Mechanisms of circadian rhythm regulation in plants literature review by dr muzamil ch

Literature Review Article:
Mechanisms of Circadian Rhythm Regulation in
Plants at the Cellular/Molecular Level
By Dr Muzamil Ch
Email: muzamilch2018@gmail.com
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owner first.

1. Introduction:
Plants are exposed to a daily cycle of light and darkness lasting approximately 24 hours. The
rhythmicity of this day-night cycle provides plants fossilized throughout their lives with time
information about environmental changes. [1] Plants can measure time and forecast future
changes using an endogenous clock that is synchronized with environmental time cues.
Circadian rhythms, which are endogenous rhythms with 24-hour periods regulated by an internal
circadian clock, affect a variety of processes in plants, including transcription and post-
transcriptional regulation. [1]
Francis Darwin described the rhythms of stomatal conductance nearly a century ago. Circadian
clocks were discovered in the 1970s to be composed of gene products. [2] Clock genes can be
transcriptionally active during a free-running period. Circadian clock genes are extremely crucial
in plants, accounting for approximately one-third of Arabidopsis transcripts. [2]
They participate in a variety of processes, including the regulation of metabolism, growth,
development, and stomatal opening. Understanding how the circadian oscillator regulates these
biological processes and how these processes affect productivity is a crucial agronomic issue.
[1,2]

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Figure 1: The Plant Circadian Clock.
A TTFL mechanism regulates the plant molecular clock. The image depicts the simplified
molecular clockwork mechanism of Arabidopsis thaliana: the central loop, which is composed of
TOC1, CCA1, and LHY; the morning loop, which is composed of PRR5, PRR7, and PRR9; the
evening complex, which is composed of ELF3, ELF4, and LUX; and the newly described positive
elements, the RVE, and LNK family. Other plant clocks are very similar to each other in nature,
with a few exceptions.

Plants' circadian clock enables them to adapt to daily environmental changes. This is
accomplished through the rhythmic regulation of gene expression, a multistep process. [3]
Posttranscriptional regulation is a vital step at the RNA level because it ensures proper control
over the various amounts and types of messenger RNA that ultimately define the plant cell's
current physiological state. [3]
Recent advances in the study of pre-mRNA processing, RNA turnover and surveillance,
translation regulation, the function of long noncoding RNAs, biogenesis, and small RNA
function, as well as the development of bioinformatics tools, have significantly increased our
understanding of how this regulatory step functions. [4] We review the current state of the art in
circadian regulation research at the post-transcriptional level in plants in this work. It is the
continuous interaction of all post-transcriptional information flow control processes that enables
a plant to precisely time and predict daily environmental changes. [5]
2. Characteristics of Circadian Rhythms:
Circadian rhythms are a subset of biological rhythms that have a period, which is defined as the
time required to complete a 24-hour cycle. This distinguishing feature inspired Franz Halberg to
coin the term circadian in 1959, combining the Latin words "circa" (about) and "dies" (day). [5]

A second distinguishing feature of circadian rhythms is that they are endogenously generated and
self-sustaining, which means they persist under constant environmental conditions, which are
typically constant light (or darkness) and temperature. [6]
The plant is deprived of external time cues under these controlled conditions, and the free-
running period of 24 h is observed. All circadian rhythms share a third characteristic: they are
temperature compensated; the period remains relatively constant across a range of ambient
temperatures. This is believed to be one aspect of a broader mechanism that protects the clock
from changes in cellular metabolism. [6]
Figure 2: Critical Terminology Used to describe Circadian Rhythms.

The term "Period" refers to the duration of one cycle. It is frequently measured from peak to
peak, but it can also be determined from trough to trough or from any specified phase marker.
The “Phase of The Day” refers to the time of day when an event occurs. For instance, if a
rhythm's peak occurs at dawn, its phase is defined as 0 h. If a rhythm peaks six hours after
sunrise, its phase is six hours, and so on. The term "Phase" is frequently used to refer to the
time period specified by the zeitgeber (ZT). Zeitgeber is a German term that refers to any
stimulus that confers time information to the clock. The emergence of light is a highly effective
zeitgeber, and dawn is defined as ZT0. The “Rhythm's Amplitude” is defined as half the
distance between its peak and trough.
Only in exceptional circumstances, such as in the laboratory, is a plant devoid of environmental
time cues derived from the alternation of day and night, such as light/dark cycles or temperature
cycles. [7] These environmental time cues, named zeitgebers (German for time givers),
synchronize the endogenous timing system to a 24-hour period that corresponds precisely to the
exogenous period of the earth's rotation. The ability of a stimulus to reset the clock is time-
dependent. [7]

