the central oscillator which is the core of the circadian system. In turn this molecular self-sustained oscillator regulates the different physiological processes by regulating output pathways.


'''Transcriptional feedback loops'''
'''Arabidopsis thaliana'''
The first regulatory feedback loop described in plants consisted of the repression by the morning expressed CCA1 (CIRCADIAN CLOCK ASSOCIATED 1) and LHY (LATE ELONGATED HYPOCOTYL) of the evening expressed TOC1 (TIMING OF CAB EXPRESSION). In turn, TOC1 has been shown to be necessary for CCA1 and LHY activation (Alabadi et al., 2001) (Figure 2). In addition to TOC1, there are several other evening expressed genes that are necessary for the morning expression of CCA1 and LHY. These include the putative MYB transcription factor LUX (LUX ARRYTHMO)(Hazen et al., 2005), as well as ELF3 and ELF4 (EARLY FLOWERING 3, 4) (Schaffer et al., 1998; Doyle et al., 2002; Kikis et al., 2005)(Figure 1).TOC1 belongs to the multigene family of circadian regulated PSEUDO-RESPONSE REGULATORS (PRR), which, in Arabidopsis consists of four other members: PRR3, PRR5, PRR7, PRR9 (Matsushika et al., 2000). We discovered that PRR7 and PRR9 form additional transcriptional feedback loops with CCA1 and LHY indicated that the plant circadian clock might have a multiloop structure similar to that of other eukaryotes (Farre et al., 2005). Using mathematical modeling we and others could show that this network structure was able to reproduce many of the system’s characteristics (Locke et al., 2006; Zeilinger et al., 2006).


[[Image:AraClock2009.jpg | center |400 px| Figure 2]]
We focus our work on the role of the PSEUDO-RESPONSE REGULATORS (PRR)(Farre and Liu, 2013). These proteins are not only involved in the regulation of the Arabidopsis circadian oscillator (Figure 2) but are also involved in the direct regulation of physiological processes (Huang et al., 2012; Liu et al., 2013; Nakamichi et al., 2012).


'''The importance of post-translational regulation'''


In animals and fungi protein degradation, phosphorylation and subcellular localization form part of the molecular mechanisms governing circadian oscillations. In plants recent results have shown that post-translational regulation of protein levels plays a key role in the control of the plant circadian clock.  
[[Image:Clock_2014.jpg | center |600 px| Figure 2]]


In Arabidopsis the ZEITLUPE (ZTL) family of F-box proteins is involved the turnover of clock and flowering time proteins. ZTL regulates the degradation of both TOC1 and PRR5 but not PRR9, PRR7, and PRR3 (Mas et al., 2003; Ito et al., 2007; Kiba et al., 2007; Fujiwara et al., 2008) (Figure 2). LKP2 (LOV KELCH PROTEIN 2) is a homologue of ZTL whose arrhythmic overexpression phenotype indicates a key role in regulating circadian rhythms (Schultz et al., 2001) but LKP targets remain unknown. This ZTL family of F-box proteins that also includes FKF1 (FLAVIN BINDING, KELCH REPEAT, F-BOX 1), a protein involved in the regulation of flowering time (Nelson et al., 2000; Imaizumi et al., 2003; Imaizumi et al., 2005), contains a LOV/PAS domain that mediates blue light dependent protein-protein interactions (Kim et al., 2007; Sawa et al., 2007) (Figure 2).
'''Figure 2.''' Current status of the Arabidopsis circadian clock (2014)


Several clock proteins in Arabidopsis have been shown to be phosphorylated. The phosphorylation of the transcription factor CCA1 by CKBII is necessary for its activity (Daniel et al., 2004). It has been shown recently that all PRR are phosphorylated in vivo (Farre and Kay, 2007; Fujiwara et al., 2008). Phosphorylation is necessary for the interaction between TOC1 and PRR3 proteins (Fujiwara et al., 2008), however the role of the phosphorylation in the other PRRs remains to be elucidated.


'''The circadian regulated pseudo-response regulators'''
'''Nannochloropsis oceanica'''


Arabidopsis has five circadian regulated PRRs. Overexpression and mutant analyses indicate that all of them play a role in the regulation of the circadian clock in Arabidopsis (Mizuno, 2004, 2005). Furthermore, experiments performed in rice, wheat and barley show that the PRRs also play a role in the regulation of the circadian rhythms and flowering time in these species (Murakami et al., 2005; Tago et al., 2005; Turner et al., 2005; Beales et al., 2007; Murakami et al., 2007b; Murakami et al., 2007a). The expression of all PRRs is clock regulated with each peaking at a different time of the day or night (Matsushika et al., 2000). As indicated above, recent results also suggest that post-translational regulation plays a key role in the function of these proteins (Mas et al., 2003; Farre and Kay, 2007; Ito et al., 2007; Kiba et al., 2007). Genetic analyses have shown that PRR7, PRR9 and PRR5 play partially overlapping functions (Farre et al., 2005; Nakamichi et al., 2005b; Nakamichi et al., 2005a; Salome and McClung, 2005).
Nannochloropsis species are small unicellular alga with a diameter of about 2 μm. Marine Nannochloropsis species are used as a source of fish food and omega-3 fatty acids (Adarme-Vega et al., 2012). Due to their high lipid content, which is particularly elevated under nitrogen deprivation, these species have been considered as a potential source of biofuels (Hu and Gao, 2003; Rodolfi et al., 2009; Van Vooren et al., 2012; Xu et al., 2004). The genomes of two Nannochloropsis species have been recently sequenced (Jinkerson et al., 2012; Pan et al., 2011; Radakovits et al., 2012; Vieler et al., 2012). Both species have a small genome of ~30 Mb, containing ~9,000-12,000 genes, similar to the diatoms Phaeodactylum tricornutum and Thalassiosira pseudonana (Armbrust et al., 2004; Bowler et al., 2008). Current research suggests that Nannochloropsis species are haploid and homologous gene replacement has been recently reported (Kilian et al., 2011; Pan et al., 2011). Cell division and lipid content are strongly diurnally regulated in Nannochloropsis (Fábregas et al., 2002; Sukenik and Carmeli, 1990).  
 
