|
Plant Physiol, January 2001, Vol. 125, pp. 98-101
Time for Plants. Progress in Plant Chronobiology
Susan S.
Golden* and
Carl
Strayer
Department of Biology, Texas A&M University, College Station, Texas
77843-3258 (S.S.G.); and Department of Cell Biology and National
Science Foundation Center for Biological Timing, The Scripps
Research Institute, La Jolla, California 92037 (C.S.)
 |
THE SEEDS OF CIRCADIAN BIOLOGY |
More than 270 years ago plants
played the pivotal role in a remarkable discovery: Organisms possess
within themselves a surprisingly accurate timing device that
synchronizes physiology with the daily environmental cycle. The field
of circadian biology arose from the curious observation of de Mairan in
1729 that the daily leaf movements of plants (Mimosa
pudica) persisted for several days after he placed them in
his basement in constant darkness (24). Plant circadian rhythms
continued to intrigue scientists from Linnaeus to Darwin, but little
progress ensued until 2 centuries later, contemporaneous with the first
years of Plant Physiology, when Erwin Bünning revived
the field, again using plants as the subject of study (24). Plant
studies are now poised to deliver novel insights of the inner workings
of a unique 24-h biological clock, largely through the development of
molecular genetic tools that allow the automation of rhythm analysis.
| |
REGULATION IN THE FOURTH DIMENSION |
The pervasive influence of the circadian clock in plants is
reflected in the variety of processes employed as circadian markers by
researchers. Over the years, overt rhythms have been measured in
processes such as stem elongation, root pressure, stomatal aperture,
cell membrane potential, plastid migration, and gas exchange (24).
Photoperiodism was first recognized in the 1920s by Garner and Allard
(who coined the term) while studying the induction of flowering in
tobacco and soybean, and plant researchers first established the
involvement of the circadian clock in controlling these timed events (a
relationship proposed by Bünning; 25).
Control points of the clock have been identified at all levels of gene
expression: transcription, translation, and protein activity through
posttranslational modification. For example, circadian regulation of
CO2 exchange in the leaves of crassulacean acid
metabolism plants is accomplished by circadian activity of the
CO2 assimilatory
phosphoenolpyruvate carboxylase (PEPc) enzyme. The
oscillation in activity derives from cyclic changes in enzyme phosphorylation state, which in turn is dependent on temporal regulation of the abundance of PEPc-specific kinase mRNA. Indirect evidence suggests that a cytological layer of regulation contributes as
well, via circadian control of partitioning of malate, a feedback inhibitor of PEPc, between the cytoplasm and tonoplast (14).
| |
THE PLANT CLOCK GETS A DIGITAL DISPLAY |
Despite progress in characterizing clock-regulated functions, the
lack of a suitable assay that would allow identification of mutants
affected in circadian timing presented a major obstacle for identifying
components of the plant clock. Circadian phenomena can be detected only
by repeated measurement of a physiological process, around the clock
for several days, to reveal peaks and troughs of daily activity.
Genetic investigations introduce the additional requirement of
determining phenotypes from large numbers of progeny, preferably by a
noninvasive assay. Strategies that proved useful in recent decades for
screening animals, such as automated collection of locomotor activity
data, were not adaptable to sessile plants. Apparatus for automated
recording of circadian leaf movements were developed over a century ago
(Fig. 1A;
24), but real progress in genetic and molecular elucidation of the plant clock awaited a more facile circadian assay.
View larger version (67K):
[in this window]
[in a new window]
|
Figure 1.
Automated monitoring systems for plant circadian
rhythms. A, Leaf movement recording device designed by W. Pfeffer in
the late 1800s (reprinted with permission from reference 24). The day
position is shown at left, and the night position at right. B,
Bioluminescence monitoring of transgenic Arabidopsis seedlings. Light
emission reports expression of a luc (firefly luciferase)
fusion to the TOC1 promoter with a trough near dawn (left)
and a peak near dusk.
|
|
Identification of timing mutants, and thus clock-associated genes,
hinged on developing technologies to exploit the circadian oscillation
of transcription of specific genes; their promoters could drive
reporter genes whose expression is amenable to automated quantitation
(12). Luciferases, as reporters, have sufficiently short-lived activity
to allow detection of circadian troughs, and they generate a product
that can be detected sensitively and by automated assay: light (Fig.
