Signalling crosstalk in light stress and

immune reactions in plants

Andrea Trotta1, Moona Rahikainen1, Grzegorz Konert1, Giovanni Finazzi2,3,4,5
and Saijaliisa Kangasjarvi1

rstb.royalsocietypublishing.org

Review
Cite this article: Trotta A, Rahikainen M,
Konert G, Finazzi G, Kangasjarvi S. 2014
Signalling crosstalk in light stress and immune
reactions in plants. Phil. Trans. R. Soc. B 369:
20130235.
http://dx.doi.org/10.1098/rstb.2013.0235
One contribution of 20 to a Theme Issue
Changing the light environment: chloroplast
signalling and response mechanisms.
Subject Areas:
plant science
Keywords:
chloroplast, photosynthesis, reactive oxygen
species, salicylic acid, plant immunity
Author for correspondence:
Saijaliisa Kangasjarvi
e-mail: saijaliisa.kangasjarvi@utu.fi

Molecular Plant Biology, University of Turku, Turku 20014, Finland

Centre National de la Recherche Scientifique, Laboratoire de Physiologie Cellulaire et Vegetale, Unite Mixte de
Recherche 5168, Grenoble 38054, France
3
Commissariat a` lEnergie Atomique et Energies Alternatives, Institut de Recherches en Technologies et Sciences
pour le Vivant, Grenoble 38054, France
4
Universite Grenoble-Alpes, Grenoble 38054, France
5
Institut National Recherche Agronomique, Unite Sous Contrat 1359, Grenoble 38054, France
2

The evolutionary history of plants is tightly connected with the evolution of

microbial pathogens and herbivores, which use photosynthetic end products
as a source of life. In these interactions, plants, as the stationary party, have
evolved sophisticated mechanisms to sense, signal and respond to the presence
of external stress agents. Chloroplasts are metabolically versatile organelles that
carry out fundamental functions in determining appropriate immune reactions in plants. Besides photosynthesis, chloroplasts host key steps in the
biosynthesis of amino acids, stress hormones and secondary metabolites,
which have a great impact on resistance against pathogens and insect herbivores. Changes in chloroplast redox signalling pathways and reactive oxygen
species metabolism also mediate local and systemic signals, which modulate
plant resistance to light stress and disease. Moreover, interplay among chloroplastic signalling networks and plasma membrane receptor kinases is emerging
as a key mechanism that modulates stress responses in plants. This review highlights the central role of chloroplasts in the signalling crosstalk that essentially
determines the outcome of plantpathogen interactions in plants.

1. Introduction
Chloroplasts are metabolically versatile organelles that mediate key functions in
the photochemical utilization of light, sensing and signalling of environmental
stresses as well as elicitation and propagation of immune reactions against plant
pathogens. Light as an environmental factor therefore has a key impact on the
outcomes of biotic stress responses in plants [1,2]. Recent discoveries have
started to uncover the sequence of events that starts with the recognition of a
biotic stress agent in the extracellular space, proceeds through intracellular
signalling interactions and culminates in physiological defence responses in
infected tissues [3]. In this review, we elaborate on the role of chloroplasts as
a central metabolic and regulatory hub, which largely specifies the extent and
quality of defensive measures in plant cells.

2. Chloroplasts are targets for regulatory signals by both

the defender and the invader in plant immunity
Plants can sense the presence of biotic stress factors by recognizing their conserved
molecular patterns, which serve as ligands for plasma membrane receptor kinases
(figure 1). One of the best-characterized examples for the recognition of pathogenor microbe-associated molecular patterns (PAMPs or MAMPs) is the binding of
flg22, a conserved peptide of bacterial flagellin, by the receptor-like kinase FLS2
[4]. The recognition of an external factor initiates a convergent sequence of
events where the activation of the mitogen-activated protein kinase (MAPK) pathway is paralleled by changes in cytoplasmic calcium concentration, activation of

& 2014 The Author(s) Published by the Royal Society. All rights reserved.