PRRs share two conserved protein domains. The pseudo-receiver domain (PR) shares homology with the receiver domains found in response regulators involved in the two-component signaling pathways found in bacteria and plants (Hwang and Sheen, 2002; Oka et al., 2002). However, it lacks the specific aspartate residue that becomes phosphorylated in canonical receiver domains and in vitro experiments suggest that unlike other plant response regulators it cannot be phosphorylated by sensor histidine kinases (Makino et al., 2000; Strayer et al., 2000). The CCT domain (CONSTANS, CONSTANTS-LIKE, TOC1) contains a putative nuclear localization signal and shares some homology with the DNA binding domain of yeast HEME activator protein 2 (HAP2), which is a subunit of the HAP2/HAP3/HAP5 trimeric complex that binds to CCAAT boxes in eukaryotic promoters (Wenkel et al., 2006). However, the DNA binding capacity of CCT domains has not been reported. Recent results have found TOC1 associated with the CCA1 promoter and indicate that it might block the inhibitory activity of the TCP transcription factor CHROMATIN HIKING EXPEDITION 1 (CHE1) on CCA1 expression (Pruneda-Paz et al., 2009), Recent work indicates that PRR3 is involved in the regulation of TOC1 stability(Para et al., 2007), which represents the first report of the biochemical function of a PRRs (Figure 2). The biochemical function of the other PRRs remains to be elucidated.


The genome of N. oceanica CCMP1779 (Vieler et al., 2012) can be found here:http://genome.jgi.doe.gov/Nanoce1779/Nanoce1779.home.html


Clocks have been studied in cyanobacteria, plants, green alga, fungi and animals (Figure 3), however, the mechanisms underlying circadian rhythms in stramenopiles including Nannochloropsis are currently unknown. We have developed circadian reporter lines in different Nannochloropsis species and are currently characterizing their circadian rhythms and searching for clock components.


[[Image:Tree_V2.jpg | center |600 px| Figure 2]]
'''Figure 3.''' Overview of the presence of circadian oscillators in different taxa. Taxa in which circadian rhythms have been detected are in italics. Trc/Trl indicates the presence of a characterized transcriptional/translational circadian clock and the main components are indicated. Trc-less indicates the presence of oscillations of peroxiredoxin oxidation in the absence of transcription (PRX-ox). The green and red circles indicate secondary endosymbiotic events involving green and red alga respectively. Tree is based on tolweb.org.


<h2><font style="color:#006400;">Bibliography</font></h2>
<h2><font style="color:#006400;">Bibliography</font></h2>


