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The functions of WHIRLY1 and REDOXRESPONSIVE TRANSCRIPTION FACTOR 1
in cross tolerance responses in plants:
a hypothesis
rstb.royalsocietypublishing.org
Christine H. Foyer1, Barbara Karpinska1 and Karin Krupinska2
1
2
Review
Cite this article: Foyer CH, Karpinska B,
Krupinska K. 2014 The functions of WHIRLY1
and REDOX-RESPONSIVE TRANSCRIPTION
FACTOR 1 in cross tolerance responses in plants:
a hypothesis. Phil. Trans. R. Soc. B 369:
20130226.
http://dx.doi.org/10.1098/rstb.2013.0226
One contribution of 20 to a Theme Issue
‘Changing the light environment: chloroplast
signalling and response mechanisms’.
Subject Areas:
cellular biology, environmental science,
plant science, molecular biology
Keywords:
cross tolerance, innate immune response,
NONEXPRESSOR OF PATHOGENESIS-RELATED
GENES 1, redox regulation, REDOX-RESPONSIVE
TRANSCRIPTION FACTOR 1, WHIRLY proteins
Author for correspondence:
Christine H. Foyer
e-mail: [email protected]
Centre for Plant Sciences, Faculty of Biology, University of Leeds, Leeds LS2 9JT, UK
Institute of Botany, Christian-Albrechts-University of Kiel, Olshausenstrasse 40, 24098 Kiel, Germany
Chloroplasts are important sensors of environment change, fulfilling key roles
in the regulation of plant growth and development in relation to environmental cues. Photosynthesis produces a repertoire of reductive and
oxidative (redox) signals that provide information to the nucleus facilitating
appropriate acclimation to a changing light environment. Redox signals are
also recognized by the cellular innate immune system allowing activation of
non-specific, stress-responsive pathways that underpin cross tolerance to
biotic–abiotic stresses. While these pathways have been intensively studied
in recent years, little is known about the different components that mediate
chloroplast-to-nucleus signalling and facilitate cross tolerance phenomena.
Here, we consider the properties of the WHIRLY family of proteins and the
REDOX-RESPONSIVE TRANSCRIPTION FACTOR 1 (RRTF1) in relation to
chloroplast redox signals that facilitate the synergistic co-activation of gene
expression pathways and confer cross tolerance to abiotic and biotic stresses.
We propose a new hypothesis for the role of WHIRLY1 as a redox sensor in
chloroplast-to-nucleus retrograde signalling leading to cross tolerance, including acclimation and immunity responses. By virtue of its association with
chloroplast nucleoids and with nuclear DNA, WHIRLY1 is an attractive candidate coordinator of the expression of photosynthetic genes in the nucleus and
chloroplasts. We propose that the redox state of the photosynthetic electron
transport chain triggers the movement of WHIRLY1 from the chloroplasts to
the nucleus, and draw parallels with the regulation of NONEXPRESSOR OF
PATHOGENESIS-RELATED GENES 1 (NPR1).
1. Introduction
Within natural environments, plants are exposed constantly to changing light
levels. Moreover, the lower leaves within plant canopies are frequently subjected
to transient but intense high light intensities. These ‘sun’ or ‘light’ flecks can last
from seconds up to minutes. Sun flecks can make a substantial contribution to
carbon gain, particularly in understorey plants [1–4]. Moreover, they can also
trigger the innate immune responses, enhancing plant defences against pathogens
and in some cases programmed cell death [5–7]. Hence, exposure to one type of
stress confers a general increase in resistance to a range of different stresses, a
phenomenon called cross-tolerance [8,9]. Cross-tolerance occurs because of the
synergistic co-activation of non-specific, stress-responsive pathways that cross
biotic–abiotic stress boundaries [9,10]. Cross-tolerance phenomena are often
associated with the accumulation of reactive oxygen species (ROS) and altered
redox and phytohormone signalling, particularly through ethylene (ET), salicylic
acid (SA), abscisic acid (ABA) and jasmonate (JA)-mediated pathways [11–14].
Chloroplasts play an important role in redox signalling events linking light
acclimation responses to immunity to pathogens as well as in the synthesis of
important plant hormones such as ABA, JA and strigolactones [5–11,15–17].