2
tho

rstb.royalsocietypublishing.org

pa

ge

O2

FLS2

Ca2+

P
P

ROS
NADPH
oxidase

CDPKs

CAT2

PTI

effectors

ROS

SA
ROS
PsbQ

ROS

HopN1

HopI1
PsbQ

Avr
ROS

defence
genes
ETI
HR

Figure 1. Chloroplast as a central component in plant immunity. Recognition of conserved microbial patterns (PAMPs) by plasma membrane receptor kinases
launches the activation of mitogen-activated protein kinase (MAPK) cascades, formation of calcium transients, calcium-dependent protein kinases (CDPKs) and apoplastic reactive oxygen species (ROS) burst through NADPH oxidase activity. These initial signals trigger defence mechanisms collectively termed PAMP-triggered
immunity (PTI). Host-adapted pathogens secrete various effector molecules to suppress PTI, while plants can specifically recognize effectors and activate effectortriggered immunity (ETI), which culminates in the onset of the hypersensitivity response (HR). Biosynthesis of salicylic acid (SA) and ROS signalling in chloroplasts
are key components in plant immunity signalling. Photorespiratory production of ROS, controlled by peroxisomal catalase 2 (CAT2), further promotes these signalling
effects. Some pathogen effectors, such as HopI1 and HopL1, aim to suppress SA and/or ROS signalling by targeting specific chloroplastic functions.

calcium-dependent protein kinase (CDPK) cascades and rapid

NADPH oxidase-driven burst of reactive oxygen species (ROS)
in the apoplast. Together, these processes launch appropriate
defence responses in infected tissues [58]. The transient
early signalling events initiate mechanisms of PAMP-triggered
immunity (PTI) [9] and are followed by more persisting
changes occurring in organellar ROS metabolism, activation
of hormonal signalling, sealing of infected cells by callose
deposition into the cell wall and biosynthesis of antimicrobial
secondary metabolites [1014]. By combining different
means of defence, plants attempt to prevent the pathogens
and insect herbivores from colonizing the host tissue.
Two recent reports demonstrated that the recognition
of external factors might also be directly signalled between
the plasma membrane and chloroplasts. Nomura et al. [15]
showed that the application of flg22 on Arabidopsis leaves promotes the formation of calcium transients in chloroplasts and
that this response depends on the chloroplast CALCIUMSENSING RECEPTOR (CAS). Analysis of gene expression in
flg22-elicited leaves further revealed that CAS is required for

the downregulation of photosynthesis-related genes and

upregulation of defence genes in response to flg22 [15].
Subsequent work [16] reported that flg22 triggers the
downregulation of non-photochemical energy quenching in
chloroplasts, suggesting that controlled changes in the photoprotective mechanism represent an intrinsic component
among plants defence programmes. By using the air pollutant
ozone as a tool to mimic pathogen-induced ROS signalling
effects in guard cells, Vahisalu et al. [17] showed that a burst
of ROS in guard cell chloroplasts coincided with a rapid
decrease in stomatal conductance, a response that essentially
limits pathogen entry sites upon infection. Evidently, plants
have adopted an ability to deploy individual components of
the photosynthetic apparatus in triggering pathogen-induced
stomata closure and gene expression through light-dependent
photosynthetic processes [3,1517].
To combat the defence strategies of the plant, host-adapted
pathogens secrete various effector molecules that suppress or
circumvent plant immunity reactions, e.g. by directly targeting
components of the PTI (figure 1). Plants in turn have evolved