*Alabadi, D., Oyama, T., Yanovsky, M.J., Harmon, F.G., Mas, P., and Kay, S.A. (2001). Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science 293, 880-883.
*Adarme-Vega TC, Lim DKY, Timmins M, Vernen F, Li Y, Schenk PM. 2012. Microalgal biofactories: a promising approach towards sustainable omega-3 fatty acid production. Microbial Cell Factories 11.
*Beales, J., Turner, A., GriYths, S., Snape, J.W., and Laurie, D.A. (2007). A Pseudo-Response Regulator is misexpressed in the photoperiod insensitive Ppd-D1a mutant of wheat (Triticum aestivum L.). Theoretical and Applied Genetics 115, 721-733.
*Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, Putnam NH, Zhou SG, Allen AE, Apt KE, Bechner M, Brzezinski MA, Chaal BK, Chiovitti A, Davis AK, Demarest MS, Detter JC, Glavina T, Goodstein D, Hadi MZ, Hellsten U, Hildebrand M, Jenkins BD, Jurka J, Kapitonov VV, Kroger N, Lau WWY, Lane TW, Larimer FW, Lippmeier JC, Lucas S, Medina M, Montsant A, Obornik M, Parker MS, Palenik B, Pazour GJ, Richardson PM, Rynearson TA, Saito MA, Schwartz DC, Thamatrakoln K, Valentin K, Vardi A, Wilkerson FP, Rokhsar DS. 2004. The genome of the diatom Thalassiosira pseudonana: Ecology, evolution, and metabolism. Science 306, 79-86.
*Daniel, X., Sugano, S., and Tobin, E.M. (2004). CK2 phosphorylation of CCA1 is necessary for its circadian oscillator function in Arabidopsis. Proc Natl Acad Sci U S A 101, 3292-3297.
*Bowler C, Allen AE, Badger JH, Grimwood J, Jabbari K, Kuo A, Maheswari U, Martens C, Maumus F, Otillar RP, Rayko E, Salamov A, Vandepoele K, Beszteri B, Gruber A, Heijde M, Katinka M, Mock T, Valentin K, Verret F, Berges JA, Brownlee C, Cadoret JP, Chiovitti A, Choi CJ, Coesel S, De Martino A, Detter JC, Durkin C, Falciatore A, Fournet J, Haruta M, Huysman MJJ, Jenkins BD, Jiroutova K, Jorgensen RE, Joubert Y, Kaplan A, Kroger N, Kroth PG, La Roche J, Lindquist E, Lommer M, Martin-Jezequel V, Lopez PJ, Lucas S, Mangogna M, McGinnis K, Medlin LK, Montsant A, Oudot-Le Secq MP, Napoli C, Obornik M, Parker MS, Petit JL, Porcel BM, Poulsen N, Robison M, Rychlewski L, Rynearson TA, Schmutz J, Shapiro H, Siaut M, Stanley M, Sussman MR, Taylor AR, Vardi A, von Dassow P, Vyverman W, Willis A, Wyrwicz LS, Rokhsar DS, Weissenbach J, Armbrust EV, Green BR, Van De Peer Y, Grigoriev IV. 2008. The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456, 239-244.
*Dodd, A.N., Salathia, N., Hall, A., Kevei, E., Toth, R., Nagy, F., Hibberd, J.M., Millar, A.J., and Webb, A.A. (2005). Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309, 630-633.
*Dodd AN, Salathia N, Hall A, Kevei E, Toth R, Nagy F, Hibberd JM, Millar AJ, Webb AA. 2005. Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309, 630-633.
*Dowson-Day, M.J., and Millar, A.J. (1999). Circadian dysfunction causes aberrant hypocotyl elongation patterns in Arabidopsis. Plant J 17, 63-71.
*Dowson-Day MJ, Millar AJ. 1999. Circadian dysfunction causes aberrant hypocotyl elongation patterns in Arabidopsis. Plant Journal 17, 63-71.
*Doyle, M.R., Davis, S.J., Bastow, R.M., McWatters, H.G., Kozma-Bognar, L., Nagy, F., Millar, A.J., and Amasino, R.M. (2002). The ELF4 gene controls circadian rhythms and flowering time in Arabidopsis thaliana. Nature 419, 74-77.
*Fábregas J, Maseda A, Domínguez A, Ferreira M, Otero A. 2002. Changes in the cell composition of the marine microalga, Nannochloropsis gaditana, during a light:dark cycle. Biotechnology Letters 24, 1699-1703.
*Farre, E.M., and Kay, S.A. (2007). PRR7 protein levels are regulated by light and the circadian clock in Arabidopsis. Plant J 52, 548-560.
*Farre EM. 2012. The regulation of plant growth by the circadian clock. Plant Biology (Stuttgart) 14, 401-410.
*Farre, E.M., Harmer, S.L., Harmon, F.G., Yanovsky, M.J., and Kay, S.A. (2005). Overlapping and distinct roles of PRR7 and PRR9 in the Arabidopsis circadian clock. Curr Biol 15, 47-54.
*Farre EM, Liu T. 2013. The PRR family of transcriptional regulators reflects the complexity and evolution of plant circadian clocks. Current Opinion in Plant Biology Epub.
*Fujiwara, S., Wang, L., Han, L., Suh, S.S., Salome, P.A., McClung, C.R., and Somers, D.E. (2008). Post-translational regulation of the Arabidopsis circadian clock through selective proteolysis and phosphorylation of pseudo-response regulator proteins. J Biol Chem 283, 23073-23083.
*Farre EM, Weise SE. 2012. The interactions between the circadian clock and primary metabolism. Current Opinion in Plant Biology 15, 293-300.
*Harmer, S.L., Hogenesch, J.B., Straume, M., Chang, H.S., Han, B., Zhu, T., Wang, X., Kreps, J.A., and Kay, S.A. (2000). Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290, 2110-2113.
*Harmer SL, Hogenesch JB, Straume M, Chang HS, Han B, Zhu T, Wang X, Kreps JA, Kay SA. 2000. Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290, 2110-2113.
*Hastings, M.H., Reddy, A.B., and Maywood, E.S. (2003). A clockwork web: circadian timing in brain and periphery, in health and disease. Nat Rev Neurosci 4, 649-661.
*Hastings MH, Reddy AB, Maywood ES. 2003. A clockwork web: circadian timing in brain and periphery, in health and disease. Nature Reviews Neuroscience 4, 649-661.
*Hazen, S.P., Schultz, T.F., Pruneda-Paz, J.L., Borevitz, J.O., Ecker, J.R., and Kay, S.A. (2005). LUX ARRHYTHMO encodes a Myb domain protein essential for circadian rhythms. Proc Natl Acad Sci U S A 102, 10387-10392.
*Hu H, Gao K. 2003. Optimization of growth and fatty acid composition of a unicellular marine picoplankton, Nannochloropsis sp., with enriched carbon sources. Biotechnology Letters 25, 421-425.
