PSEUDO-RESPONSE REGULATOR 7 and 9 Are Partially
Redundant Genes Essential for the Temperature
Responsiveness of the Arabidopsis Circadian Clock
Patrice A. Salome ´ and C. Robertson McClung1
Dartmouth College, Department of Biological Sciences, Hanover, New Hampshire 03755-3576
Environmental time cues, such as photocycles (light/dark) and thermocycles (warm/cold), synchronize (entrain) endoge-
nous biological clocks to local time. Although much is known about entrainment of the Arabidopsis thaliana clock to
photocycles, the determinants of thermoperception and entrainment to thermocycles are not known. The Arabidopsis
PSEUDO-RESPONSE REGULATOR (PRR) genes, including the clock component TIMING OF CAB EXPRESSION 1/PRR1, are
related to bacterial, fungal, and plant response regulators but lack the conserved Asp that is normally phosphorylated by an
upstream sensory kinase. Here, we show that two PRR family members, PRR7 and PRR9, are partially redundant; single
prr7-3 or prr9-1 mutants exhibit modest period lengthening, but the prr7-3 prr9-1 double mutant shows dramatic and more
than additive period lengthening in the light and becomes arrhythmic in constant darkness. The prr7-3 prr9-1 mutant fails
both to maintain an oscillation after entrainment to thermocycles and to reset its clock in response to cold pulses and thus
represents an important mutant strongly affected in temperature entrainment in higher plants. We conclude that PRR7 and
PRR9 are critical components of a temperature-sensitive circadian system. PRR7 and PRR9 could function in temperature
and light input pathways or they could represent elements of an oscillator necessary for the clock to respond to
Most organisms on the planet live under the daily cycles of night
and day, a consequence of the rotation of the earth on its axis.
Among these organisms, biological rhythmswith a period of 24 h
are widespread. Circadian rhythms are endogenously generated
and maintain a period close to 24 h even in the absence of the
entrainment provided by the daily cycles. These oscillations and
their synchronization with the environment are under genetic
control, and many mutants affecting one or a combination of
these important aspects of circadian rhythmicity have been
isolated in model systems, including Drosophila melanogaster,
and mice (Bell-Pedersen, 2002; Panda et al., 2002a; Golden and
Canales, 2004). Because expression of many clock components
is rhythmic, a coupled transcription/translation feedback loop
was proposed to comprise the central oscillator. The identifica-
tion and characterization of additional mutants has complicated
the simple feedback loop, and current models incorporate two
interconnected feedback loops as the core of the oscillatory
mechanism in fungi and animals (Loros and Dunlap, 2001;
Williams and Sehgal, 2001; Albrecht and Eichele, 2003).
In Arabidopsis thaliana, the current model proposes a single
feedback loop composed of the proteins CIRCADIAN CLOCK
ASSOCIATED 1 (CCA1), LATE AND ELONGATED HYPOCOTYL
(LHY), andTIMING OF CAB
RESPONSE REGULATOR 1 (TOC1/PRR1) (Alabadı ´ et al., 2001).
CCA1 and LHY are single-Myb domain transcription factors that
show dawn peaks in transcription as well as mRNA and protein
abundance (Schaffer et al., 1998; Wang and Tobin, 1998). CCA1
and LHY repress the expression of TOC1 through direct binding
to the TOC1 promoter (Alabadı ´ et al., 2001). Upon turnover
of CCA1 and LHY by an as yet unidentified mechanism, TOC1
repression is alleviated and TOC1 accumulates to peak levels
near dusk. Directly or indirectly, TOC1 closes the loop by
upregulating CCA1 and LHY. TOC1 is degraded via the protea-
some, mediated through SCFZTL, an SCF complex including the
F-box protein ZEITLUPE (ZTL) (Ma ´s et al., 2003a; Han et al.,
2004). CCA1 and LHY are partially redundant, because either
single mutant displays a short period, but the double mutant
becomes arrhythmic after 2 d in continuous conditions (Alabadı ´
et al., 2002; Mizoguchi et al., 2002). Plants carrying the strong
loss of function toc1-2 allele retain rhythmicity, albeit with short
period, under someconditions (in bluelightand in whitelight) but
fail to sustain an oscillation when assayed in red light and in the
dark (Ma ´s et al., 2003b). This suggests that other genes in
addition to TOC1 participate in the generation of the oscillation
and compensate for the loss of TOC1 under some conditions.