Phil. Trans. R. Soc. B 369: 20130235

MAPKs

3
P

th

og

en

retrograde
signalling

degradation
callose
deposition

Ind

Ind

S P

PAP

indolic GLS
biosynthesis

PAPS
P

PAPST

chloroplast

GSH

tryptophan

S P

cytosol

SA

cysteine
P

SAL1

AS

APK

ICS

SO32

chorismate

APR

S P

CS

APS

DAHP

ATPS

Trx

SO42

DAHP
synthase
erythrose 4-phosphate

phosphoenolpyruvate

Figure 2. Metabolic crosstalk in light acclimation and defence signalling. Shikimate pathway and sulfur assimilation are redox activated at 3-deoxy-D-arabino-heptulosonate 7-phosphate synthase (DAHP synthase), chorismate synthase (CS) and APS reductase (APR) upon photosynthetic electron transport in light. The shikimate
pathway provides precursors for SA and aromatic amino acids, of which tryptophan is used for biosynthesis of indolic glucosinolates (GLS). Rate-limiting steps in
these branches include isochorismate synthase (ICS) for SA and anthranilate synthase (AS) for tryptophan. Biosynthesis and sulfonylation of GLS requires glutathione
(GSH) and the sulfur donor 50 -phosphosulphate (PAPS). The reaction product phosphoadenosine 50 -phosphate (PAP) is a retrograde signalling molecule in high light
stress. Level of PAP is controlled by the chloroplastic phosphatase SAL1 and the PAPS transporter (PAPST). Degradation products of the indolic GLS act in parallel
with SA signalling to promote callose deposition to the cell wall. APS, adenosine 50 -phosphosulphate; ATPS, ATP sulphurylase; APK, APS kinase; APS, adenosine
phosphosulphate; Ind, indole; Glc, glucose.
systems to recognize the activities of pathogen effectors, which
trigger a process termed effector-triggered immunity (ETI) [9].
The hypersensitive response (HR), a hallmark of ETI characterized by cell death in the vicinity of the pathogen entry site,
relies on a burst of ROS in chloroplasts. It is, therefore, not surprising that bacterial effectors may directly target chloroplastic
functions. For example, the bacterial pathogen Pseudomonas
syringae secretes an effector molecule, HopI1, which alters the
structural organization of the thylakoid membranes and suppresses the accumulation of the stress hormone salicylic acid
(SA), thus negatively regulating SA-mediated defences [18].
Another Pseudomonas effector molecule, HopN1, annuls
ROS production in chloroplasts, thereby inhibiting callose
deposition and cell death in infected leaves [19]. HopN1 is a
cysteine protease that targets the PsbQ protein of the oxygenevolving complex and is therefore likely to mediate its effects
by deteriorating electron transport in photosystem II (PSII)
[19]. Requirement of intact PsbQ for full resistance against
Pseudomonas infection also speaks for the importance of

functional chloroplast electron transfer chain in defence

responses [19]. In this respect, it is intriguing that the PsbO1
and PsbP proteins rapidly increased in abundance upon
infection by avirulent (ETI-triggering) P. syringae expressing
the effector AvrRpm1 [20]. Thus, the oxygen-evolving complex seems to form a central component that modulates ROS
metabolism and cell death during an ETI.

3. Biosynthetic pathways of chloroplasts

contribute to defensive measures of plants
Organelles contribute to plant immunity also by hosting diverse
biosynthetic pathways, the reaction products of which carry out
important functions in stress resistance and signalling in plant
cells (figure 2). The isochorismate branch of the shikimate
pathway, for example, is the main source of SA in infected
leaves. The gene encoding ISOCHORISMATE SYNTHASE 1
(ICS1), the rate-limiting step in the biosynthesis of SA, is

Phil. Trans. R. Soc. B 369: 20130235

Glc
Glc
ON S
HO N S

rstb.royalsocietypublishing.org

pa
P

Photosynthesis is a key modulator of cellular redox metabolism and has far-reaching effects on the metabolic status
and stress tolerance of plants [3,29]. Photosynthetic activity
provides NADPH, ATP and carbon skeletons, which fuel
the initiation and maintenance of responses against external
stress factors. Sudden exposure of plants to high light intensity may cause different levels of light stress, which may
vary from the transient over-reduction of the photosynthetic
electron transfer chain and photoinhibition of PSII to irreversible ROS-induced damage to photosynthetic components. As
discussed below, these differentially harmful effects may
have completely different stress signalling effects in plant
cells. Formation of ROS, including superoxide and hydrogen
peroxide (O2  and H2O2, respectively), is in principle unavoidable in photosynthesis owing to the generation of
strongly reactive species during primary photochemistry. It
should be noted, however, that although the formation of
O2  and H2O2 is commonly associated with photosystem I
(PSI) activity, recent reports have questioned the role of PSI
electron transfer to molecular oxygen as a main source of
ROS in higher plants [30,31]. Imbalanced electron transfer
reactions may also lead to the formation of singlet oxygen
(1O2) in PSII [32,33]. However, chloroplasts are well equipped
with a multitude of overlapping antioxidant systems, which
maintain ROS below dangerous levels for the cells.
Even though harsh redox modifications may have deleterious effects on photosynthetic activity [34], the accumulation
of redox-active intermediates and/or ROS becomes beneficial
in terms of signalling effects against different types of stress,
including high light and pathogens [35]. Recent work done
with green algae has suggested a possible mechanism
explaining this tight relationship. Expression of a nuclearencoded reporter gene coupled to a H2O2 sensitive promoter
was shown to respond not only to the levels of exogenously
added H2O2 but also to light-induced photosynthetic electron
transfer, its transcriptional activation correlating with a lower
intracellular H2O2 scavenging activity [36]. This suggests that