1B). Paired with ever-improving imaging technologies and methods for
tagging, mapping, and cloning genes in Arabidopsis, bioluminescence
reporting has provided the means to discover circadian clock-associated
genes of plants, and to explore the connection between the circadian
timing circuit and the signal transduction pathways of
photomorphogenesis and floral development.
| |
CLOCK GENETICS IN PLANTS |
The first plant mutant identified in a screen specifically for
circadian timing mutants was toc1 (timing of CAB)
of Arabidopsis (11), and this locus remains the best candidate to date
for encoding a component of the plant circadian oscillator. Two point
mutant alleles have been cloned, both of which cause shortening of the circadian period of all rhythms tested (23). The data are consistent with a role for TOC1 that is central and unique to the
circadian timing circuit, although its necessity for rhythmicity has
not been established. TOC1 is not homologous to clock
components of animals, fungi, or cyanobacteria
(6); likewise, there are no homologs of most of the clock genes of
other organisms in the Arabidopsis genome. Thus, it appears likely that
the plant circadian mechanism will be quite different from those being
revealed from other phylogenetic groups. TOC1 does not have a
PAS domain, which is found in many other eukaryotic clock
components (6). Rather, it exhibits motifs not described previously in
circadian systems: a receiver domain common among the response
regulator proteins of bacterial two-component sensory transduction
systems, and a basic motif found in the CONSTANS family of plant
proteins (10, 23). The sequence features of TOC1 and its nuclear
localization suggest a role in transcriptional control.
Other clock-associated genes have been described in recent years, such
as those that encode the Myb-type transcription factors CIRCADIAN CLOCK
ASSOCIATED 1 (26) and LATE ELONGATED HYPOCOTYL (18), and the novel
protein GIGANTEA (7, 16). Most of these were found by recognition of a
circadian phenotype in mutants that were originally defined by defects
in photomorphogenesis or flowering time. These mutants underscore a
convergence between the circadian timing system and that of
photoperiodic regulation of flowering, and the reliance of both of
these processes on the perception of light.
| |
PHOTORECEPTORS PROVIDE ENVIRONMENTAL INPUT TO THE CLOCK |
One canonical property of circadian systems is the ability to be
reset, or to have the timing of peaks and troughs synchronized to the
sidereal day. In plants, photoreceptors that are important for
photomorphogenesis, the cryptochromes (1) and phytochromes (17), are
also used to entrain the circadian clock to the day/night cycle, and
they influence the endogenous period of the clock (20). Cryptochromes
serve light input roles to the clock in both Arabidopsis and
Drosophila melanogaster, but in mammals they are more
closely involved in the oscillator mechanism in a light-independent
capacity (1). The sharing of this class of proteins among the circadian systems of diverse organisms is not strong evidence for homology of
clock mechanisms because cryptochromes likely diverged from DNA
photolyases, which are universally distributed and have had ample
opportunity for convergence of function throughout evolution (1).
The phytochromes as clock input photoreceptors have parallels in the
circadian systems of another group, the cyanobacteria. A
bacteriophytochrome, CikA (circadian input kinase), is important for
resetting the clock in Synechococcus elongatus (19). CikA has similarity to the lyase domain of phytochromes, and to the His
protein kinase domain of bacterial two component sensors. It is
intriguing that the protein also carries an unusual receiver motif
that, like the motif in TOC1, lacks the expected aspartyl residue
needed for phosphoryl transfer in response regulator proteins (22).