Moreover, chloroplasts play an important role in systemic as well as local signals,
& 2014 The Author(s) Published by the Royal Society. All rights reserved.
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The photosynthetic electron transport chain is a major sensor
of the light environment, facilitating short-term and longterm adjustments to the photosynthetic machinery in order
to optimize photosynthetic efficiency [30,31]. Within this context, the redox states of the plastoquinone (PQ) pool and the
cytochrome b6,f complex are important in the short-term control of electron transport and in the longer-term adjustments of
membrane protein content and composition through the regulation of gene expression [5,31]. The protein kinase STN7 is
associated with the cytochrome b6,f complex. This kinase is
activated when the PQ pool is reduced. The STN7 kinase is
considered to sense the redox state of the PQ pool in order
to regulate the phosphorylation states of the light harvesting
complex proteins that mediate the state transitions enabling
short-term rebalancing of the supply of excitation energy to
photosystem I (PSI) and photosystem II (PSII) [22]. The
STN7 kinase also participates in long-term responses that
influence nuclear and chloroplast gene expression.
Other plastid protein kinases that are important in the
regulation of gene expression are regulated by redox changes
in the chloroplasts. For example, the plastid-localized Ser/
Thr protein kinase called PTK, which is associated with the
plastid-encoded RNA polymerase, is a global regulator of
chloroplast gene expression [25]. PTK is activated by GSH
and regulated by the phosphorylation state of s-factors [32].
The STN7 kinase regulates the phosphorylation of the PTK
protein, which is less active in the phosphorylated form [22].
Redox-mediated regulation of chloroplast gene expression is
controlled through the phosphorylation of the s-factor called
Sig1, which is triggered by oxidization of the PQ pool to
regulate expression of the psaA and psaB genes, a process
requiring the synergistic activation of thiol signals [25,26,32].
Thiol redox systems involving GSH, thioredoxins, glutaredoxins and peroxiredoxins are widely used as integrators
2. REDOX-RESPONSIVE TRANSCRIPTION FACTOR 1
When leaves experience high light, innate defence and immunity responses are triggered alongside acclimation responses,
which affect leaves that have not experienced high light stress
and newly developing leaves as well as existing leaves
2
Phil. Trans. R. Soc. B 369: 20130226
(a) Chloroplast redox signals
of cellular functions, including electron transport and metabolism, and the linking of photosynthetic functions to gene
transcription and translation, protein synthesis and degradation [11–13,31]. Peroxiredoxins, which use thioredoxins as
a reductant, complement the well-studied glutathione/ascorbate system in peroxide elimination, redox regulation and
signalling [11]. The photosynthetic electron transport chain
generates a number of powerful oxidants, including singlet
oxygen in PSII and superoxide and hydrogen peroxide in PSI
as a result of electron transfer to oxygen [11]. Singlet oxygen
and hydrogen peroxide are important regulators of gene
expression that interface with hormone signalling pathways
to mediate changes in plant morphology, development and
defence [8–14]. These oxidative signals are considered to function alongside signals arising from changes in the reduction
state of the PQ pool to regulate the expression of genes
involved in photosynthesis and defence. For example, the
hydrogen peroxide generated by photosynthesis is required
for the induction of heat shock transcription factors that
occurs as an early response to high light [33].
Much of our current understanding of singlet oxygen
signalling in plants comes from the analysis of the high fluorescence ( flu) mutant, which accumulates protochlorophyllide
when grown in the dark [34,35]. The analysis of transcriptome
patterns in the flu mutant allowed the identification of singletoxygen-induced gene expression patterns that were distinct
from those induced by hydrogen peroxide [35–37]. The singlet
oxygen generated by PSII triggered a signalling pathway that
involves two plastid proteins, called EXECUTER1/2, that participate in the control of oxidant-activated programmed cell
death pathways [38]. Moreover, singlet oxygen-mediated
damage to b-carotene produced the volatile signal b-cyclocitral, which was found to generate gene expression patterns
that were similar to those triggered by singlet oxygen [39].