5. Interplay between apoplastic and chloroplastic

reactive oxygen species signalling impacts
on light acclimation, disease resistance and
plant development
Light-induced ROS signalling effects may also arise as a result
of crosstalk between different cellular compartments. In the
plasma membrane, NADPH oxidases transfer electrons from
NADPH to oxygen, leading to the generation of superoxide
and hydrogen peroxide in the apoplast [41]. The activation of
the NADPH oxidase, which mediates the progression of ROS
signals from cell to cell in a ROS wave, is now known to be
mediated by CDPK 5 [42,43]. Through yet unknown mechanisms, NADPH oxidase-dependent apoplastic ROS burst also
triggers ROS production in chloroplasts [15,44]. This is structurally feasible, because under high light chloroplasts adopt

Phil. Trans. R. Soc. B 369: 20130235

4. Light-induced reactive oxygen species signals

trigger a genetically encoded cell death
pathway in plant immunity

enhanced H2O2 production in the light should reflect a transient inactivation of the ROS scavenging processes rather
than an increased H2O2 production, possibly to trigger
specific ROS signalling responses within the cell.
How are ROS signals translated into physiological
responses? Using Arabidopsis as a model organism, Lee et al.
[37] have demonstrated the existence of genetic determinants
that control ROS signalling. Starting from the Arabidopsis flu
mutant, which accumulates the chlorophyll precursor protochlorophyllide in the dark (and therefore shows enhanced
1
O2 accumulation upon re-illumination), the authors selected
and characterized second site suppressors. This led to the isolation of EXECUTERS 1 and 2, two chloroplast-targeted and
thylakoid-bound proteins, which control 1O2 responses [37].
A comparative global analysis of transcript changes upon
light exposure of dark-adapted Arabidopsis wild-type and
mutant plants showed that the FLU-mediated 1O2 signalling
pathway is similar to the general stress response induced by
pathogen attack, wounding or high light and drought stress.
Moreover, the fact that the flu phenotype is conditioned by
the presence of EXECUTER proteins demonstrates that the
pathway is genetically determined. More recently, another
essential piece of information on ROS signal transduction has
been provided by the finding that ROS-related pathogen
responses occur via Ca2 signalling, via the activity of the
chloroplast CAS [15]. However, the molecular mechanisms
relating ROS, pathogen defence response and CAS are still
largely undetermined.
In contrast to the large number of Arabidopsis mutants that
display enhanced cell death upon increasing irradiance levels
[38], a knockdown mutant deficient in a specific cytosolic regulatory B0 g subunit of the trimeric protein phosphatase 2A
(PP2A-B0 g) shows a constitutive pathogenesis response and premature leaf yellowing under moderate light intensity, whereas
high light partially rescues the phenotype [39]. The pp2a-b 0 g
mutant shows disintegration of chloroplasts and accumulation
of H2O2 in the leaf mesophyll cells even in visually healthy
leaves [39]. The disintegration of chloroplasts in pp2a-b 0 g precedes the degradation of other cellular components and in this
respect resembles the early steps of singlet oxygen-induced programmed cell death of the flu mutant [40]. PP2A-B0 g therefore
has a role in the crosstalk between defence and light acclimation,
and is likely to control cytoplasmic components that respond to
organellar signals [39].

rstb.royalsocietypublishing.org

transcriptionally regulated and becomes activated in response to

infection [21,22]. The shikimate pathway also serves the biosynthesis of aromatic amino acids, which are precursors for the
biosynthesis of indolic and phenolic secondary metabolites,
and has been estimated to consume at least 30% of photosynthetically fixed carbon [23]. Indolic glucosinolates (GLS) derive
from tryptophan and provide an intricate example of metabolic
connections between chloroplast signalling and defence mechanisms in plants (figure 2). In Brassicaceae, the biosynthesis of
the sulfur-rich GLS is linked to the universal sulfate donor phosphoadenosine 50 -phosphosulphate (PAPS), whose by-product
phosphoadenosine 50 -phosphate (PAP) has been shown to mediate retrograde signals from chloroplast to nucleus under high
light stress [2426]. As sulfur metabolism is regulated by
photosynthesis-driven redox chemistry [27], a link between the
biosynthesis of these secondary compounds and light-mediated
signalling seems evident [28]. Moreover, degradation products
of the indolic GLS have also been shown to act in parallel with
SA signalling to promote callose deposition to the cell wall [14].

Acknowledgements. Guido Durian is acknowledged for critical comments on the manuscript.

Funding statement. This work was supported by Academy of Finland
projects 263772, 218157, 259888 and 130595 for S.K., Finnish Graduate Program in Plant Biology for G.K. G.F. was supported by the
investissement davenir projet GRAL and ITN accliphot (grant
agreement number 316427).

References
1.

2.

3.

4.