A pulse of light given before dawn advances the clock's phase, while the same pulse given after
dusk retards the phase. At noon, the same pulse of light has no effect. As a result, it's clear that
the clock controls its sensitivity to environmental stimuli. [6,7] This variable sensitivity can be
quantified and visualized using a phase response curve, which plots the phase shift caused by a
stimulus applied at various times throughout the circadian cycle. [6,7]
3. Mechanisms of Circadian Rhythms Regulation:
3.1. Phosphorylation:
Phosphorylation of key clock proteins is a crucial post-translational modification that is required
for the maintenance of the circadian system in Neurospora, Drosophila, and others, as well as for
clock output pathways. CASEIN KINASES (CK) are conserved across species and are required
for the phosphorylation of a large number of essential clock proteins, including BMAL1 and
PERIOD2 (PER2) in mammals, PERIOD (PER) and TIMELESS (TIM) in Drosophila, and
FREQUENCY in Neurospora. [8]

Figure 3: Phosphorylation of Clock Proteins has an effect on their circadian rhythm regulation
function. (a) CK2 phosphorylates CCA1 and inhibits its binding to target promoters, resulting in
decreased transcriptional activity and a shortened circadian period (LHY indicates that CK2
phosphorylates LHY in vitro, but no evidence of this has been reported in vivo). (b) TOC1 and
PRR5 are phosphorylated by CKL4. TOC1 and PRR5 are phosphorylated to facilitate their
interaction with ZTL and subsequent proteasomal degradation. Additionally, phosphorylation
stabilizes TOC1 via PRR5-mediated nuclear sequestration and through competitive interaction
with PRR3, which protects TOC1 from proteasomal degradation by ZTL. It is unknown whether
the interaction and/or transport properties of TOC1 and PRR5 are mediated by CKL4
phosphorylation. (c) Mutation of the ELF4 phosphorylation site reduces the interaction between
ELF4 and ELF3 and lengthens the circadian period.

The first evidence for CKs being involved in plant clock regulation came from a yeast two-
hybrid screen in which CKB3, a subunit of CK2, was identified as an interacting partner of a
crucial component of the Arabidopsis central oscillator, CCA1. [8] Additional studies
demonstrated that CK2 phosphorylates CCA1 and its closely related homolog, LHY, in vitro,
and that CCA1 phosphorylation is required for its DNA binding to the LIGHT-HARVESTING
CHLOROPHYLL A/B1*3 (LHCB1*3) promoter. [8]
Consistent with this, the cka1a2a3 triple mutant exhibits decreased CCA1 phosphorylation, a
lengthened circadian period, and a diminished photoperiodic flowering response. [9] Ectopic
expression of CKB3 or CKB4 increases CK2 activity and shortens the circadian period in a
manner similar to the cca1 and lhy mutants. In comparison to the cka1a2a3 triple mutant,
silencing the CKB3 gene family prolongs the circadian period. [9]
Later analysis of the role of CKB4 revealed that while CK2 has no effect on the protein
accumulation or subcellular localization of CCA1, it impairs its transcriptional activity, with
dephosphorylated CCA1 protein preferentially bound to the promoters of its target clock genes.
[8,9]
Dephosphorylated CCA1 has a stronger promoter binding to key clock genes, which is consistent
with the long period of the cka1a2a3 mutant and CKB3 gene family knockdown. Both CCA1

binding and CK2 phosphorylation are enhanced at elevated temperatures (which should reduce
binding). [10]
These opposing effects of CK2 and CCA1 are proposed to balance and maintain a stable period
over a physiological temperature range, implying a molecular mechanism underlying the
Arabidopsis clock's temperature compensation. It is possible, however, that CKs are also
involved in the phosphorylation of other clock proteins. [9,10]
3.2. O-Glycosylation:
In Drosophila and mice, protein O-GlcNAcylation mediated by O-linked N-acetylglucosamine
transferases (OGTs) can control the speed of the circadian clock by regulating nuclear entry and
contributing to the stability of core clock proteins. [11]
SPINDLY (SPY) and SECRET AGENT (SEC) were predicted to encode OGTs in higher plants
because they contain an N-terminal tetratricopeptide repeat (TPR) domain and a C-terminal
putative OGT catalytic domain similar to animal OGTs. SEC does O-GlcNAcylate the DELLA
protein RGA in Arabidopsis, as determined by mass spectrometry (MS). However, SPY acts as a
POFUT, modifying RGA by attaching monofucose to specific serine and threonine residues. [11]