*Hennessey, T.L., and Field, C.B. (1991). Circadian Rhythms in Photosynthesis : Oscillations in Carbon Assimilation and Stomatal Conductance under Constant Conditions. Plant Physiol 96, 831-836.
*Huang W, Perez-Garcia P, Pokhilko A, Millar AJ, Antoshechkin I, Riechmann JL, Mas P. 2012. Mapping the core of the Arabidopsis circadian clock defines the network structure of the oscillator. Science 336, 75-79.
*Hwang, I., and Sheen, J. (2002). Two-component circuitry in Arabidopsis cytokinin signal transduction. Developmental Biology 247, 484-484.
*Imaizumi T, Kay SA. 2006. Photoperiodic control of flowering: not only by coincidence. Trends in Plant Science 11, 550-558.
*Imaizumi, T., and Kay, S.A. (2006). Photoperiodic control of flowering: not only by coincidence. Trends Plant Sci 11, 550-558.
*Jinkerson RE, Radakovits R, Posewitz MC. 2012. Genomic insights from the oleaginous model alga Nannochloropsis gaditana. Bioengineered 4, 1-7.
*Imaizumi, T., Tran, H.G., Swartz, T.E., Briggs, W.R., and Kay, S.A. (2003). FKF1 is essential for photoperiodic-specific light signalling in Arabidopsis. Nature 426, 302-306.
*Kilian O, Benemann CSE, Niyogi KK, Vick B. 2011. High-efficiency homologous recombination in the oil-producing alga Nannochloropsis sp. Proceedings of the National Academy of Sciences of the United States of America 108, 21265-21269.
*Imaizumi, T., Schultz, T.F., Harmon, F.G., Ho, L.A., and Kay, S.A. (2005). FKF1 F-box protein mediates cyclic degradation of a repressor of CONSTANS in Arabidopsis. Science 309, 293-297.
*Liu T, Carlsson J, Takeuchi T, Newton L, Farre EM. 2013. Direct regulation of abiotic responses by the Arabidopsis circadian clock component PRR7. Plant Journal Epub.
*Ito, S., Nakamichi, N., Kiba, T., Yamashino, T., and Mizuno, T. (2007). Rhythmic and Light-Inducible Appearance of Clock-Associated Pseudo-Response Regulator Protein PRR9 Through Programmed Degradation in the Dark in Arabidopsis thaliana. Plant Cell Physiol., pcm122.
*Michael TP, McClung CR. 2003. Enhancer trapping reveals widespread circadian clock transcriptional control in Arabidopsis. Plant Physiology 132, 629-639.
*Kiba, T., Henriques, R., Sakakibara, H., and Chua, N.H. (2007). Targeted Degradation of PSEUDO-RESPONSE REGULATOR5 by an SCFZTL Complex Regulates Clock Function and Photomorphogenesis in Arabidopsis thaliana. Plant Cell 19, 2516-2530.
*Nakamichi N, Kiba T, Kamioka M, Suzuki T, Yamashino T, Higashiyama T, Sakakibara H, Mizuno T. 2012. Transcriptional repressor PRR5 directly regulates clock-output pathways. Proceedings of the National Academy of Sciences of the United States of America 109, 17123-17128.
*Kikis, E.A., Khanna, R., and Quail, P.H. (2005). ELF4 is a phytochrome-regulated component of a negative-feedback loop involving the central oscillator components CCA1 and LHY. Plant J 44, 300-313.
*Ouyang Y, Andersson CR, Kondo T, Golden SS, Johnson CH. 1998. Resonating circadian clocks enhance fitness in cyanobacteria. Proceedings of the National Academy of Sciences of the United States of America 95, 8660-8664.
*Kim, W.Y., Fujiwara, S., Suh, S.S., Kim, J., Kim, Y., Han, L.Q., David, K., Putterill, J., Nam, H.G., and Somers, D.E. (2007). ZEITLUPE is a circadian photoreceptor stabilized by GIGANTEA in blue light. Nature 449, 356-+.
*Pan K, Qin J, Li S, Dai W, Zhu B, Jin Y, Yu W, Yang G, Li D. 2011. Nuclear monoploidy and asexual propagation of Nannochloropsis oceanica (Eustigmatophyceae) as revealed by its genome sequence. Journal of Phycology 47, 1425-1432.
*Locke, J.C., Kozma-Bognar, L., Gould, P.D., Feher, B., Kevei, E., Nagy, F., Turner, M.S., Hall, A., and Millar, A.J. (2006). Experimental validation of a predicted feedback loop in the multi-oscillator clock of Arabidopsis thaliana. Mol Syst Biol 2, 59.
*Radakovits R, Jinkerson RE, Fuerstenberg SI, Tae H, Settlage RE, Boore JL, Posewitz MC. 2012. Draft genome sequence and genetic transformation of the oleaginous alga Nannochloropis gaditana. Nature Communications 3.
*Makino, S., Kiba, T., Imamura, A., Hanaki, N., Nakamura, A., Suzuki, T., Taniguchi, M., Ueguchi, C., Sugiyama, T., and Mizuno, T. (2000). Genes encoding pseudo-response regulators: insight into His-to-Asp phosphorelay and circadian rhythm in Arabidopsis thaliana. Plant Cell Physiol 41, 791-803.
*Rodolfi L, Zittelli GC, Bassi N, Padovani G, Biondi N, Bonini G, Tredici MR. 2009. Microalgae for Oil: Strain Selection, Induction of Lipid Synthesis and Outdoor Mass Cultivation in a Low-Cost Photobioreactor. Biotechnology and Bioengineering 102, 100-112.
*Mas, P., Kim, W.Y., Somers, D.E., and Kay, S.A. (2003). Targeted degradation of TOC1 by ZTL modulates circadian function in Arabidopsis thaliana. Nature 426, 567-570.
*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.
*Matsushika, A., Makino, S., Kojima, M., and Mizuno, T. (2000). Circadian waves of expression of the APRR1/TOC1 family of pseudo-response regulators in Arabidopsis thaliana: insight into the plant circadian clock. Plant Cell Physiol 41, 1002-1012.
*Sukenik A, Carmeli Y. 1990. LIPID SYNTHESIS AND FATTY ACID COMPOSITION IN NANNOCHLOROPSIS SP. (EUSTIGMATOPHYCEAE) GROWN IN A LIGHT-DARK CYCLE1. Journal of Phycology 26, 463-469.
*Michael, T.P., and McClung, C.R. (2003). Enhancer trapping reveals widespread circadian clock transcriptional control in Arabidopsis. Plant Physiol 132, 629-639.
*Van Vooren G, Le Grand F, Legrand J, Cuine S, Peltier G, Pruvost J. 2012. Investigation of fatty acids accumulation in Nannochloropsis oculata for biodiesel application. Bioresource Technology 124, 421-432.
*Mizuno, T. (2004). Plant response regulators implicated in signal transduction and circadian rhythm. Curr Opin Plant Biol 7, 499-505.