Such observations demonstrate that carotenoids, like other
chloroplast antioxidants, not only prevent the accumulation
of ROS but are also involved in the transmission of signals.
Modulation of glutathione redox homeostasis is also
important in the transmission of oxidative signals generated
by photosynthetic and photorespiratory metabolism [12–14].
Oxidative signals arising from photorespiration make an
important contribution to immunity towards pathogens
[40,41]. Cysteine residues on proteins such as peroxiredoxins,
and thioredoxins and on low molecular weight thiols such as
GSH mediate signal transduction leading to the activation of
defence responses [13,14,29,40].
ROS generated by NADPH oxidases (or respiratory burst
oxidase homologues, RBOHs) are considered to be important
in both local and systemic redox signalling. In particular,
RBOHD is considered to function in the initiation and selfpropagation of waves of ROS signalling that may facilitate
a means of cell-to-cell communication [9]. It is possible that
along with other signals, RBOH-mediated generation of
ROS waves may contribute to the transmission of systemic
signals over long distances [7,42].
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facilitating a whole plant response to the high light experienced
by a single leaf, a process that is called systemic acquired
acclimation or systemic acquired resistance (SAR) [6,7].
Chloroplast-to-nucleus retrograde signalling is important
for acclimation and defence responses [6,7,15,18–26]. Many
metabolites such as intermediates of tetrapyrrole biosynthesis
such as Mg-ProtoIX, haem, 30 -phosphoadenosine 50 -phosphate
(PAP); b-cyclocitral, ROS and methylerythritol cyclodiphosphate are considered to act as signalling molecules involved
in the transmission of signals to the nucleus [18–26]. Thioredoxins and reduced glutathione (GSH) also participate in the
transmission of redox signals to the nucleus [13,14]. However,
relatively few transcription factors, such as the chloroplast
envelope-bound plant homeodomain (PHD) protein called
PTM and the Apetala 2 (AP2)-type transcription factor (TF),
ABSCISIC ACID INSENSITIVE (ABI)4, have been shown to
function in retrograde signalling [27–29], and their target
genes and mechanisms of action are largely unknown. Similarly, much remains uncertain concerning the mechanisms by
which chloroplast redox metabolism regulates the synthesis
of hormones such as ABA, SA and strigolactones, and signalling metabolites such as oxylipin. Here, we discuss the
functions of the WHIRLY family of proteins and REDOXRESPONSIVE TRANSCRIPTION FACTOR 1 (RRTF1) within
the network of signals that facilitate plant adaptation to
environmental stress.
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SAR is a broad-spectrum resistance in plants that involves
the upregulation of a suite of pathogenesis-related (PR) genes.
The co-activator protein called NONEXPRESSOR OF PATHOGENESIS-RELATED GENES 1 (NPR1) is one the most
intensively studied factors in plant immunity, particularly
relative abundance
relative abundance
(b)
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5
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2000
LL
HL
1500
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500
0
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Figure 1. The effects of high irradiance and the light/dark transition on the
abundance of RRFT1 transcripts in Arabidopsis thaliana. (a) Plants were grown
under low-light conditions (200 mmol m22 s21; open bars) with an 8 h
photoperiod for four weeks. They were then either maintained under lowlight conditions or transferred to a high light (800 mmol m22 s21; filled
bars) chamber for 5 h. The abundance of RRFT1 transcripts was determined
during the first 5 h of illumination under low-light or high-light conditions.
(b) Plants were grown under low-light conditions (200 mmol m22 s21; solid
line) with an 8 h photoperiod for four weeks. Two hours into the photoperiod
plants were either maintained under low-light conditions or transferred to a
high-light (800 mmol m22 s21; dashed line) chamber. In both cases, the
plants were exposed to continuous darkness from the end of the photoperiod
at the 6 h time point for 18 h.
with regard to the SA-mediated pathway [50–52]. The translocation of NPR1 from the cytosol to the nucleus is a critical
regulatory step in PR gene expression. Monomerization of the
oligomeric protein, which is localized in the cytosol, together
with changes in the thiol-disulfide status and nitrosylation of
the NPR1 protein are important for the movement into the
nucleus [50–53]. SA-induced changes in cellular redox status
trigger the reduction of the disulfide bonds on the NPR1 [51].
