Retrograde signaling and plant stress: plastid signals initiate cellular stress responses

Available online at www.sciencedirect.com

Retrograde signaling and plant stress: plastid signals initiatecellular stress responsesAurora Pinas Fernandez and Asa Strand

Retrograde signaling coordinates the expression of nuclear

genes encoding organellar proteins with the metabolic and

developmental state of the organelle. These plastid signals are

essential not only for coordinating photosynthetic gene

expression in both the nucleus and in the chloroplasts but also

for mediating plant stress responses. The chloroplasts

therefore act as sensors of environmental changes and

complex networks of plastid signals coordinate cellular

activities and assist the cell during plant stress responses.

Recent work suggests that information from both cytosolic-

signaling and plastid-signaling networks must be integrated for

the plant cell to respond optimally to environmental stress.

Addresses

Umea Plant Science Centre, Department of Plant Physiology, Umea

University, S-901 87 Umea, Sweden

Corresponding author: Fernandez, Aurora Pinas (aurora.pinas-

[email protected]) and Strand, Asa ([email protected])

Current Opinion in Plant Biology 2008, 11:509–513

This review comes from a themed issue on

Cell Signalling and Gene Regulation

Edited by Jason Reed and Bonnie Bartel

Available online 17th July 2008

1369-5266/$ – see front matter

# 2008 Elsevier Ltd. All rights reserved.

DOI 10.1016/j.pbi.2008.06.002

IntroductionThe presence of genes encoding organellar proteins in

different cellular compartments of the plant cell creates a

complex problem in coordinating the activities of the

different genomes [1–3]. In order to achieve this coordi-

nation, retrograde (organelles-to-nucleus) control has

evolved [3]. Retrograde communication coordinates the

expression of nuclear genes encoding organellar proteins

with the metabolic and developmental state of the plastid

and mitochondria [4] through signals emitted from the

organelles that regulate nuclear gene expression. It is now

clear that several different plastid processes produce

these signals [2,5,6] and that plastid to nucleus communi-

cation appears to be of particular importance during plant

stress responses. The plastid signals identified so far can

be linked to specific stress conditions. The photosyn-

thetic reactions housed in the chloroplasts are extremely

sensitive to stress [7] and the chloroplasts could therefore

play a crucial role as sensors of changes in the growth

www.sciencedirect.com

environment [8��]. This review will focus on the plastid

processes shown to produce signals influencing nuclear

gene expression during different stress conditions: firstly,

changes of the redox state of the chloroplast; secondly,

accumulation of reactive oxygen species (ROSs); and

thirdly, accumulation of tetrapyrroles.

Chloroplast redox signals communicatephotosynthetic activityIt was established several years ago that the redox state of

one of the electron carriers, plastoquinone (PQ), influ-

ences the expression of photosynthetic genes encoded

both in the chloroplast and in the nucleus [9–11]. How-

ever, subsequent detailed analysis in cyanobacteria [12]

and higher plants [13–14] demonstrated that very few

nuclear-encoded genes were regulated directly by the

reduction state of PQ. In experiments combining light

shifts with an inhibitor that blocks the flow of electrons

from PSII to PQ, leaving the PQ pool oxidized in the

light, only 54 Arabidopsis genes were shown to be ‘ideal

redox regulated genes’ [13]. Only 2 of those 54 genes,

encoded components directly associated with photosyn-

thesis strongly suggesting that the reduction state of PQ

does not modulate expression of nuclear-encoded photo-

synthesis genes and thus, the redox state of the PQ pool is

not the major source of the chloroplast-to-nucleus com-

munication during fluctuating light conditions. Further-

more, a different study where the redox state of the PQ

pool was modulated using wavelengths of light that pre-

ferentially excited either PSII or PSI showed that

elements on the reducing side of PSI were of greater

importance in light-regulated modulation of nuclear gene

expression than was the redox state of PQ [14]. In

addition, the CO2-fixation rate was demonstrated to

influence the expression of nuclear-encoded photosyn-

thesis-related genes, suggesting that the metabolic

activity of the chloroplast could also be a source of plastid

signals [14]. Thus, the more recent work suggests that

rather than the reduction state of the PQ itself, the

generation of metabolites or signaling molecules during

photosynthesis is more likely to be involved in the relay of

information from chloroplasts to the nucleus. This new

model is attractive because the redox state of the down

stream components of the photosynthetic electron trans-

port chain are tightly linked to the energy balance of the

cell.