*Vieler A, Wu G, Tsai CH, Bullard B, Cornish AJ, Harvey C, Reca IB, Thornburg C, Achawanantakun R, Buehl CJ, Campbell MS, Cavalier D, Childs KL, Clark TJ, Deshpande R, Erickson E, Armenia Ferguson A, Handee W, Kong Q, Li X, Liu B, Lundback S, Peng C, Roston RL, Sanjaya, Simpson JP, Terbush A, Warakanont J, Zauner S, Farre EM, Hegg EL, Jiang N, Kuo MH, Lu Y, Niyogi KK, Ohlrogge J, Osteryoung KW, Shachar-Hill Y, Sears BB, Sun Y, Takahashi H, Yandell M, Shiu SH, Benning C. 2012. Genome, Functional Gene Annotation, and Nuclear Transformation of the Heterokont Oleaginous Alga Nannochloropsis oceanica CCMP1779. PLoS Genetics 8, e1003064.
*Mizuno, T. (2005). Two-component phosphorelay signal transduction systems in plants: from hormone responses to circadian rhythms. Biosci Biotechnol Biochem 69, 2263-2276.
*Woelfle MA, Ouyang Y, Phanvijhitsiri K, Johnson CH. 2004. The adaptive value of circadian clocks: an experimental assessment in cyanobacteria. Current Biology 14, 1481-1486.
*Murakami, M., Tago, Y., Yamashino, T., and Mizuno, T. (2007a). Characterization of the rice circadian clock-associated pseudo-response regulators in Arabidopsis thaliana. Bioscience Biotechnology and Biochemistry 71, 1107-1110.
*Xu F, Cai ZL, Cong W, Ouyang F. 2004. Growth and fatty acid composition of Nannochloropsis sp. grown mixotrophically in fed-batch culture. Biotechnology Letters 26, 1319-1322.
*Murakami, M., Tago, Y., Yamashino, T., and Mizuno, T. (2007b). Comparative Overviews of Clock-Associated Genes of Arabidopsis thaliana and Oryza sativa. Plant Cell Physiol. 48, 110-121.
*Murakami, M., Matsushika, A., Ashikari, M., Yamashino, T., and Mizuno, T. (2005). Circadian-associated rice pseudo response regulators (OsPRRs): insight into the control of flowering time. Biosci Biotechnol Biochem 69, 410-414.
*Nakamichi, N., Kita, M., Ito, S., Yamashino, T., and Mizuno, T. (2005a). PSEUDO-RESPONSE REGULATORS, PRR9, PRR7 and PRR5, together play essential roles close to the circadian clock of Arabidopsis thaliana. Plant Cell Physiol 46, 686-698.
*Nakamichi, N., Kita, M., Ito, S., Sato, E., Yamashino, T., and Mizuno, T. (2005b). The Arabidopsis pseudo-response regulators, PRR5 and PRR7, coordinately play essential roles for circadian clock function. Plant Cell Physiol 46, 609-619.
*Nelson, D.C., Lasswell, J., Rogg, L.E., Cohen, M.A., and Bartel, B. (2000). FKF1, a clock-controlled gene that regulates the transition to flowering in Arabidopsis. Cell 101, 331-340.
*Oka, A., Sakai, H., and Iwakoshi, S. (2002). His-Asp phosphorelay signal transduction in higher plants: receptors and response regulators for cytokinin signaling in Arabidopsis thaliana. Genes & Genetic Systems 77, 383-391.
*Ouyang, Y., Andersson, C.R., Kondo, T., Golden, S.S., and Johnson, C.H. (1998). Resonating circadian clocks enhance fitness in cyanobacteria. Proc Natl Acad Sci U S A 95, 8660-8664.
*Para, A., Farre, E.M., Imaizumi, T., Pruneda-Paz, J.L., Harmon, F.G., and Kay, S.A. (2007). PRR3 Is a vascular regulator of TOC1 stability in the Arabidopsis circadian clock. Plant Cell 19, 3462-3473.
*Pruneda-Paz, J.L., Breton, G., Para, A., and Kay, S.A. (2009). A functional genomics approach reveals CHE as a component of the Arabidopsis circadian clock. Science 323, 1481-1485.
*Salome, P.A., and McClung, C.R. (2005). PSEUDO-RESPONSE REGULATOR 7 and 9 are partially redundant genes essential for the temperature responsiveness of the Arabidopsis circadian clock. Plant Cell 17, 791-803.
*Sawa, M., Nusinow, D.A., Kay, S.A., and Imaizumi, T. (2007). FKF1 and GIGANTEA complex formation is required for day-length measurement in Arabidopsis. Science 318, 261-265.
*Schaffer, R., Landgraf, J., Accerbi, M., Simon, V., Larson, M., and Wisman, E. (2001). Microarray analysis of diurnal and circadian-regulated genes in Arabidopsis. Plant Cell 13, 113-123.
*Schaffer, R., Ramsay, N., Samach, A., Corden, S., Putterill, J., Carre, I.A., and Coupland, G. (1998). The late elongated hypocotyl mutation of Arabidopsis disrupts circadian rhythms and the photoperiodic control of flowering. Cell 93, 1219-1229.
*Schultz, T.F., Kiyosue, T., Yanovsky, M., Wada, M., and Kay, S.A. (2001). A role for LKP2 in the circadian clock of Arabidopsis. Plant Cell 13, 2659-2670.
*Strayer, C., Oyama, T., Schultz, T.F., Raman, R., Somers, D.E., Mas, P., Panda, S., Kreps, J.A., and Kay, S.A. (2000). Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response regulator homolog. Science 289, 768-771.
*Tago, Y., Murakami, M., Yamashino, T., and Mizuno, T. (2005). Pseudo response regulators implicated in circadian rhythm of rice: Characterization of OsPRR1 orthlogous to the Arabidopsis clock-component TOC1. Plant and Cell Physiology 46, S98-S98.
*Turner, A., Beales, J., Faure, S., Dunford, R.P., and Laurie, D.A. (2005). The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley. Science 310, 1031-1034.
*Wenkel, S., Turck, F., Singer, K., Gissot, L., Le Gourrierec, J., Samach, A., and Coupland, G. (2006). CONSTANS and the CCAAT box binding complex share a functionally important domain and interact to regulate flowering of Arabidopsis. Plant Cell 18, 2971-2984.
*Woelfle, M.A., Ouyang, Y., Phanvijhitsiri, K., and Johnson, C.H. (2004). The adaptive value of circadian clocks: an experimental assessment in cyanobacteria. Curr Biol 14, 1481-1486.
*Yanovsky, M.J., and Kay, S.A. (2003). Living by the calendar: how plants know when to flower. Nat Rev Mol Cell Biol 4, 265-275.
*Zeilinger, M.N., Farre, E.M., Taylor, S.R., Kay, S.A., and Doyle, F.J., 3rd. (2006). A novel computational model of the circadian clock in Arabidopsis that incorporates PRR7 and PRR9. Mol Syst Biol 2, 58.