5.

6.

7.

8.

Muhlenbock P, Szechynska-Hebda M, Plaszczyca M,

Baudo M, Mateo A, Mullineaux PM, Parker JE,
Karpinska B, Karpinski S. 2008 Chloroplast signaling
and LESION SIMULATING DISEASE1 regulate crosstalk
between light acclimation and immunity in
Arabidopsis. Plant Cell 20, 2339 2356. (doi:10.
1105/tpc.108.059618)
Kangasjarvi S, Neukermans J, Li S, Aro EM, Noctor G.
2012 Photosynthesis, photorespiration, and light
signalling in defence responses. J. Exp. Bot. 63,
16191636. (doi:10.1093/jxb/err402)
Sierla M, Rahikainen M, Salojarvi J, Kangasjarvi J,
Kangasjarvi S. 2013 Apoplastic and chloroplastic
redox signaling networks in plant stress responses.
Antioxid. Redox Signal. 18, 2220 2239. (doi:10.
1089/ars.2012.5016)
Chinchilla D, Bauer Z, Regenass M, Boller T, Felix G.
2006 The Arabidopsis receptor kinase FLS2 binds
flg22 and determines the specificity of flagellin
perception. Plant Cell 18, 465476. (doi:10.1105/
tpc.105.036574)
Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL,
Gomez-Gomez L, Boller T, Ausubel FM, Sheen J.
2002 MAP kinase signalling cascade in Arabidopsis
innate immunity. Nature 415, 977983. (doi:10.
1038/415977a)
Torres MA, Dangl JL. 2005 Functions of the
respiratory burst oxidase in biotic interactions,
abiotic stress and development. Curr. Opin. Plant
Biol. 8, 397403. (doi:10.1016/j.pbi.2005.05.014)
Gao M, Liu J, Bi D, Zhang Z, Cheng F, Chen S, Zhang
Y. 2008 MEKK1, MKK1/MKK2 and MPK4 function
together in a mitogen-activated protein kinase
cascade to regulate innate immunity in plants. Cell
Res. 18, 1190 1198. (doi:10.1038/cr.2008.300)
Boudsocq M, Willmann MR, McCormack M, Lee H,
Shan L, He P, Bush J, Cheng SH, Sheen J. 2010
Differential innate immune signalling via Ca2

9.

10.

11.

12.

13.

14.

15.

16.

17.

sensor protein kinases. Nature 464, 418 422.

(doi:10.1038/nature08794)
Jones JD, Dangl JL. 2006 The plant immune
system. Nature 444, 323329. (doi:10.1038/
nature05286)
Tena G, Asai T, Chiu WL, Sheen J. 2001 Plant
mitogen-activated protein kinase signaling cascades.
Curr. Opin. Plant Biol. 4, 392400. (doi:10.1016/
S1369-5266(00)00191-6)
Glawischnig E. 2007 Camalexin. Phytochemistry
68, 401 406. (doi:10.1016/j.phytochem.2006.
12.005)
Qiu JL et al. 2008 Arabidopsis MAP kinase 4
regulates gene expression through transcription
factor release in the nucleus. EMBO J. 27,
2214 2221. (doi:10.1038/emboj.2008.147)
Bednarek P et al. 2009 A glucosinolate metabolism
pathway in living plant cells mediates broadspectrum antifungal defense. Science 323,
101 106. (doi:10.1126/science.1163732)
Clay NK, Adio AM, Denoux C, Jander G, Ausubel FM.
2009 Glucosinolate metabolites required for an
Arabidopsis innate immune response. Science 323,
95 101. (doi:10.1126/science.1164627)
Nomura H et al. 2012 Chloroplast-mediated
activation of plant immune signalling in
Arabidopsis. Nat. Commun. 3, 926. (doi:10.1038/
ncomms1926)
Gohre V, Jones AM, Sklenar J, Robatzek S, Weber AP.
2012 Molecular crosstalk between PAMP-triggered
immunity and photosynthesis. Mol. Plant Microbe
Interact. 25, 10831092. (doi:10.1094/MPMI-1111-0301)
Vahisalu T et al. 2010 Ozone-triggered rapid
stomatal response involves the production of
reactive oxygen species, and is controlled by SLAC1
and OST1. Plant J. 62, 442 453. (doi:10.1111/j.
1365-313X.2010.04159.x)