The actual mechanism(s) of how the plant cell can convey

the changes in redox status or energy balance of the

chloroplast to the nucleus is(are) still unknown. However,

a small LuxR-type regulator in Synechocystis, photosynthetic


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http://dx.doi.org/10.1016/j.pbi.2008.06.002

510 Cell Signalling and Gene Regulation

electron transport-dependent regulation (PedR), was

suggested to work as a sensor for the availability of reducing

equivalents supplied from the photosynthetic electron

transport chain [15]. Furthermore, a unique light and

redox-controlled protein phosphorylation system has

evolved in plant thylakoid membranes [16]. The thylakoid

protein kinase STN7 is required for state transitions

and photosynthetic acclimation [17,18]. In addition, the

stn7 mutant demonstrated differential expression of

nuclear-encoded photosynthetic genes compared to wild

type [18]. Possibly STN7 participates in the implementa-

tion of the redox signal from the chloroplast to the nucleus

(Figure 1). The first true redox imbalanced mutants (rimb)

have been described [19�] and in the rimb mutants, the

expression of the nuclear gene encoding the antioxidant

Figure 1

A working model for plastid-to-nucleus communication during stress respon

state of PQ or via elements on the reducing side of PSI. Possibly the thylak

chloroplast to the nucleus. H2O2 and 1O2 accumulate during exposure to exce

the chloroplast is sensed or mediated to the nucleus via a concerted action o

nucleus the blue light photoreceptor cry1 is involved in the 1O2-mediated st

under stress conditions and its accumulation triggers large changes in the nu

within the plastids, either to generate or transmit a common plastid signal to

factor ABI4 prevents the binding of factors required for light-induced expres


enzyme 2-cys-peroxiredoxin, 2-CPA, is uncoupled from

the redox state of the PSI acceptor side. Cloning of

the RIMB genes could provide a breakthrough in our

understanding of the redox-mediated retrograde-signaling

pathway(s).

Reactive oxygen species accumulate underexposure to excess lightWhen photon fluence exceeds the photon utilization

capacity of the chloroplast, the production of ROSs, such

as superoxide, O2��, hydrogen peroxide, H2O2, and sing-

let oxygen, 1O2, increases [20,21]. Although the different

forms of ROS cause similar cellular damages [22], the

different ROS activate distinct signaling pathways [23].

In addition, plants lacking chloroplastic and cytosolic

ses in higher plants. Redox signals are mediated through the reduction

oid protein kinase STN7 convey the changes in redox status of the

ss light and activate distinct signaling pathways. The 1O2 accumulated in

f two chloroplast proteins EXECUTER1 and EXECUTER2. In the cytosol/

ress response. The tetrapyrrole Mg-ProtoIX accumulates in the cytosol

clear transcriptome. The GUN1 protein integrates several plastid signals

the nucleus. In response to the GUN1-derived signal, the transcription

sion of nuclear-encoded photosynthesis genes.


Plant stress and plastid signals Fernandez and Strand 511

hydrogen peroxide removal enzymes trigger different

signals [24] suggesting that the cellular source of ROS

is also crucial. A specific function for 1O2 in retrograde

communication was discovered by the conditional fluor-

escent mutant, flu, of Arabidopsis [25,26]. The release of1O2 primarily activates genes encoding components

involved in cell death and less than 15% of the 1O2-

responsive genes are predicted to encode plastid proteins

[27,28]. Thus, the 1O2-mediated pathway may be prim-

arily used for general stress responses rather than genome

coordination. Transcriptome analysis using the flu mutant

and the herbicide paraquat demonstrated that 1O2 acti-

vates a distinct set of genes that is different from that

induced by superoxide (O2��), and/or H2O2. In addition,

it was demonstrated that H2O2 antagonizes the 1O2-

mediated stress responses observed in the flu mutant.

This crosstalk between H2O2-dependent and 1O2-de-

pendent signaling pathways may contribute to the fine-

tuning of the response to environmental stresses [23].

The 1O2 has a very short half-life (200 ns) [29],

suggesting that the singlet oxygen-derived plastid signal

must exit the chloroplast in a different form. EXE-

CUTER1 (EX1) and EXECUTER2 (EX2) are two

chloroplast-localized proteins identified through a muta-

tional suppressor screen for flu suppressor mutants that

potentially could act as sensors and/or mediators of 1O2

accumulation in the chloroplast [8��] (Figure 1). The

EX1 and EX2 proteins are unrelated to known proteins

but highly conserved homologs of the EX proteins have

been found in all higher plants for which sequence data

are available [8��]. The EX1 and EX2 proteins are

suggested to be associated with the thylakoid membrane

and thus would be in close vicinity to the production sites

of 1O2 [8��]. The ex1 flu double mutant over accumulates1O2 but abrogates the stress responses of the flu mutant.