Recently, Wang et al. reported that spy mutants, but not sec mutants, exhibit a significantly
prolonged circadian period in both Col-0 and Ler backgrounds. [12] Unlike an earlier report
demonstrating that SPY physically interacts with GI in yeast and in vitro, affinity purification
followed by mass spectrometry (AP-MS) identified PRR5, not GI, as an SPY target, and
additional tests confirmed that SPY O-fucosylates PRR5 in plants. SPY O-fucosylation of PRR5
regulates period by increasing PRR5 proteolysis and alleviating PRR5-mediated repression of
target genes. [12]
Given that SPY O-fucosylates serine and threonine residues that can be phosphorylated
alternatively, it is tempting to speculate that O-fucosylation may regulate clock protein activity
and stability by affecting PRR5 phosphorylation status. [11,12] The crosstalk between O-
GlcNAcylation and phosphorylation is well established, and recent work in the field of
vernalization elaborates the dynamic interaction between phosphorylation and O-glycosylation in
the regulation of gene expression in plants. [13]
Additional studies focusing on the identification of O-fucosylated and phosphorylated PRR5
residues, as well as examination of other clock proteins that may be modified by O-
glycosylation, are necessary to gain a better understanding of the role of O-glycosylation in
circadian period modulation. [13]
3.3. Protein Methylation:
Protein arginine methylation is one of the most prevalent post-translational modifications in
eukaryotes and is required for the regulation of a variety of cellular processes, including
transcriptional regulation and RNA processing. PRMT5, a type II protein arginine
methyltransferase with dual nuclear-cytoplasmic localization, catalyzes the symmetric

dimethylation of arginine residues in histone and non-histone proteins. [14] PRMT5 can
methylate transcription complex components such as SPT5, altering its interaction with RNA
polymerase II and thereby affecting global transcription rates. [14]
Histone methylation mediated by PRMT5 is frequently involved in repressing target gene
expression, and its absence results in a variety of developmental and flowering defects in plants.
[14] Another function of PRMT5 is to methylate Sm spliceosomal proteins, which are required
for RNA processing, with prmt5 mutants exhibiting widespread RNA splicing defects in a
variety of genes involved in multiple biological processes in plants, including the circadian
clock. [14]
Two independent forward genetic screens in Arabidopsis isolated PRMT5 long period mutants,
establishing for the first time a link between protein arginine methylation and the circadian
system. [14] The abundance of PRMT5 transcripts oscillates and responds to both light and
temperature cues, indicating that PRMT5 is a component of the Arabidopsis clock's feedback
loop. [15]
Genome-wide transcriptome abundance and pre-mRNA splicing analyses revealed a
significantly altered gene expression profile in prmt5 mutants, as well as increased intron
retention and enrichment in alternative 5′ splice sites, indicating improper splicing. In prmt5, an
alternatively spliced isoform of PRR9 that retains intron 3 accumulates, whereas the full-length
protein-coding isoform is significantly reduced. [14,15]