Latest revision as of 07:29, 2 May 2017


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Circadian clocks


Circadian clocks have evolved to provide an adaptive advantage to most organisms that live under alternating cycles of light and darkness (Dodd et al., 2005; Ouyang et al., 1998; Woelfle et al., 2004). The clock provides a mechanism whereby physiological and behavioral processes can be performed at the appropriate times of day or night. Furthermore, the evolution of a true oscillator, rather than just a light-responsive sand-timer, enables organisms to predict the alterations that occur in relative proportion to day and night throughout the year in most clines. In mammals, many aspects of behavior and physiology are regulated by endogenous circadian clocks and are subject to daily oscillations (Hastings et al., 2003). In higher plants, the circadian clock regulates many key physiological processes, ranging from flowering time (Imaizumi and Kay, 2006; Yanovsky and Kay, 2003) and growth (Dowson-Day and Millar, 1999; Farre, 2012) to stomatal opening and CO2 assimilation (Farre and Weise, 2012). Moreover, in Arabidopsis thaliana the expression of at least 6% of the transcriptome is regulated by the circadian clock (Harmer et al., 2000; Michael and McClung, 2003; Schaffer et al., 2001), and recent findings show that the matching of internal and external cycles optimizes growth and survival (Dodd et al., 2005).

Figure 1
Figure 1

Circadian systems can be thought of consisting of 3 parts (Figure 1). The imput pathways are involved in the entrainment or reprograming of the central oscillator which is the core of the circadian system. In turn this molecular self-sustained oscillator regulates the different physiological processes by regulating output pathways.


Arabidopsis thaliana

We focus our work on the role of the PSEUDO-RESPONSE REGULATORS (PRR)(Farre and Liu, 2013). These proteins are not only involved in the regulation of the Arabidopsis circadian oscillator (Figure 2) but are also involved in the direct regulation of physiological processes (Huang et al., 2012; Liu et al., 2013; Nakamichi et al., 2012).