18. Jelenska J, Yao N, Vinatzer BA, Wright CM, Brodsky

JL, Greenberg JT. 2007 A J domain virulence effector
of Pseudomonas syringae remodels host chloroplasts
and suppresses defenses. Curr. Biol. 17, 499508.
(doi:10.1016/j.cub.2007.02.028)
19. Rodrguez-Herva JJ et al. 2012 A bacterial cysteine
protease effector protein interferes with
photosynthesis to suppress plant innate immune
responses. Cell Microbiol. 14, 669 681. (doi:10.
1111/j.1462-5822.2012.01749.x)
20. Jones AM, Thomas V, Bennett MH, Mansfield J,
Grant M. 2006 Modifications to the Arabidopsis
defense proteome occur prior to significant
transcriptional change in response to inoculation
with Pseudomonas syringae. Plant Physiol. 142,
1603 1620. (doi:10.1104/pp.106.086231)
21. Wildermuth MC, Dewdney J, Wu G, Ausubel FM.
2001 Isochorismate synthase is required to
synthesize salicylic acid for plant defence. Nature
414, 562565. (doi:10.1038/35107108)
22. Chaouch S, Queval G, Vanderauwera S, Mhamdi A,
Vandorpe M, Langlois-Meurinne M, Van Breusegem
F, Saindrenan P, Noctor G. 2010 Peroxisomal
hydrogen peroxide is coupled to biotic defense
responses by ISOCHORISMATE SYNTHASE1 in a
daylength-related manner. Plant Physiol. 153,
1692 1705. (doi:10.1104/pp.110.153957)
23. Maeda H, Dudareva N. 2012 The shikimate pathway
and aromatic amino acid biosynthesis in plants.
Annu. Rev. Plant Biol. 63, 73 105. (doi:10.1146/
annurev-arplant-042811-105439)
24. Estavillo GM et al. 2011 Evidence for a SAL1-PAP
chloroplast retrograde pathway that functions in
drought and high light signaling in Arabidopsis.
Plant Cell 23, 39924012. (doi:10.1105/tpc.
111.091033)
25. Lee BR et al. 2012 Effects of fou8/fry1 mutation on
sulfur metabolism: is decreased internal sulfate the

Phil. Trans. R. Soc. B 369: 20130235

interconnect photoperiodic growth, amino acid homoeostasis

and ROS signalling in Arabidopsis leaves [48,50,51]. Indeed,
the photoperiod is emerging as a key environmental factor
that modulates plant responses to organellar ROS signals
[2,22,48,5256].
In conclusion, plant biotic interactions are under multifaceted influence of light, which exerts its effects through
light-intensity-dependent photosynthetic processes, as well
as mechanisms that may respond to the quality and duration
of light [2]. Understanding the complex molecular crosstalk
in environmental light signalling will be highly relevant in
efforts to enhance the stress tolerance of plants for sustainable
productivity in the future.

rstb.royalsocietypublishing.org

a position adjacent to the plasma membrane, thus allowing

efficient communication.
A key role for the chloroplast envelope in cellular signalling has also recently become evident [45,46]. For example,
Arabidopsis reticulata (re) mutants, deficient in a transmembrane protein of the chloroplast inner envelope, exhibit
reticulated leaf pigmentation and constitutive accumulation
of ROS along leaf veins conditionally under long day conditions [47,48]. The re mutants also show enhanced cell
death in response to apoplastic ROS signals when exposed
to ozone fumigation under moderately high light intensity
[48,49]. Thus, the interplay between apoplastic and chloroplastic ROS signalling cascades seems to enhance cell death
initiation in re leaves.
Despite their imbalanced ROS metabolism, re mutants
display a decreased expression of SA signalling markers, a
response attributed to imbalanced amino acid homoeostasis
and a consequent inability to synthesize SA through the
ICS1-dependent pathway [48]. These characteristics position
RE in a regulatory network, which seems to functionally

27.

29.

30.

31.

32.

33.

34.

35.

36.

48.

49.

50.

51.

52.

53.

54.

55.

