Harmer Lab:Research

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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 transcriptional network underlying the plant clock. Many additional genes implicated in clock function have been omitted for clarity. Model from [2]; see this review for further details.

Circadian rhythms have been studied for hundreds of years, with plants used as the first model system (see [3] for an excellent summary of the history of clock research in plants). As rooted organisms living in a continually changing world, plants are masters at withstanding environmental variation. The circadian clock is key: it both ensures the optimal timing of daily and seasonal events to cope with predictable stresses and regulates myriad signaling pathways to optimize responses to environmental cues. Perhaps for these reasons, the transcriptional network underlying the plant circadian oscillator is uniquely complex and a higher percentage of the transcriptome is under clock control than in other eukaryotes. 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.

Understanding the plant circadian oscillator

We are using forward genetic, genomic, and proteomic approaches to better understand the molecular nature of the transcriptional network underlying the plant clock. In previous work [4, 5], we discovered that RVE4, RVE6, and RVE8, members of a small family of Myb-like transcription factors, are components of the clock (see Figure 1 for a simplified model).

Figure 2. Luciferase activity in a transgenic Arabidopsis plant.

Like their well-known homologs CCA1 and LHY (reviewed in [6]), the RVEs bind to evening element (EE; AAAATATCT) sequences in the regulatory regions of both central clock genes and output genes. However, while the RVEs activate expression of evening-phased target genes, CCA1 and LHY repress expression of these same genes. Thus these related proteins carry out antagonistic biochemical functions within the circadian clock. We are currently investigating the mechanism by which these Myb-like transcription factors control rhythmic expression of clock and output genes. In related work, we are investigating the role of a novel gene in the plant circadian clock. We identified XCT in a forward genetic screen for period mutants using a luciferase reporter gene (Figure 2) [7]. Luciferase imaging is a relatively high throughput, non-destructive, and automated way to monitor circadian rhythms in plants.

Later, we discovered that XCT is also involved in ethylene signaling [8]. XCT is highly conserved across eukaryotes; not only can the Arabidospsis gene complement fission yeast mutant for the XCT ortholog Xap5 [9], but Xap5 can rescue xct mutant plants (Figure 3).

Figure 3. The fission yeast Xap5 gene rescues multiple phenotypes in xct-2 mutants. Unpublished, S. Anver, C. Ellison, and S. Harmer.

Genetic, transcriptomic, and chromatin immunoprecipitation data suggest that yeast Xap5 acts in a similar manner as the variant histone H2A.Z to regulate gene expression and suppress expression of aberrant transcripts[9]. We are now investigating whether XCT plays a similar role in Arabidopsis and working to identify a biochemical function for the XCT protein.

Clock regulation of physiology

Plants with a circadian period matching that of environmental light/dark cycles have a growth advantage [10]. It is therefore perhaps not surprising that most species exhibit daily rhythms in leaf, stem, and root growth [11]. Growth rhythms may be driven directly by environmental factors such as light, temperature, and water availability, but many are the product of complex interactions between external cues and the circadian system[12, 13, 14, 15]. Although great advances have been made in understanding how the clock and environment cooperate to control growth, most such studies have been carried out using the embryonic stem (or hypocotyl) of Arabidopsis as a model. Investigations using different systems are likely to provide novel insights into how plant growth is optimized with the environment.

Figure 4. The apex of a sunflower plant re-orients during the night so that it is facing east well before sunrise. Images were acquired at 30-minute intervals using a consumer camera and a dim solar-powered light. Unpublished, S. Harmer.