The monomerization process unmasks a nuclear localization
signal motif that allows the protein to relocate to the nucleus
where it interacts with TGACG-sequence-specific protein-binding (TGA) transcription factors [52], leading to the induction of
expression of defence genes such as PR1 [50]. The oligomer-tomonomer reaction is complex and far from understood, but it
involves S-nitrosylation and thioredoxins [51–53]. S-nitrosylation has the opposite effect to reduction by thioredoxin in the
regulation of NPR1 functions. Hence, monomerization of
the NPR1 protein to the active form is triggered by thioredoxin,
but S-nitrosoglutathione (GSNO)-dependent nitrosylation of
NPR1 monomers favours re-oligomerization [53] as well as
translocation of an NPR1–GFP fusion protein into the nucleus
[54]. Phosphorylation of NPR1 is also required for full induction
of target genes and the establishment of SAR. However, NPR1
is continuously removed from the nucleus by the proteasome,
which restricts its co-activator activity [55].
Redox controls are also important in other pathways that
regulate PR gene expression through components other than
NPR1. For example, GSH is required for H2O2-induced SA
accumulation and signalling leading to PR gene expression in
Phil. Trans. R. Soc. B 369: 20130226
3. Redox regulation of NPR1 and related proteins
(a)
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[5,7,15,43,44]. Relatively few components that are involved in
systemic light signalling pathways have been identified to
date. A likely candidate is the nuclear localized DNA-binding,
AP2/ERF domain transcription factor RRTF1. RRTF1 transcripts are increased in response to a range of biotic and
abiotic stresses. The RRTF1 gene is a target for the WRKY 40
transcription factor, which binds to the RRTF1 promoter [45].
In addition, RRTF1 expression was induced by singlet oxygen
but not by hydrogen peroxide [46]. This finding may suggest
that singlet oxygen-dependent activation of JA and oxylipin signalling pathways may be important in the activation of RRTF1
expression in systemic leaves.
RRTF1 transcripts accumulate in systemic leaves as a result
of systemic light signalling from leaves that had been directly
exposed to high light [44]. We first became interested in
RRTF1 functions, because RRTF1 mRNAs accumulated more
than any other transcript in aphid-infested leaves, and this
response occurred within the first hours of aphids being
placed on the leaves [47]. However, RRTF1 mRNA levels did
not increase in systemic leaves as a result of aphid infestation.
Moreover, aphid fecundity was unaffected in Drrtf1 mutants
that lack a functional RRTF1 [47]. RRTF1 transcripts were
increased in response to JA [48], and this transcription factor
may function alongside JAZ8 and proteins in the JA pathway
to regulate plant defence responses [49].
Some of the characteristics of the light responses of RRTF1
transcripts are shown in figure 1. RRTF1 mRNAs are low in
darkness, but levels increase rapidly but transiently upon illumination. The extent of RRTF1 accumulation depends on the
light level experienced by the leaves (figure 1a). The lightdependent increase in RRTF1 transcripts is transient even in
leaves exposed to high light, with transcript levels falling to
near undetectable levels within hours of the onset of exposure
to light (figure 1a). When the leaves are exposed to an extended
dark period, there is a small, but significant increase in transcripts at the point where the photoperiod would normally
begin, suggesting possible links to circadian control (figure 1b).
The Drrtf1 mutants do not show marked phenotypic differences to the wild-type when grown under low light (figure 2a).
However, the rosettes of wild-type leaves were visibly darker
than those of the Drrtf1 mutants when plants were grown for
two weeks under high light (figure 2b). This difference was
presumably due to the accumulation of protective pigments
such as anthocyanin in the wild-type but not in the Drrtf1
mutant leaves, because the levels of total chlorophyll, the chlorophyll a/b ratios and the ratios of carotenoid pigments to
chlorophyll were similar in both genotypes (figure 2c). A transcriptomic analysis of the leaves of the Drrtf1 mutants
suggested an association between RRTF1 and PAP1 [49],
which is a transcription factor that is involved in the regulation of
anthocyanin biosynthesis. Although the dark-adapted Fv/Fm
values decreased in leaves as a result of transfer from lowlight to high-light growth conditions, the high-light-induced
decrease was similar in mutant and wild-type leaves (figure 2d).
