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Room 2123
Department of Plant Biology
1002 Life Sciences, One Shields Ave.
University of California Davis
Davis, CA 95616

Contact: slharmer at ucdavis.edu

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As one adage has it, the only constant is change. A striking example of such constant change is the regular alterations in the environment caused by the daily rotation of the earth on its axis. Along with the obvious diurnal changes in light and temperature, other important environmental variables such as humidity also change on a daily basis. This periodicity in the geophysical world is mirrored by daily periodicity in the behavior and physiology of most organisms. Examples include sleep/wake cycles in animals, developmental transitions in filamentous fungi, the incidence of heart attacks in humans, and changes in organ position in plants. Many of these daily biological rhythms are controlled by the circadian clock, an internal timer or oscillator that keeps approximately 24-hour time. Less obviously, the circadian clock is also important for processes that occur seasonally, including flowering in plants, hibernation in mammals, and long-distance migration in butterflies. In fact, circadian clocks have been found in most organisms that have been appropriately investigated, ranging from photosynthetic bacteria to trees [1].

Figure 1. Model of the plant clock. Three feedback loops (loops A - C) form a transcriptional network that regulates clock function. Also essential to clock function are post-transcriptional regulatory mechanisms (loop D). Many additional genes implicated in clock function have been omitted for clarity. Model from [1]; see this review for further details.

Circadian rhythms have been studied for hundreds of years, with plants used as the first model system (see [2] for an excellent summary of the history of clock research in plants). Recent experimental and mathematical studies have suggested that the plant circadian clock consists of three interlocked transcriptional feedback loops (see Figure 1 for a simplified model). In addition to regulated transcription, post-transcriptional regulation is also clearly essential for proper clock function. Our lab is interested in understanding the molecular nature of the plant circadian clock and how the clock influences plant physiology.

Identification of a novel clock-associated gene

Figure 2. Luciferase activity in a transgenic Arabidopsis plant.

We use firefly luciferase driven by a clock-regulated promoter to monitor circadian rhythms in transgenic plants (Figure 2). This system has the advantage of being relatively high throughput, non-destructive, and automated.

After inducing mutations in plants carrying such a luciferase reporter gene, we isolated many mutants with altered circadian rhythms [3]. One such mutant has an alteration in a gene of unknown function. When this gene, XAP5 CIRCADIAN TIMEKEEPER (XCT), is mutated, plants show altered clock function and light responses (Figure 3). Intriguingly, the C. elegans XCT homolog is essential for viability [4] and this gene is highly conserved across eukaryotes (Figure 4). Despite this high degree of conservation, the molecular function of XCT or its homologs is currently unknown. We are using genetic and biochemical approaches in Arabidopsis and S. pombe to better understand the molecular function of XCT in plant clock and light signaling pathways and its fundamental biochemical role in eukaryotes.

Figure 3. xct mutants have a short-period phenotype when monitored in constant darkness or in different light conditions. Figure 4. Percentage of identical amino acids between species across the entire XAP5 protein is presented in a similarity matrix. Figures from [5].

In addition, we have carried out an enhancer screen to identify mutations that exacerbate the short-period phenotype of gi-200 plants [3]. One such enhancer of gi (egi) mutant has been mapped to a region of the genome with no known clock genes, suggesting it represents a new locus involved in clock function. We are currently using positional cloning to molecularly identify this gene.

Clock regulation of plant physiology

Figure 5. Hormone-responsive genes are circadian regulated. The proportions of clock-regulated genes among all that are upregulated or downregulated by each phytohormone are plotted as columns. Asterisks indicate statistically significant circadian enrichment (p < 0.05). The overlaid polar plots show the average circadian phases of expression for the hormone-responsive genes. Figure from [6].