To better understand links between the clock, environmental sensing pathways, and growth regulation, we are now collaborating with the Blackman Lab to study growth regulation in sunflower. Sunflower is well-known for diaheliotropism or solar tracking, with plants changing the angle of their leaves and stems over the day so that they remain perpendicular to the sun’s rays. This special type of rhythmic growth is found in many plants (including various crop and pasture species) and is associated with increased yield, likely due to increases in photosynthetic and water use efficiency [16, 17, 18]. The conspicuous movement of aerial organs from east to west during the day is likely mediated by activity of the phototropin blue light photoreceptors [19]. Much more mysterious is the reorientation that occurs during the night so that sunflower leaves and apices face east well before the sun rises (Figure 4) (see also Plants-In-Motion for a wonderful movie of a solar-tracking sunflower). Thus solar tracking is in part a phototropic response, but it also entails directional growth at night in anticipation of the timing and direction of dawn. This anticipatory behavior suggests involvement of the circadian clock. We have confirmed this in growth experiments carried out in environmental control chambers, and are now taking genomic and metabolomics approaches to identify genes and pathways involved in solar tracking. In the future, we plan to carry out functional analysis of selected candidate genes and pathways, taking advantage of the genomic tools now becoming available in sunflower. 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. Harmer SL. The circadian system in higher plants. Annu Rev Plant Biol. 2009;60:357-77. DOI:10.1146/annurev.arplant.043008.092054 | PubMed ID:19575587 | HubMed [Harmer-AnnRev-2009]
  2. Hsu PY and Harmer SL. Wheels within wheels: the plant circadian system. Trends Plant Sci. 2014 Apr;19(4):240-9. DOI:10.1016/j.tplants.2013.11.007 | PubMed ID:24373845 | HubMed [Hsu-TIPS-2014]
  3. McClung CR. Plant circadian rhythms. Plant Cell. 2006 Apr;18(4):792-803. DOI:10.1105/tpc.106.040980 | PubMed ID:16595397 | HubMed [McClung-Rev-2006]
  4. Rawat R, Takahashi N, Hsu PY, Jones MA, Schwartz J, Salemi MR, Phinney BS, and Harmer SL. REVEILLE8 and PSEUDO-REPONSE REGULATOR5 form a negative feedback loop within the Arabidopsis circadian clock. PLoS Genet. 2011 Mar;7(3):e1001350. DOI:10.1371/journal.pgen.1001350 | PubMed ID:21483796 | HubMed [Rawat-PLoSGen_2011]
  5. Hsu PY, Devisetty UK, and Harmer SL. Accurate timekeeping is controlled by a cycling activator in Arabidopsis. Elife. 2013 Apr 30;2:e00473. DOI:10.7554/eLife.00473 | PubMed ID:23638299 | HubMed [Hsu-eLife_2013]
  6. Carré I and Veflingstad SR. Emerging design principles in the Arabidopsis circadian clock. Semin Cell Dev Biol. 2013 May;24(5):393-8. DOI:10.1016/j.semcdb.2013.03.011 | PubMed ID:23597453 | HubMed [Carre-Rev-2013]
  7. 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-XCT-2008]
  8. Ellison CT, Vandenbussche F, Van Der Straeten D, and Harmer SL. XAP5 CIRCADIAN TIMEKEEPER regulates ethylene responses in aerial tissues of Arabidopsis. Plant Physiol. 2011 Feb;155(2):988-99. DOI:10.1104/pp.110.164277 | PubMed ID:21163961 | HubMed [Ellison-XCT-2011]
  9. Anver S, Roguev A, Zofall M, Krogan NJ, Grewal SI, and Harmer SL. Yeast X-chromosome-associated protein 5 (Xap5) functions with H2A.Z to suppress aberrant transcripts. EMBO Rep. 2014 Aug;15(8):894-902. DOI:10.15252/embr.201438902 | PubMed ID:24957674 | HubMed [Anver-Xap5-2014]
  10. Dodd AN, Salathia N, Hall A, Kévei E, Tóth R, Nagy F, Hibberd JM, Millar AJ, and Webb AA. Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science. 2005 Jul 22;309(5734):630-3. DOI:10.1126/science.1115581 | PubMed ID:16040710 | HubMed [Dodd-Science-2005]
  11. Walter A, Silk WK, and Schurr U. Environmental effects on spatial and temporal patterns of leaf and root growth. Annu Rev Plant Biol. 2009;60:279-304. DOI:10.1146/annurev.arplant.59.032607.092819 | PubMed ID:19575584 | HubMed [Walter-AnnRev-2009]
  12. Nozue K, Covington MF, Duek PD, Lorrain S, Fankhauser C, Harmer SL, and Maloof JN. Rhythmic growth explained by coincidence between internal and external cues. Nature. 2007 Jul 19;448(7151):358-61. DOI:10.1038/nature05946 | PubMed ID:17589502 | HubMed [Nozue-Nature-2007]
  13. 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-GenBio-2008]
  14. Michael TP, Breton G, Hazen SP, Priest H, Mockler TC, Kay SA, and Chory J. A morning-specific phytohormone gene expression program underlying rhythmic plant growth. PLoS Biol. 2008 Sep 16;6(9):e225. DOI:10.1371/journal.pbio.0060225 | PubMed ID:18798691 | HubMed [Michael-PLoSBio-2008]
  15. ISBN:0521395631 [Ehleringer-Canopies-1988]
  16. Kao and Forseth (1992) Diurnal leaf movement, chlorophyll fluorescence and carbon assimilation in soybean grown under different nitrogen and water availabilities. Plant, Cell and Environment 15, 703-710.

  17. Zhang, Zhang, Feng, Tian, & Zhang (2009) Leaf diaheliotropic movement can improve carbon gain and water use efficiency and not intensify photoinhibition in upland cotton (Gossypium hirsutum L.). Photosynthetica 47, 609-615.

  18. Vandenbrink JP, Brown RI, Harmer SL, and Blackman BK. Turning heads: the biology of solar tracking in sunflower. Plant Sci. 2014 Jul;224:20-6. DOI:10.1016/j.plantsci.2014.04.006 | PubMed ID:24908502 | HubMed [Vandenbrink-PlantSci-Rev-2014]
All Medline abstracts: PubMed | HubMed