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(a)
4
WT
Drrtf
Drrtf
(d)
chl a/b
carotene/chl a + b
1.00
WT
Drrtf
Fv/Fm
0.90
0.85
0.80
0.75
0.70
LL
HL
WT
LL
Drrtf
HL
0.65
0
4
8
10 14 20 24 30
time (h)
Figure 2. A comparison of rosette parameters in the Arabidopsis thaliana Drrtf mutants and the wild-type (WT). (a) The phenotype of four-week-old plants grown
under low-light conditions (200 mmol m22 s21; rosettes); (b) the phenotype of plants grown under low-light conditions (200 mmol m22 s21) for four weeks and
then under high-light conditions (800 mmol m22 s21) for two weeks; (c) the ratio of chlorophyll a to chlorophyll b (chl a/b) and the ratio of total carotenoid
pigments to total chlorophyll (carotene/chl a þ b) measured under low-light (LL) and high-light conditions (HL) and (d ) the effect of high light on the ratio of
dark-adapted variable chlorophyll a fluorescence to maximal chlorophyll a fluorescence (Fv/Fm) in leaves of the wild-type (WT) and Drrtf mutants (Drrtf ) over the
first 30 h after transfer from low- to high-light conditions. (Online version in colour.)
a pathway that does not involve NPR1 [13,14]. H2O2-induced
JA signalling pathways are also blocked when GSH synthesis
is blocked [13,14]. Hence, oxidant-induced changes in cellular
glutathione status are important mediators of signals in
plant responses to oxidative stress. Moreover, TGA transcription factors are also redox-sensitive. For example, the four
cysteine residues on the purified TGA1 protein can undergo
S-nitrosylation and S-glutathionylation after GSNO treatment.
4. The WHIRLY family of proteins
Plants have a small family of single-stranded DNA binding proteins called WHIRLY that are also involved in the control of
defence gene expression [56,57]. Although most plant species
have two members, some species including Arabidopsis thaliana
have three WHIRLY proteins. In fusion with GFP, the Arabidopsis
WHIRLY1 and 3 proteins were shown to be targeted to chloroplasts, and the WHIRLY2 was targeted to mitochondria [58].
An intriguing feature of WHIRLY1 is its dual location in plastids
and the nucleus of the same cell [59]. Even more intriguing is the
observation that WHIRLY1 in the nucleus has the same molecular weight as the processed form in chloroplasts [59]. The dual
location in plastids and the nucleus of the same cell makes
WHIRLY1 an ideal candidate for information trafficking from
plastids to the nucleus. The translocation of WHIRLY1 from
chloroplasts to the nucleus has been demonstrated recently
in studies using transplastomic tobacco plants synthesizing
an HA-tagged version of WHIRLY1 at the 70S ribosomes of
the organelles [57]. The tagged WHIRLY1 was detected in the
nucleus, where it stimulated expression of PR genes [57].
Early studies on potato revealed that WHIRLY1 binds to the
promoter of the PR10a potato pathogen response gene in the
nucleus [60]. In barley, WHIRLY1 binds to the promoter
of the senescence-associated gene HvS40, which is induced
Figure 3. Immunogold labelling of WHIRLY1 showing its distribution within
a chloroplast in the mesophyll of a primary leaf of Hordeum vulgare L. The
labelling was performed with 10 nm gold particles [56].
during pathogen infection and by senescence as well as by
the hormones such as SA, JA and ABA, whose synthesis
begins in plastids [61,62]. SA levels increase during senescence
[63]. Moreover, SA promotes senescence [64]. Transgenic barley
plants with a reduced level of WHIRLY1 show a stay-green phenotype, despite having a higher level of SA than untransformed
controls (C.H.F., B.K. and K.K. 2012, unpublished data). Moreover, the delayed leaf senescence phenotype observed in the
mutant lines relative to controls was only apparent in plants
grown under high light intensities, suggesting that WHIRLY1
functions downstream of light-dependent SA signalling. As discussed above, high-light-dependent induction of SA signalling
pathways requires redox changes and protein nitrosylation
events that result in NPR1 movement into the nucleus [50,53].