PRMT5 also has an effect on PRR7 expression but not on its splicing, despite the fact that
genetic analysis indicates that both PRR7 and PRR9 are required to account for PRMT5's clock
effects. Along with PRR9, other clock-associated genes have been identified as potential targets
of PRMT5, as evidenced by the increased amplitude of GI in the prmt5 mutant. [14]
However, the functional significance of this observation remains unknown, and alternative
splicing-related regulatory mechanisms cannot be ruled out given PRMT5's broad role in protein
arginine methylation. At the very least, methylation by PRMT5 appears to affect the efficiency
with which snRNPs interact with specific splice sites in some clock transcripts. [15]
PRMT5 is also involved in the circadian rhythms of other organisms. Alternative splicing in
clock output pathways rather than the core oscillator was discovered in prmt5 mutants in
Drosophila, indicating evolutionary divergence between plants and animals. Later studies in
Neurospora revealed that PRMT5 is involved in regulating the circadian clock gene frequency
splicing (frq). [15]
JMJD5 contains a jumonji-C domain, which is frequently found in histone demethylase-active
proteins. JMJD5 transcripts oscillate with an early evening phase in Arabidopsis, similar to
TOC1. [15] A jmjd5 mutant shortens the circadian period and can be rescued by a mammalian
JMJD5 ortholog with validated histone demethylase activity, strongly indicating that plants have
a similar function. CCA1 and LHY transcript levels are decreased in jmjd5, consistent with the
cca1 lhy mutant's short circadian period, but no additional work on the demethylase's potential
targets has been reported. [14,15]
3.4. Intercellular/Interorgan Coupling and Tissue-Specific Clocks:

The early understanding of the plant clock was largely limited to whole-plant studies. However,
early work with bean leaves demonstrated that leaf movement and stomatal rhythms had distinct
periods, indicating the presence of multiple types of circadian oscillators in plants. [16] With the
advent of tissue-specific promoters fused to luciferase reporters, the repertoire of luminescent
markers capable of following circadian rhythms in Arabidopsis was expanded. [16]
The Millar lab's work established distinct periods using CAB-, phyB-, and CHS-luciferase
reporters and was the first to extensively document the possibility of multiple tissue-, cell-, or
organ-specific clocks. A recent report indicating that older Arabidopsis leaves have shorter
periods may be due to clock changes in specific leaf tissues or cells as they age. [16]
Recent advances in deciphering the molecular network underlying clock-regulated
synchronization of developmental and physiological processes have been made. Numerous
groups have discovered tissue-specific clocks with distinct rhythmic properties that can affect
one another reciprocally. [17] Direct tissue isolation in conjunction with global gene expression
profiling reveals that vasculature has more robust and sustained rhythms than mesophyll cells, as
well as inverse gene expression profiles in comparison to the whole leaf and mesophyll. [17]

Figure 4: The Coordination of The Plant Clock Within And Between Tissues.
Rhythms are tissue-specific in their phases and durations across the plant. Single-cell imaging
demonstrates both local cell-to-cell coupling (indicated by short gray arrows pointing in the
same direction) and long-distance clock coordination via spatial waves of clock gene expression
(indicated by long gray arrows). Experiments with tissue grafting demonstrate that shoots from
wild-type plants restore the period in the roots of mutants with arrhythmic clocks. ELF4 has the
ability to migrate from shoots to roots, thereby influencing the root clock. Low temperatures
promote ELF4 trafficking, extending the circadian period in roots, whereas high temperatures
inhibit ELF4 movement, shortening the period in roots (the blue arrow in Figure indicates shoot-

to-root movement of ELF4, increased by decreased temperature). Additionally, it has been
demonstrated that light piped from shoots can synchronize the root clock of seedlings (indicated
by yellow arrow).
A spatiotemporal luciferase complementation assay using clock and tissue-specific promoters
confirmed the presence of divergent circadian clock regulation properties in the vasculature. [17]
Organ dissection and grafting experiments revealed that the shoot apical meristem has more
robust and precise rhythms, in contrast to the hypocotyl and root, which have a longer period and
dampened rhythms.[17]
3.5. Polyadenylation and Regulation of Translation:
Polyadenylation plays a critical role in the storage, degradation, and translation of messenger
RNA. As early as 1988, poly (A) tail length was linked to mammalian circadian regulation. [18]
This study established that the neuropeptide vasopressin oscillated in rats' cerebrospinal fluid and
that this oscillation was correlated with the length of the vasopressin mRNA poly(A) tail, which
varied with the time of day. [18]
It was discovered a few years ago that hundreds of mouse liver mRNAs had poly(A) tail lengths
consistent with circadian rhythmicitAnd, while 80% were due to nuclear adenylation in
conjunction with rhythmic transcription, 20% were due to rhythmic cytoplasmic
polyadenylation. The latter was discovered to be partially regulated by polyadenylation element-
binding proteins in the cytoplasm. [18]