Whether this similarity between TOC1 and CikA is coincidental, or
indicative of an important biochemical function that cyanobacterial and
plant mechanisms share, has yet to be determined. As is true for
cryptochromes, bacteriophytochromes and phytochromes have widely
diverged family members (8), and their presence in diverse circadian
input systems may owe more to the ease of sculpting a handy
cofactor-binding domain for a variety of functions than to lineage.
The affected gene in the toc7 period mutant
zeitlupe (ZTL) suggests the role of another class
of signal transduction proteins in providing light information to the
circadian clock (20, 21). ZTL period phenotypes are evident
in a variety of circadian-controlled processes, and are strongly
fluence dependent. However, acute responses to light and
photomorphogenesis are not affected by ZTL mutation. Thus,
ZTL may define a signal input mechanism that is more specifically
allied with the clock than are the previously described photoreceptor
pathways. The protein sequence reveals similarity to the PAS domains of
the blue-light sensitive NPH1 (3) and white-collar proteins (5) of
plants and fungi, respectively, as well as kelch motifs. The latter
predict a conserved tertiary structure with unknown activity, called a
beta propeller, which is found in a variety of proteins of diverse
cellular function. ZTL defines a small gene family that
includes one paralog identified as the affected gene in a flowering
time mutant, fkf1 (13).
None of the known light signal transduction genes appears to be
individually essential for circadian timing or entrainment to a diurnal
world. Rather, each has a role in a providing a subset of light
property information, fine-tuning the clock in an environment of
changing fluence and light quality.
| |
FUTURE PROSPECTS |
Insights into the molecular workings of the plant clock are
unfolding at an increasing pace, and will be accelerated dramatically by various genome projects. Components of the plant circadian clock
will likely have partners that interact with constituents of other
systems as well, connecting the circadian timing mechanism with plant
development and light-regulated processes. Additional signatures of the
bacterial contributors to the genome may be evident in plants that are
not seen in animals, like the receiver domain of TOC1. Homology of
plant oscillators with those of other groups of organisms is unlikely,
but conservation of some mechanisms is probable. Extensive
posttranscriptional and especially post-translational control is
expected. Shuttling of clock proteins among subcellular compartments
occurs in animal systems (2, 6), and is a feature of phytochromes (27).
Phosphorylation of the FRQ protein of Neurospora crassa and the PER protein in D. melanogaster influences the accumulation and turnover of
these central clock proteins (6); the cyanobacterial clock protein KaiC
is also phosphorylated, although the function of this modification has
not been demonstrated (15). The wealth of information accessible from
the genome will allow deeper investigation of protein turnover in
circadian timing by assessing the contributions of identifiable players
in the ubiquitination and proteasome pathways (4).
Molecular technologies will reveal a more complete view of the extent
to which the clock controls plant physiology. Approaches such as
differential display can expand the search for circadian regulated
genes without prejudice (9). The most comprehensive global pictures
will come soon from analysis of arrays of genes identified from genome
projects in Arabidopsis and other species, which will allow the
recognition of patterns of circadian coregulation among groups of
genes, at least some of which can be assigned to known physiological pathways.
| |
FOOTNOTES |
*
Corresponding author; e-mail sgolden{at}tamu.edu; fax
979-862-7659.