However, WHIRLY1 was identified as a downstream component of SA signalling pathways that are independent of
NPR1 [56]. It has been suggested that SA converts an inactive
Phil. Trans. R. Soc. B 369: 20130226
pigment ratio
0.95
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thylakoid
chloroplast
WHIRLY1
oligomer
PSI
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cytb6f
nucleoid
PSII
nucleus
stroma
response
PSI
s
gnal
ox si
red
target genes
environmental stimuli
lumen
cytb6f
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WHIRLY1 monomers
Figure 5. Schematic model of the WHIRLY1-dependent perception and transduction of redox signals originating from the photosynthetic apparatus. Under control
conditions WHIRLY1 forms 24-oligomers which form a bridge between the thylakoid and the nucleoid. In response to environmental stimuli, the redox state of the
photosynthetic apparatus is altered and this induces a monomerization of WHIRLY1.
form of WHIRLY1 into an active, DNA-binding form by detachment of an unknown inhibitor [60]. With regard to the dual
location of the protein, it is likely that the inactive form is the
plastid isoform of WHIRLY1.
Here, we propose that WHIRLY1 is involved in the perception of redox changes in the photosynthetic apparatus and
in an SA-dependent transduction of this information to the
nucleus. Biochemical studies have shown that chloroplast
WHIRLY1 is present in nucleoid fractions [65,66]. Moreover,
immunogold-labelling studies have shown that WHIRLY1 is
closely associated with thylakoid membranes [59], as shown in
figure 3. These results indicate that WHIRLY1 is located at the
boundary between thylakoids and the nucleoids (figure 4), an
attractive location for a protein whose function might be to
link the operation of the photosynthetic electron transport
chain to gene expression. Given the close association of
WHIRLY1 with components of the thylakoid electron chain, it
is tempting to suggest that WHIRLY1 is important in the
perception of redox functions within the electron transport
system, particularly as the WHIRLY3 protein was identified as
a redox-affected protein in the chloroplasts [67].
All WHIRLY proteins have a cysteine residue in a conserved position (figure 4), which might be involved in the
formation of disulfide bridges between two WHIRLY proteins.
Analyses of the crystal structure of WHIRLY proteins revealed
that they form tetramers [68] and that these tetramers can also
assemble into 24-mers [69,70]. The 24-oligomers of WHIRLY1
have been isolated from chloroplasts [70] and they are likely
to be the structures that bind to the thylakoids. However,
WHIRLY1 functions in plastids are not restricted to photosynthesis. For example, the presence of WHIRLY1 in plastids is
also required for the sensing of ABA during seed germination
[71]. We propose that over-reduction of one or more components of the thylakoid electron transport system such as
the PQ pool/cytochrome b6,f complex leads to destabilization
of the oligomeric WHIRLY1 structure on the thylakoid membrane. This could involve reduction of the cysteine residues
and possibly also nitrosylation in a manner analogous to that
observed in NPR1. Moreover, it is also possible that phosphorylation by the kinases that are activated when the PQ
pool is reduced may also mediate regulation leading to a
release of monomeric proteins, which are then translocated to
Phil. Trans. R. Soc. B 369: 20130226
Figure 4. Amino acid sequences of the WHIRLY1 proteins of Hordeum vulgare L. (Hv), Zea mays (Zm), Solanum tuberosum (St) and Arabidopsis thaliana (At) as well
as of WHIRLY3 of Arabidopsis thaliana (AtWHY3). The plastid targeting sequences (PTP) were determined with either iPSORT prediction (green colour) or with
ChloroP (small letters). Purple: region of the putative transactivation domain important for protein – protein interaction; dark blue: WHIRLY-domain with the
ssDNA-binding domain (KGKAAL, in light blue); red: conserved Cys residue in the sequence of the mature protein (all other Cys are in PTP); orange: putative
autoregulation domain.