The length of the poly(A) tail can change rhythmically as a result of nuclear and/or cytoplasmic
adenylation and deadenylation processes. Numerous deadenylases and poly(A) polymerases are
circadian regulated in mice, indicating that they may contribute to these rhythmic changes in
poly(A) tail length. [18] Interestingly, the rhythmicity of poly(A) tail length is highly correlated
with rhythmic protein expression and that poly(A) tail length peaks several hours before the
observed peak in protein expression. Four poly(A) polymerases and several deadenylases from
the PARN and CCR4/CAF1 complex deadenylase systems have been identified in A. thaliana.
[18]
Researchers searched for these genes, as well as several other homologs identified through
BlastP homology searches, in two publicly available circadian datasets and discovered that,
similar to mice, several of them exhibited circadian rhythmicity at the gene expression level. [18]
It would be interesting to investigate the rhythmicity of poly(A) tail length in plants and to
determine whether rhythmic poly(A) polymerases and deadenylases play a role in this process.
[18]
Additionally, there appears to be a correlation between environmental cues and polyadenylation.
Cirbp and Rbm3, two cold-induced RNA binding proteins, were shown in 2013 to regulate

circadian gene expression by regulating the length of the 3′UTR. Under cold conditions, these
two proteins preferentially bind to proximal polyadenylation sites (PAS). Additionally,
proximal/distal PAS selection was frequently strongly regulated by circadian rhythms. [18]

Figure 5: Rhythmic Poly(A) Polymerases And Deadenylases In A. Thaliana.
(A) A Venn diagram depicting the relationship between the two circadian datasets and the poly
(A) polymerases list. (B) A Venn diagram representing the relationship between two circadian
datasets and the list of known deadenylases and additional deadenylases discovered via BlastP
homology searches. (C) The table represents the poly(A) polymerases and deadenylases of A.
thaliana that are rhythmic and arrhythmic.
Whether or not the same mechanism operates in plants remains unknown. Translation is another
process that is controlled by the circadian rhythm. [19] In mammals, it has been demonstrated
that hnRNP Q regulates AANAT translation via interaction with the 5′UTR of Aanat. hnRNP Q
is expressed rhythmically and exhibits a strong correlation with the AANAT phase of expression.
[19] CHLAMY1, an RNA binding protein with RNA recognition motifs (RRM), regulates the
circadian translation of proteins involved in nitrogen and carbon metabolism in Chlamydomonas
reinhardtii by recognizing UG repeat sequences in the 3′UTR of target messenger RNAs. [19]
Although this process has not been shown to be circadian-regulated in plants, the studies
mentioned above are excellent examples of how to conduct circadian biology research in plants.
It is worth noting, however, that a 2003 study discovered that light-induced translation of a
critical clock component LHY occurred. [19]

Additionally, researchers discovered that when light:dark cycles are present, a combination of
two concurrent processes, translational induction and transcriptional repression of LHY
expression, may help narrow the peak of LHY protein at dawn. [19]
Later that year, in 2012, two global studies demonstrating minimal translational regulation were
published. Both studies investigated the translational landscape of A. thaliana using sucrose-
gradient profiling of ribosomes in conjunction with high-throughput microarray analysis of
ribosome-associated mRNAs.[19]
4. Conclusion:
While the transcription-translation feedback loop (TTFL) model of the circadian clock in
plants has long been dominant, evidence from a variety of sources and organisms indicates that
cytosolic processes may contribute to the maintenance of robust circadian oscillations and may
even affect the circadian period. [20]
In plant cells, for example, oscillations in cytosolic calcium can be connected to the TTFL via
the Ca2+-dependent action of CALMODULIN-LIKE24 (CML24) altering the levels of the
clock-associated transcription factor CHE via a TOC1-dependent signaling pathway. [20]
However, evidence for a purely cytosolic oscillator in plants that is sustained solely by changes
in the PTMs of clock proteins, such as similar hypo/hyperphosphorylation cycles of KaiC in the
cyanobacterium Synechococcus elongatus's remarkable posttranslational oscillator, is lacking.
[20]