56.

organ shape in Arabidopsis leaves. J. Exp. Bot. 57,

3019 3031. (doi:10.1093/jxb/erl063)
Perez-Perez JM, Esteve-Bruna D, Gonzalez-Bayon R,
Kangasjarvi S, Caldana C, Hannah MA, Willmitzer L,
Ponce MR, Micol JL. 2013 Functional redundancy
and divergence within the Arabidopsis RETICULATARELATED gene family. Plant Physiol. 162, 589 603.
(doi:10.1104/pp.113.217323)
Overmyer K et al. 2008 Complex phenotypic profiles
leading to ozone sensitivity in Arabidopsis thaliana
mutants. Plant Cell Environ. 31, 12371249.
(doi:10.1111/j.1365-3040.2008.01837.x)
Lepisto A, Kangasjarvi S, Luomala EM, Brader G,
Sipari N, Keranen M, Keinanen M, Rintamaki E.
2009 Chloroplast NADPH-thioredoxin reductase
interacts with photoperiodic development in
Arabidopsis. Plant Physiol. 149, 12611276.
(doi:10.1104/pp.108.133777)
Diaz Vivancos P, Wolff T, Markovic J, Pallardo FV,
Foyer CH. 2010 A nuclear glutathione cycle within
the cell cycle. Biochem. J. 431, 169178. (doi:10.
1042/BJ20100409)
Bechtold U, Richard O, Zamboni A, Gapper C, Geisler
M, Pogson B, Karpinski S, Mullineaux PM. 2008
Impact of chloroplastic- and extracellular-sourced
ROS on high light-responsive gene expression in
Arabidopsis. J. Exp. Bot. 59, 121133. (doi:10.1093/
jxb/erm289)
Becker B, Holtgrefe S, Jung S, Wunrau C,
Kandlbinder A, Baier M, Dietz KJ, Backhausen JE,
Scheibe R. 2006 Influence of the photoperiod on
redox regulation and stress responses in Arabidopsis
thaliana L. (Heynh.) plants under long- and shortday conditions. Planta 224, 380393. (doi:10.
1007/s00425-006-0222-3)
Queval G, Issakidis-Bourguet E, Hoeberichts FA,
Vandorpe M, Gakie`re B, Vanacker H, MiginiacMaslow M, Van Breusegem F, Noctor G. 2007
Conditional oxidative stress responses in the
Arabidopsis photorespiratory mutant cat2
demonstrate that redox state is a key modulator of
daylength-dependent gene expression, and define
photoperiod as a crucial factor in the regulation of
H2O2-induced cell death. Plant J. 52, 640 657.
(doi:10.1111/j.1365-313X.2007.03263.x)
Queval G, Neukermans J, Vanderauwera S, Van
Breusegem F, Noctor G. 2012 Day length is a key
regulator of transcriptomic responses to both CO2
and H2O2 in Arabidopsis. Plant Cell Environ. 35,
374387. (doi:10.1111/j.1365-3040.2011.02368.x)
Michelet L, Krieger-Liszkay A. 2012 Reactive oxygen
intermediates produced by photosynthetic electron
transport are enhanced in short-day grown plants.
Biochim. Biophys. Acta 1817, 13061313. (doi:10.
1016/j.bbabio.2011.11.014)

Phil. Trans. R. Soc. B 369: 20130235

28.

37. Lee KP, Kim C, Landgraf F, Apel K. 2007 EXECUTER1and EXECUTER2-dependent transfer of stress-related
signals from the plastid to the nucleus of
Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 104,
10 270 10 275. (doi:10.1073/pnas.0702061104)
38. Lorrain S, Vailleau F, Balague C, Roby D. 2003 Lesion
mimic mutants: keys for deciphering cell death and
defense pathways in plants? Trends Plant Sci. 8,
263271. (doi:10.1016/S1360-1385(03) 00108-0)
39. Trotta A et al. 2011 Regulatory subunit B0 g of
protein phosphatase 2A prevents unnecessary
defense reactions under low light in Arabidopsis.
Plant Physiol. 156, 14641480. (doi:10.1104/pp.
111.178442)
40. Kim C, Meskauskiene R, Zhang S, Lee KP,
Lakshmanan Ashok M, Blajecka K, Herrfurth C,
Feussner I, Apel K. 2012 Chloroplasts of Arabidopsis
are the source and a primary target of a plantspecific programmed cell death signaling pathway.
Plant Cell 24, 30263039. (doi:10.1105/tpc.
112.100479)
41. Sagi M, Fluhr R. 2006 Production of reactive
oxygen species by plant NADPH oxidases.
Plant Physiol. 141, 336 340. (doi:10.1104/
pp.106.078089)
42. Miller G, Schlauch K, Tam R, Cortes D,
Torres MA, Shulaev V, Dangl JL, Mittler R.
2009 The plant NADPH oxidase RBOHD mediates
rapid systemic signaling in response to diverse
stimuli. Sci. Signal. 2, ra45. (doi:10.1126/
scisignal.2000448)
43. Dubiella U, Seybold H, Durian G, Komander E, Lassig
R, Witte CP, Schulze WX, Romeis T. 2013 Calciumdependent protein kinase/NADPH oxidase activation
circuit is required for rapid defense signal
propagation. Proc. Natl Acad. Sci. USA 110,
8744 8749. (doi:10.1073/pnas.1221294110)
44. Joo JH, Wang S, Chen JG, Jones AM, Fedoroff NV.
2005 Different signaling and cell death roles of
heterotrimeric G protein alpha and beta subunits
in the Arabidopsis oxidative stress response to
ozone. Plant Cell 17, 957970. (doi:10.1105/tpc.
104.029603)
45. Sun X, Feng P, Xu X, Guo H, Ma J, Chi W, Lin R, Lu
C, Zhang L. 2011 A chloroplast envelope-bound PHD
transcription factor mediates chloroplast signals to
the nucleus. Nat. Commun. 2, 477. (doi:10.1038/
ncomms1486)
46. Furumoto T et al. 2011 A plastidial sodiumdependent pyruvate transporter. Nature 476,
472 475. (doi:10.1038/nature10250)
47. Gonzalez-Bayon R, Kinsman EA, Quesada V, Vera A,
Robles P, Ponce MR, Pyke KA, Micol JL. 2006
Mutations in the RETICULATA gene dramatically alter
internal architecture but have little effect on overall