Figure 2
Figure 2

Figure 2. Current status of the Arabidopsis circadian clock (2014)


Nannochloropsis oceanica

Nannochloropsis species are small unicellular alga with a diameter of about 2 μm. Marine Nannochloropsis species are used as a source of fish food and omega-3 fatty acids (Adarme-Vega et al., 2012). Due to their high lipid content, which is particularly elevated under nitrogen deprivation, these species have been considered as a potential source of biofuels (Hu and Gao, 2003; Rodolfi et al., 2009; Van Vooren et al., 2012; Xu et al., 2004). The genomes of two Nannochloropsis species have been recently sequenced (Jinkerson et al., 2012; Pan et al., 2011; Radakovits et al., 2012; Vieler et al., 2012). Both species have a small genome of ~30 Mb, containing ~9,000-12,000 genes, similar to the diatoms Phaeodactylum tricornutum and Thalassiosira pseudonana (Armbrust et al., 2004; Bowler et al., 2008). Current research suggests that Nannochloropsis species are haploid and homologous gene replacement has been recently reported (Kilian et al., 2011; Pan et al., 2011). Cell division and lipid content are strongly diurnally regulated in Nannochloropsis (Fábregas et al., 2002; Sukenik and Carmeli, 1990).

The genome of N. oceanica CCMP1779 (Vieler et al., 2012) can be found here:http://genome.jgi.doe.gov/Nanoce1779/Nanoce1779.home.html

Clocks have been studied in cyanobacteria, plants, green alga, fungi and animals (Figure 3), however, the mechanisms underlying circadian rhythms in stramenopiles including Nannochloropsis are currently unknown. We have developed circadian reporter lines in different Nannochloropsis species and are currently characterizing their circadian rhythms and searching for clock components.

Figure 2
Figure 2

Figure 3. Overview of the presence of circadian oscillators in different taxa. Taxa in which circadian rhythms have been detected are in italics. Trc/Trl indicates the presence of a characterized transcriptional/translational circadian clock and the main components are indicated. Trc-less indicates the presence of oscillations of peroxiredoxin oxidation in the absence of transcription (PRX-ox). The green and red circles indicate secondary endosymbiotic events involving green and red alga respectively. Tree is based on tolweb.org.