Phosphorylation, the most extensively studied PTM in plants, is generally found to alter period
and amplitude but is not required for oscillator maintenance. Similarly, phosphorylation is likely
a modulator of the circadian system in plants. [20,21]
Numerous protein modifications are associated with circadian factors in plants. The increasing
sensitivity of mass spectrometric and genome-wide proteomic techniques is allowing us to refine
our understanding of when and where these various moieties are added and removed. However,
interpretation of their functional significance is becoming more complicated as a result of high-
resolution cell- and tissue-specific clock studies. [20,21]
These reports suggest that the "core clock" may take on a variety of configurations, with some
components being absent or expressed at varying levels depending on the tissue or cell type. The
majority of the PTM studies described above invariably use whole seedling extracts, obscuring
any potential differences between leaf, stem (hypocotyl), or root tissues. [21]
Unlike many metazoan systems, where individual tissues can be harvested and studied
individually, similar work in plants can be extremely laborious and difficult to obtain in
sufficient quantities for protein analysis. Perhaps with the advent of single-cell proteomics, we
will be able to resolve the circadian heterogeneity in plants more precisely. [20,21]

References:
1. Graf, A. Schlereth, “Circadian control of carbohydrate availability for growth in Arabidopsis
plants at night”. Retrieved from Pubmd.gov
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2. Farre, E.M. “The interactions between the circadian clock and primary metabolism”.
Retrieved from Pubmd.gov
3. Brody, S. “The Genetics of Circadian Rhythms”, Retrieved from Europepmc.org
https://europepmc.org/article/med/21924973
4. McClung, C.R. “Plant circadian rhythms”. Retrieved from Pubmd.gov
5. Covington, M.F. “ELF3 modulates resetting of the circadian clock in Arabidopsis”. Retrieved
from Pubmd.gov
6. Andrés Romanowski, “Circadian rhythms and post-transcriptional regulation in higher
plants”. Retrieved from Pubmd.gov

7. Pittendrigh, C.S. “On the temperature independence in the clock system controlling emergence
time in Drosophila”. Retrieved from Pubmd.gov
8. Kusakina, J. “Phosphorylation in the plant circadian system”. Retrieved from Pubmd.gov
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10. Sugano, S. “The protein kinase CK2 is involved in regulation of circadian rhythms in
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https://www.pnas.org/content/96/22/12362.short
11. Jeong, E.H. “A role for O-GlcNAcylation in setting circadian clock speed”. Retrieved from
Genesdev.org
http://genesdev.cshlp.org/content/26/5/490.short
12. Zentella, R. “O-GlcNAcylation of master growth repressor DELLA by SECRET AGENT
modulates multiple signaling pathways in Arabidopsis. Genes”. Retrieved from Genesdev.org
http://genesdev.cshlp.org/content/30/2/164.short
13. Xiao, J. “O-GlcNAc-mediated interaction between VER2 and TaGRP2 elicits TaVRN1 mRNA
accumulation during vernalization in winter wheat”. Retrieved from Pubmd.gov

14. Ren, J.; Wang, Y. “Methylation of ribosomal protein S10 by protein-arginine
methyltransferase 5 regulates ribosome biogenesis” Retrieved from Jbc.org
https://www.jbc.org/article/S0021-9258(20)55050-3/fulltext
15. Pahlich, S. “Protein arginine methylation: Cellular functions and methods of analysis.”
Retrieved from Sciencedirect.com
https://www.sciencedirect.com/science/article/abs/pii/S1570963906002810
16. Bordage, S. “Organ specificity in the plant circadian system is explained by different light
inputs to the shoot and root clocks”. Retrieved from Nph.com
https://nph.onlinelibrary.wiley.com/doi/full/10.1111/nph.14024
17. James, A.B. “The circadian clock in Arabidopsis roots is a simplified slave version of the
clock in shoots”. Retrieved from Pubmd.gov
18. Robinson, B. G. “Vasopressin mRNA in the suprachiasmatic nuclei: daily regulation of
polyadenylate tail length”. Retrieved from Pubmd.gov
19. Liu, Y., Hu, W. “Coldinduced RNA-binding proteins regulate circadian gene expression by
controlling alternative polyadenylation.” Retrieved from Pubmd.gov

20. O’Neill, J.S. “Cellular mechanisms of circadian pacemaking: Beyond transcriptional loops”.
Retrieved from Springer.com
https://link.springer.com/chapter/10.1007/978-3-642-25950-0_4
21. Labib, M. “Single-cell analysis targeting the proteome.” Retrieved from Nature.com
https://www.nature.com/articles/s41570-020-0162-7

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