rstb.royalsocietypublishing.org

26.

trigger of sulfate starvation response? PLoS ONE 7,

e39425. (doi:10.1371/journal.pone.0039425)
Gigolashvili T et al. 2012 The Arabidopsis thylakoid
ADP/ATP carrier TAAC has an additional role
in supplying plastidic phosphoadenosine
50 -phosphosulfate to the cytosol. Plant Cell 24,
41874204. (doi:10.1105/tpc.112.101964)
Huseby S, Koprivova A, Lee BR, Saha S, Mithen R,
Wold AB, Bengtsson GB, Kopriva S. 2013 Diurnal
and light regulation of sulphur assimilation and
glucosinolate biosynthesis in Arabidopsis. J. Exp.
Bot. 64, 1039 1048. (doi:10.1093/jxb/ers378)
Chan KX, Wirtz M, Phua SY, Estavillo GM, Pogson BJ.
2013 Balancing metabolites in drought: the sulfur
assimilation conundrum. Trends Plant Sci. 18,
18 29. (doi:10.1016/j.tplants.2012.07.005)
Foyer CH, Noctor G. 2009 Redox regulation in
photosynthetic organisms: signaling, acclimation,
and practical implications. Antioxid. Redox Signal.
11, 861905. (doi:10.1089/ars.2008.2177)
Driever SM, Baker NR. 2011 The water water cycle
in leaves is not a major alternative electron sink for
dissipation of excess excitation energy when CO2
assimilation is restricted. Plant Cell Environ. 34,
837846. (doi:10.1111/j.1365-3040.2011.02288.x)
Badger MR, von Caemmerer S, Ruuska S, Nakano H.
2000 Electron flow to oxygen in higher plants and
algae: rates and control of direct photoreduction
(Mehler reaction) and rubisco oxygenase. Phil.
Trans. R. Soc. Lond. B 355, 1433 1446. (doi:10.
1098/rstb.2000.0704)
Hideg E, Kalai T, Hideg K, Vass I. 1998
Photoinhibition of photosynthesis in vivo results in
singlet oxygen production detection via nitroxideinduced fluorescence quenching in broad bean
leaves. Biochemistry 37, 11 405 11 411. (doi:10.
1021/bi972890+)
Macpherson AN, Telfer A, Truscott TG, Barber J.
1993 Direct detection of singlet oxygen from
isolated photosystem II reaction centres. Biochim.
Biophys. Acta 1143, 301309. (doi:10.1016/00052728(93)90201-P)
Barber J, Andersson B. 1992 Too much of a good
thing: light can be bad for photosynthesis. Trends
Biochem. Sci. 17, 61 66. (doi:10.1016/09680004(92)90503-2)
Karpinski S, Gabrys H, Mateo A, Karpinska B,
Mullineaux PM. 2003 Light perception in plant
disease defence signalling. Curr. Opin. Plant Biol. 6,
390396. (doi:10.1016/S1369-5266(03)00061-X)
Shao N, Beck CF, Lemaire SD, Krieger-Liszkay A.
2008 Photosynthetic electron flow affects H2O2
signaling by inactivation of catalase in
Chlamydomonas reinhardtii. Planta 228,
10551066. (doi:10.1007/s00425-008-0807-0)