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20
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6
nucleus
cytoplasm
PR proteins
WHIRLY1
oligomer
S
S
TRX
SNO
SH
S
S S
S
S
S
S
NPR1
oligomer
S
target genes
NPR1
monomer
Figure 6. Schematic model showing the regulation of PR gene expression by NPR1-dependent and NPR1-independent signalling pathways, which function in
parallel. In this model, the NPR1-independent pathway involves the chloroplast located WHIRLY1 protein. We propose that NPR1 [76] and WHIRLY1 are activated
by redox-mediated processes that regulate monomerization of oligomers. The monomeric forms of both proteins can be translocated to the nucleus to induce PR
gene expression. We propose that thioredoxin (TRX)-dependent reduction of S– S bridges, protein nitrosylation and possibly also protein kinases are involved in the
conformational regulation of WHIRLY1 that regulates monomerization and transport of the monomeric proteins to the nucleus. However, the details of this control
remain to be demonstrated.
the nucleus by an as yet unknown mechanism, as illustrated
in figure 5.
5. Summary and conclusion
A wealth of literature evidence supports the concept that chloroplast redox processes play a pivotal role in the orchestration of
gene expression, and also in post-transcriptional regulation
including translation, protein folding and protein degradation
[9,11,72–75]. The thylakoid electron transport system is a
key sensor of the environment, producing a range of redox
signals that trigger both acclimation and immunity responses.
Downstream thiols such as glutathione and thioredoxins are
important transducers of oxidative signals. Regulation of the
NPR1 pathway involves thioredoxins and nitrosylation,
whereas hydrogen-peroxide-mediated regulation of SA and
JA signalling pathways requires GSH [12–14]. Moreover,
redox processes based in the thylakoid electron transport
system transmit systemic as well as local signals. This is possible at least in part because of the high reactivity of singlet
oxygen. Oxidation of carotenoid pigments and membrane
lipids by singlet oxygen triggers the production of volatile signals that activate the expression of transcription factors such as
RRTF1 in distant systemic leaves to stimulate secondary metabolism and defence processes in leaves that have not directly
experienced the high light stimulus.
It has long been recognized that protein kinases and
phosphatases are important components of chloroplast-tonucleus signalling. However, relatively little is known about
other proteins and mechanisms that link thylakoid redox
state to changes in gene expression. Here, we propose
that the WHIRLY1 protein is ideally placed to function in
transducing information concerning redox changes in the
thylakoid electron transport chain (and the stroma) to regulate
gene expression in the chloroplasts and in the nucleus. We
propose that redox changes in the thylakoid electron transport
chain directly, or indirectly, regulate the degree of association/
dissociation of the WHIRLY1 protein with the thylakoid
membrane and that these redox changes and/or additional
redox processing also regulate the monomerization of the
WHIRLY1 protein, in a manner that might by analogous to
that observed in the regulation of NPR1 (figure 6). In this
way, the WHIRLY1 protein would function as a redoxregulated chloroplast component in retrograde signalling
leading to acclimation and immunity responses, whereas
NPR1 is a cytosolic component linked to the same network
[76]. In this way, WHIRLY1 and NPR1 could function independently in the redox-dependent regulation of gene expression.
Moreover, SA produced in chloroplasts could promote changes
in the distribution of WHIRLY1 and perhaps also translocation
of WHIRLY1 from the chloroplasts to the nucleus by promoting changes in the redox state of the protein. In accordance
with this hypothesis, an Arabidopsis T-DNA insertion mutant
of WHIRLY1 was found to be insensitive towards SA [71].
Acknowledgements. The authors acknowledge funding from the EU Marie
Curie ITN ‘Croplife’ project (Leeds, Kiel: ITN: PITN-GA-2010-264394).
Maria Mulisch (Central Microcopy, University of Kiel) is thanked for
expert immunogold labelling. Rena Isemer (University of Kiel,
Germany) is thanked for the comparison of WHIRLY sequences.
Luca Boschian (University of Kiel, Germany) is thanked for design
and preparation of figures 5 and 6. Barbara Karpinska thanks the EU
for a Marie Curie Individual Fellowship: PIEF-GA-2010-276206.
Phil. Trans. R. Soc. B 369: 20130226
SH
WHIRLY1
monomer
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