Taking the CCA1/LHY redundancy asamodel, onemight expect
that TOC1-related genes may function within or close to the
oscillator itself and show partial functional overlap with TOC1.
TOC1 is a member of the Arabidopsis PRR family, composed of
the rhythmically expressed genes PRR9, PRR7, PRR5, PRR3,
1To whom correspondence should be addressed. E-mail mcclung@
dartmouth.edu; fax 603-646-1347.
The author responsible for distribution of materials integral to the
findings presented in this article in accordance with the policy described
in the Instructions for Authors (www.plantcell.org) is: C. Robertson
Article, publication date, and citation information can be found at
The Plant Cell, Vol. 17, 791–803, March 2005, www.plantcell.org ª 2005 American Society of Plant Biologists
and TOC1/PRR1 (Matsushika et al., 2000). PRRs lack the
conserved Asp that in typical response regulators is phosphor-
ylated by the upstream kinase of the two-component cascade
(Hwang et al., 2002). We and others have shown that loss-of-
function alleles in any of the five PRR genes yield a range of
circadian defects, including period and phase phenotypes,
although no single prr mutation confers arrhythmicity (Eriksson
et al., 2003; Kaczorowski and Quail, 2003; Ma ´s et al., 2003b;
Michael et al., 2003b; Mizuno, 2004). The PRRs can be divided
into three groups based on sequence similarity: PRR3/PRR7,
PRR5/PRR9, and TOC1. However, sequence similarity alone is
not an accurate predictor of functional overlap because loss-of-
function alleles of PRR5 and PRR9 display additive phenotypes
in the double mutant, implying distinct functions (Eriksson et al.,
We reasoned that mutants involved in the same clock function
(warm/cool) or photocycles (light/dark) and constant conditions
in which the clock is predicted to free-run. We therefore charac-
short period mutants prr3-1 and prr5-3 affect period length
modestly, indicating that PRR3 and PRR5 are not necessary for
the plant response to thermocycles. By contrast, prr7-3 and
prr9-1 double mutant exhibits a much stronger clock defect than
prr9-1 double mutant fails to reset in response to temperature
that the phenotypes of prr7-3 prr9-1 are not all dependent on
light. This mutant with insensitivity to temperature signals should
of plant circadian rhythms.
Effect of Thermocycles on Mutants Carrying
Loss-of-Function lhy, ztl, and prr Alleles
h at 228C followed by 12 h at 128C) or 22 to 188C thermocycles
(McClung et al., 2002). We analyzed cotyledon movement
rhythms for the representative short and long period clock
mutants, lhy-20 and ztl-4 (Michael et al., 2003b), and for prr
mutants. To facilitate the comparison of the timing of the
acrophase (peak) of the cotyledon rhythms on successive
days, data were presented as double plots, wherein the first
line shows the peak in cotyledon position of day 1 and day 2, the
to 22 to 128C cycles in constant light and released into free-run
(continuous conditions) at 228C. All mutant seedlings are en-
trained by thermocycles because the mutants share the same
phase as the wild type on the first day after release from
entrainment. Loss-of-function alleles of each of the PRRs, of
the clock components LHY and ZTL (Figure 1), as well as CCA1
and TOC1 (data not shown) yield circadian defects after either
light or temperature entrainment. Their cotyledon movement
phenotypes after thermocycles are also identical to their de-
scribed phenotypes after entrainment to photocycles (Figures
1A, 1D, 1G, 1J, 1M, and 1P). By contrast, loss-of-function alleles
of the PHYTOCHROME B red light photoreceptor, which func-
tions in light input but not in oscillator function, alter the phase of
expression of the clock output gene LIGHT HARVESTING
COMPLEX B (LHCB) after photocycles but not thermocycles
(Salome ´ et al., 2002). This suggests that varying entraining
conditions may prove useful in determining the respective
contribution of putative components of the clock and suggest
a role for the PRRs in temperature response either proximal to or
within the Arabidopsis oscillator.