| |
LITERATURE CITED |
-
Cashmore AR, Jarillo JA, Wu YJ, Liu D
(1999)
Science
284: 760-765
[Abstract/Free Full Text]
-
Ceriani MF, Darlington TK, Staknis D, Mas P, Petti AA, Weitz CJ, Kay SA
(1999)
Science
285: 553-556
[Abstract/Free Full Text]
-
Christie JM, Salomon M, Nozue K, Wada M, Briggs WR
(1999)
Proc Natl Acad Sci U S A
96: 8779-8783
[Abstract/Free Full Text]
-
Ciechanover A, Orian A, Schwartz AL
(2000)
Bioessays
22: 442-451
[CrossRef][ISI][Medline]
-
Crosthwaite SK, Dunlap JC, Loros JJ
(1997)
Science
276: 763-769
[Abstract/Free Full Text]
-
Dunlap JC
(1999)
Cell
96: 271-290
[CrossRef][ISI][Medline]
-
Fowler S, Lee K, Onouchi H, Samach A, Richardson K, Morris B, Coupland G, Putterill J
(1999)
EMBO J
18: 4679-4688
[CrossRef][ISI][Medline]
-
Hughes J, Lamparter T
(1999)
Plant Physiol
121: 1059-1068
[Free Full Text]
-
Kreps JA, Muramatsu T, Furuya M, Kay SA
(2000)
J Biol Rhythms
15: 208-217
[Abstract]
-
Makino S, Kiba T, Imamura A, Hanaki N, Nakamura A, Suzuki T, Taniguchi M, Ueguchi C, Sugiyama T, Mizuno T
(2000)
Plant Cell Physiol
41: 791-803
-
Millar AJ, Carré IA, Strayer CA, Chua N-H, Kay SA
(1995)
Science
267: 1161-1163
[Abstract/Free Full Text]
-
Millar AJ, Short SR, Chua N-H, Kay SA
(1992)
Plant Cell
4: 1075-1087
[Abstract/Free Full Text]
-
Nelson DC, Lasswell J, Rogg LE, Cohen MA, Bartel B
(2000)
Cell
101: 331-340
[CrossRef][ISI][Medline]
-
Nimmo HG
(2000)
Trends Plant Sci
5: 75-80
[CrossRef][ISI][Medline]
-
Nishiwaki T, Iwasaki H, Ishiura M, Kondo T
(2000)
Proc Natl Acad Sci U S A
97: 495-499
[Abstract/Free Full Text]
-
Park DH, Somers DE, Kim YS, Choy YH, Lim HK, Soh MS, Kim HJ, Kay SA, Nam HG
(1999)
Science
285: 1579-1582
[Abstract/Free Full Text]
-
Quail PH
(1998)
Philos Trans R Soc Lond B Biol Sci
353: 1399-1403
[CrossRef][ISI][Medline]
-
Schaffer R, Ramsay N, Samach A, Corden S, Putterill J, Carre IA, Coupland G
(1998)
Cell
93: 1219-1229
[CrossRef][ISI][Medline]
-
Schmitz O, Katayama M, Williams SB, Kondo T, Golden SS
(2000)
Science
289: 765-768
[Abstract/Free Full Text]
-
Somers DE, Devlin PF, Kay SA
(1998)
Science
282: 1488-1490
[Abstract/Free Full Text]
-
Somers DE, Schultz TF, Milnamow M, Kay SA
(2000)
Cell
101: 319-329
[CrossRef][ISI][Medline]
-
Stock JB, Surette MG, Levit M, Park P
(1995)
In
JA Hoch, TJ Silhavy, eds, Two-Component Signal Transduction Systems: Structure-Function Relationships and Mechanisms of Catalysis. ASM Press, Washington, DC, pp 25-51
-
Strayer C, Oyama T, Schultz TF, Raman R, Somers DE, Mas P, Panda S, Kreps JA, Kay SA
(2000)
Science
289: 768-771
[Abstract/Free Full Text]
-
Sweeney BM
(1987)
Rhythmic Phenomena in Plants. Academic Press, San Diego
-
Thomas B
(1998)
In
PJ Lumsden, AJ Millar, eds, Photoperiodism: A Review. Bios Scientific Publishers, Oxford, Washington DC, pp 151-165
-
Wang ZY, Tobin EM
(1998)
Cell
93: 1207-1217
[CrossRef][ISI][Medline]
-
Yamaguchi R, Nakamura M, Mochizuki N, Kay SA, Nagatani A
(1999)
J Cell Biol
145: 437-445
[Abstract/Free Full Text]
© 2001 American Society of Plant Physiologists
|
|
TOP
THE SEEDS OF CIRCADIAN...
REGULATION IN THE FOURTH...