We are interested in how the clock influences plant physiology at both the mechanistic and descriptive levels. What processes are influenced by the clock? How does the clock regulate its many outputs so that each occurs at the most appropriate time of day? We have taken a genomic approach to address both kinds of questions. Using DNA microarrays, we have found that in young seedlings grown in constant light and temperature, at least 30% of expressed genes show circadian variation in steady-state mRNA levels [6, 7]. Peak expression of these genes occurs at a wide range of times, just as clock regulated physiological pathways show peak activity at diverse times of day.

We have taken advantage of the large number of gene expression profiling experiments carried out in Arabidopsis to identify pathways that might be clock regulated. We found that clock-regulated genes are over-represented among all of the classical plant hormone and multiple stress response pathways, suggesting that all of these pathways are influenced by the circadian clock [6] (Figure 5).

Figure 6. Circadian gating of auxin sensitivity. Plants expressing the auxin-sensitive reporter eDR5::LUC were treated with auxin at 4 h intervals. The black line represents untreated control plants and illustrates circadian regulation of endogenous auxin signaling. Bioluminescence levels at 1 h prior to treatment and 1, 3, and 5 h after treatment are shown in various colors for each auxin application. Areas shaded light- and dark-gray correspond to the 6-h periods during which exogenous auxin promotes or has no effect, respectively, on hypocotyl elongation. Figure from [8].

Indeed, physiological studies revealed that endogenous auxin signaling is clock regulated and that plant responses to exogenous auxin are gated by the clock (that is, auxin sensitivity varies with the time of day) (Figure 6). In recent studies, we have identified a transcription factor that acts a node between the clock and auxin signaling networks. Further exploration of the links between the clock and diverse signaling pathways will lead to a better understanding of how the circadian clock affects plant growth and leads to improved fitness.


  1. Array. . PubMed ID:19133818 | HubMed [Harmer-2009]
  2. McClung CR. Plant circadian rhythms. Plant Cell. 2006 Apr;18(4):792-803. DOI:10.1105/tpc.106.040980 | PubMed ID:16595397 | HubMed [McClung-2006]
  3. Martin-Tryon EL, Kreps JA, and Harmer SL. GIGANTEA acts in blue light signaling and has biochemically separable roles in circadian clock and flowering time regulation. Plant Physiol. 2007 Jan;143(1):473-86. DOI:10.1104/pp.106.088757 | PubMed ID:17098855 | HubMed [Martin-Tryon-2007]
  4. Piano F, Schetter AJ, Morton DG, Gunsalus KC, Reinke V, Kim SK, and Kemphues KJ. Gene clustering based on RNAi phenotypes of ovary-enriched genes in C. elegans. Curr Biol. 2002 Nov 19;12(22):1959-64. DOI:10.1016/s0960-9822(02)01301-5 | PubMed ID:12445391 | HubMed [Piano-2002]
  5. Martin-Tryon EL and Harmer SL. XAP5 CIRCADIAN TIMEKEEPER coordinates light signals for proper timing of photomorphogenesis and the circadian clock in Arabidopsis. Plant Cell. 2008 May;20(5):1244-59. DOI:10.1105/tpc.107.056655 | PubMed ID:18515502 | HubMed [Martin-Tryon-2008]
  6. Covington MF, Maloof JN, Straume M, Kay SA, and Harmer SL. Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development. Genome Biol. 2008;9(8):R130. DOI:10.1186/gb-2008-9-8-r130 | PubMed ID:18710561 | HubMed [Covington-2008]
  7. Harmer SL, Hogenesch JB, Straume M, Chang HS, Han B, Zhu T, Wang X, Kreps JA, and Kay SA. Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science. 2000 Dec 15;290(5499):2110-3. DOI:10.1126/science.290.5499.2110 | PubMed ID:11118138 | HubMed [Harmer-2000]
  8. Covington MF and Harmer SL. The circadian clock regulates auxin signaling and responses in Arabidopsis. PLoS Biol. 2007 Aug;5(8):e222. DOI:10.1371/journal.pbio.0050222 | PubMed ID:17683202 | HubMed [Covington-2007]
All Medline abstracts: PubMed | HubMed