Another approach to test the response of a mutant to thermo-
cycles is to characterize its circadian phenotype during entrain-
ment. We first tested the ability of mutants in the clock genes
to five photocycles at 228C and then released to 22 to 188C
thermocycles, provided in phase with the light–dark entrainment
(228C replaces light, 188C replaces dark), in continuous light. As
expected for short period mutants that are reset to an exact 24-h
period by the entraining cycles, lhy-20 (Figures 1B and 1C) and
toc1-2 (data not shown; Strayer et al., 2000) display a leading
circadian phase in cotyledon movement. The long period mutant
ztl-4 exhibits the expected lagging phase (Figures 1E and 1F).
thermocycles, we conclude that mutations in the clock genes
LHY, TOC1, and ZTL do not compromise entrainment to thermo-
response to thermocycles.
Mutations in PRR3 do not cause a leading phase during
rhythm is always in phase with the wild type, indicating that it is
effectively entrained by the thermocycles (Figures 1H and 1I).
response to thermocycles.
wild type, but the synchrony between the two genotypes is lost
after 3 to 4 d in the new entraining routine. By the end of the
experiment, prr5-3 mutant seedlings display a phaseopposite to
the wild type (Figures 1K and 1L). The double plot of acrophase
(phase of the peak) during thermocycles suggests that prr5-3
short period seen in the prr5-3 mutant is always modest
(;1 h shorter than the wild type; Michael et al., 2003b) and is
insufficient to readily explain the observed change in phase.
This phenomenon is not seen when the mutant is assayed in
T-cycles with T ¼ 28, or with T ¼ 12 (data not shown), indicating
normal entrainment to these thermocycles. T-cycles are entrain-
in a 28-h T-cycle, the plants are exposed to cycles of 14 h warm
(or light) and 14 h cool (or dark). Although we do not understand
the basis of this phase alteration of prr5-3 during entrainment to
thermocycles, we believe that prr5-3 mutants retain the ability to
entrain to thermocycles because the initial phase of cotyledon
movement is normal after thermocycles (Figure 1J) and during
T-cycles (Figure 1K; data not shown). Nonetheless, the delayed
achievement of a stable phase relationship seen in prr5-3 during
thermocycles suggests that PRR5 plays a role in temperature
entrainment of cotyledon movement.
792The Plant Cell
Leaf Movement Assays, Luciferase Measurement,
and Data Analysis
Leaf movement was measured as described previously (Millar et al.,
1995; Salome ´ et al., 2002). All manipulations, LUC activity measurements
of seedlings entrained to photocycles and thermocycles, and data
analysis were performed as described (Michael and McClung, 2002).
For LUC measurement in the dark, adult prr7-3 prr9-1 plants were
sprayed with 2.5 mM luciferin and 0.05% Triton X-100 the day before the
start of imaging. Plants were transferred back into the long-day cycle
for 1 d. LUC activity in the wild type was measured on 10- to 14-d-old
seedlings transferred to 96-well plates. At zeitgeber time 12, plants were
transferred into a light-tight chamber, and LUC activity was recorded
every 2 h with a Hamamatsu digital CCD camera (C4742-98 ERG;
Hamamatsu Photonics, Hamamatsu City, Japan) using MetaMorph
software. All circadian data were analyzed by fast Fourier transform
nonlinear least squares (Plautz et al., 1997) and by Chrono (Roenneberg
and Taylor, 2000).
We thank Monika Swiatecka for help with luciferase imaging and Jay
Dunlap for helpful discussions. This work was supported by grants from
the National Science Foundation (MCB-0091008 and MCB-0343887).
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NOTE ADDED IN PROOF
While this manuscript was in press, an article by Farre ´ et al. also
described the role of PRR7 and PRR9 in the Arabidopsis clock.
Farre ´, E.M., Harmer, S.L., Harmon, F.G., Yanovsky, M.J., and Kay,
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Temperature-Insensitive Circadian Mutant803