Bibliography

  • Adarme-Vega TC, Lim DKY, Timmins M, Vernen F, Li Y, Schenk PM. 2012. Microalgal biofactories: a promising approach towards sustainable omega-3 fatty acid production. Microbial Cell Factories 11.
  • Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, Putnam NH, Zhou SG, Allen AE, Apt KE, Bechner M, Brzezinski MA, Chaal BK, Chiovitti A, Davis AK, Demarest MS, Detter JC, Glavina T, Goodstein D, Hadi MZ, Hellsten U, Hildebrand M, Jenkins BD, Jurka J, Kapitonov VV, Kroger N, Lau WWY, Lane TW, Larimer FW, Lippmeier JC, Lucas S, Medina M, Montsant A, Obornik M, Parker MS, Palenik B, Pazour GJ, Richardson PM, Rynearson TA, Saito MA, Schwartz DC, Thamatrakoln K, Valentin K, Vardi A, Wilkerson FP, Rokhsar DS. 2004. The genome of the diatom Thalassiosira pseudonana: Ecology, evolution, and metabolism. Science 306, 79-86.
  • Bowler C, Allen AE, Badger JH, Grimwood J, Jabbari K, Kuo A, Maheswari U, Martens C, Maumus F, Otillar RP, Rayko E, Salamov A, Vandepoele K, Beszteri B, Gruber A, Heijde M, Katinka M, Mock T, Valentin K, Verret F, Berges JA, Brownlee C, Cadoret JP, Chiovitti A, Choi CJ, Coesel S, De Martino A, Detter JC, Durkin C, Falciatore A, Fournet J, Haruta M, Huysman MJJ, Jenkins BD, Jiroutova K, Jorgensen RE, Joubert Y, Kaplan A, Kroger N, Kroth PG, La Roche J, Lindquist E, Lommer M, Martin-Jezequel V, Lopez PJ, Lucas S, Mangogna M, McGinnis K, Medlin LK, Montsant A, Oudot-Le Secq MP, Napoli C, Obornik M, Parker MS, Petit JL, Porcel BM, Poulsen N, Robison M, Rychlewski L, Rynearson TA, Schmutz J, Shapiro H, Siaut M, Stanley M, Sussman MR, Taylor AR, Vardi A, von Dassow P, Vyverman W, Willis A, Wyrwicz LS, Rokhsar DS, Weissenbach J, Armbrust EV, Green BR, Van De Peer Y, Grigoriev IV. 2008. The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456, 239-244.
  • Dodd AN, Salathia N, Hall A, Kevei E, Toth R, Nagy F, Hibberd JM, Millar AJ, Webb AA. 2005. Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309, 630-633.
  • Dowson-Day MJ, Millar AJ. 1999. Circadian dysfunction causes aberrant hypocotyl elongation patterns in Arabidopsis. Plant Journal 17, 63-71.
  • Fábregas J, Maseda A, Domínguez A, Ferreira M, Otero A. 2002. Changes in the cell composition of the marine microalga, Nannochloropsis gaditana, during a light:dark cycle. Biotechnology Letters 24, 1699-1703.
  • Farre EM. 2012. The regulation of plant growth by the circadian clock. Plant Biology (Stuttgart) 14, 401-410.
  • Farre EM, Liu T. 2013. The PRR family of transcriptional regulators reflects the complexity and evolution of plant circadian clocks. Current Opinion in Plant Biology Epub.
  • Farre EM, Weise SE. 2012. The interactions between the circadian clock and primary metabolism. Current Opinion in Plant Biology 15, 293-300.
  • Harmer SL, Hogenesch JB, Straume M, Chang HS, Han B, Zhu T, Wang X, Kreps JA, Kay SA. 2000. Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290, 2110-2113.
  • Hastings MH, Reddy AB, Maywood ES. 2003. A clockwork web: circadian timing in brain and periphery, in health and disease. Nature Reviews Neuroscience 4, 649-661.
  • Hu H, Gao K. 2003. Optimization of growth and fatty acid composition of a unicellular marine picoplankton, Nannochloropsis sp., with enriched carbon sources. Biotechnology Letters 25, 421-425.
  • Huang W, Perez-Garcia P, Pokhilko A, Millar AJ, Antoshechkin I, Riechmann JL, Mas P. 2012. Mapping the core of the Arabidopsis circadian clock defines the network structure of the oscillator. Science 336, 75-79.
  • Imaizumi T, Kay SA. 2006. Photoperiodic control of flowering: not only by coincidence. Trends in Plant Science 11, 550-558.
  • Jinkerson RE, Radakovits R, Posewitz MC. 2012. Genomic insights from the oleaginous model alga Nannochloropsis gaditana. Bioengineered 4, 1-7.
  • Kilian O, Benemann CSE, Niyogi KK, Vick B. 2011. High-efficiency homologous recombination in the oil-producing alga Nannochloropsis sp. Proceedings of the National Academy of Sciences of the United States of America 108, 21265-21269.
  • Liu T, Carlsson J, Takeuchi T, Newton L, Farre EM. 2013. Direct regulation of abiotic responses by the Arabidopsis circadian clock component PRR7. Plant Journal Epub.
  • Michael TP, McClung CR. 2003. Enhancer trapping reveals widespread circadian clock transcriptional control in Arabidopsis. Plant Physiology 132, 629-639.
  • Nakamichi N, Kiba T, Kamioka M, Suzuki T, Yamashino T, Higashiyama T, Sakakibara H, Mizuno T. 2012. Transcriptional repressor PRR5 directly regulates clock-output pathways. Proceedings of the National Academy of Sciences of the United States of America 109, 17123-17128.
  • Ouyang Y, Andersson CR, Kondo T, Golden SS, Johnson CH. 1998. Resonating circadian clocks enhance fitness in cyanobacteria. Proceedings of the National Academy of Sciences of the United States of America 95, 8660-8664.
  • Pan K, Qin J, Li S, Dai W, Zhu B, Jin Y, Yu W, Yang G, Li D. 2011. Nuclear monoploidy and asexual propagation of Nannochloropsis oceanica (Eustigmatophyceae) as revealed by its genome sequence. Journal of Phycology 47, 1425-1432.
  • Radakovits R, Jinkerson RE, Fuerstenberg SI, Tae H, Settlage RE, Boore JL, Posewitz MC. 2012. Draft genome sequence and genetic transformation of the oleaginous alga Nannochloropis gaditana. Nature Communications 3.
  • Rodolfi L, Zittelli GC, Bassi N, Padovani G, Biondi N, Bonini G, Tredici MR. 2009. Microalgae for Oil: Strain Selection, Induction of Lipid Synthesis and Outdoor Mass Cultivation in a Low-Cost Photobioreactor. Biotechnology and Bioengineering 102, 100-112.
  • 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.
  • Sukenik A, Carmeli Y. 1990. LIPID SYNTHESIS AND FATTY ACID COMPOSITION IN NANNOCHLOROPSIS SP. (EUSTIGMATOPHYCEAE) GROWN IN A LIGHT-DARK CYCLE1. Journal of Phycology 26, 463-469.
  • Van Vooren G, Le Grand F, Legrand J, Cuine S, Peltier G, Pruvost J. 2012. Investigation of fatty acids accumulation in Nannochloropsis oculata for biodiesel application. Bioresource Technology 124, 421-432.
  • Vieler A, Wu G, Tsai CH, Bullard B, Cornish AJ, Harvey C, Reca IB, Thornburg C, Achawanantakun R, Buehl CJ, Campbell MS, Cavalier D, Childs KL, Clark TJ, Deshpande R, Erickson E, Armenia Ferguson A, Handee W, Kong Q, Li X, Liu B, Lundback S, Peng C, Roston RL, Sanjaya, Simpson JP, Terbush A, Warakanont J, Zauner S, Farre EM, Hegg EL, Jiang N, Kuo MH, Lu Y, Niyogi KK, Ohlrogge J, Osteryoung KW, Shachar-Hill Y, Sears BB, Sun Y, Takahashi H, Yandell M, Shiu SH, Benning C. 2012. Genome, Functional Gene Annotation, and Nuclear Transformation of the Heterokont Oleaginous Alga Nannochloropsis oceanica CCMP1779. PLoS Genetics 8, e1003064.
  • Woelfle MA, Ouyang Y, Phanvijhitsiri K, Johnson CH. 2004. The adaptive value of circadian clocks: an experimental assessment in cyanobacteria. Current Biology 14, 1481-1486.
  • Xu F, Cai ZL, Cong W, Ouyang F. 2004. Growth and fatty acid composition of Nannochloropsis sp. grown mixotrophically in fed-batch culture. Biotechnology Letters 26, 1319-1322.
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