Although, inactivation of the EX1 gene in the flu mutant

background was not sufficient to fully suppress 1O2-

induced changes in nuclear gene expression, inactivation

of both EX1/2 proteins in the ex1 ex2 flu triple mutant did

fully suppress the 1O2-induced genes, suggesting that

the singlet oxygen-derived plastid signal requires con-

certed action of both EX1 and EX2 [8��]. Interestingly,

the blue light photoreceptor, cry1, is involved in the1O2-mediated stress response (Figure 1). In the flu cry1double mutant, the plant cell death response was lost

[30]. In addition, new cry1 alleles were isolated as

genome-uncoupled mutants and in response to an

unknown plastid signal, cry1 becomes a negative regu-

lator of LHCB expression when this plastid signal

converts the transcription factor HY5 from a positive

to a negative regulator of LHCB [31�]. This finding

indicates that plastid signals interact and converge with

the light-signaling networks, which has also been indi-

cated by the finding that cis-elements responding to light

and plastid signals cannot be separated from each other

[32��,33,34].


Tetrapyrroles, indicators of metabolicimbalance in the chloroplastsThere is clear genetic and biochemical evidence for a role

of tetrapyrroles in communication between the chloro-

plast and the nucleus in both green algae and higher

plants [5,33,35]. Arabidopsis mutants where the communi-

cation between the chloroplast and the nucleus has been

disrupted were identified in the laboratory of Joanne

Chory and referred to as the genome-uncoupled mutants,

or gun mutants [4]. Five mutants were identified (gun1–5)

that express nuclear-encoded photosynthetic genes in the

absence of proper chloroplast development [4]. Analysis

of the genome-uncoupled mutants, gun2 and gun5, with

restrictions in defined steps in tetrapyrrole biosynthesis

provided evidence that accumulation of the chlorophyll

intermediate Mg-protoporphyrinIX (Mg-ProtoIX)

initiates retrograde communication between the chloro-

plast and the nucleus [33]. Mg-ProtoIX acts as a negative

regulator of photosynthetic gene expression in the

nucleus and in the chloroplast [36�]. Similar to the

nuclear-encoded photosynthesis genes, expression of

the plastid-encoded RNA-polymerase (PEP)-dependent

photosynthesis genes psbA, psbD, psaA, psaC, and rbcL was

mis-regulated following norflurazon treatment in the Mg-

ProtoIX-under accumulator, gun5 [36�]. Thus, in addition

to exerting control over nuclear-encoded photosynthesis

genes, Mg-ProtoIX also affects the expression of the

plastid-encoded photosynthesis genes by controlling

the expression of the sigma factors necessary for the

function of the multi-subunit enzyme PEP [36�]. Mg-

ProtoIX has been shown to accumulate under stress

conditions such as treatment with the herbicide norflur-

azon or exposure to low temperature [33,37] (Strand A,

unpublished) and thus acts as an indicator of metabolic

imbalance in the chloroplast. Further support for Mg-

ProtoIX as a signaling metabolite was provided from

transgenic tobacco plants with either overexpression or

underexpression of CHLM, the gene encoding Mg-Pro-

toIX methyl transferase, that contained either lower or

increased pool levels of Mg-ProtoIX, which correlated

with either elevated or reduced expression of nuclear-

encoded photosynthesis genes [38]. In addition, an Ara-bidopsis mutant that accumulates Mg-ProtoIX due to a T-

DNA insertion in CHLM showed repression of the

nuclear-encoded LHCB gene in the absence of norflur-

azon [39].

In the green alga Chlamydomonas reinhardtii, it was recently

demonstrated that both tetrapyrroles Heme and Mg-Pro-

toIX could act as plastid signals inducing the nuclear-

encoded HSP70A [40�]. Analysis of the HSP70A promoter

uncovered the plastid response element PRE [34] and the

activation of HSP70A expression by Heme or Mg-ProtoIX

was mediated by the same PRE, suggesting that these two

tetrapyrroles supply the same signaling pathway [40�].Tetrapyrroles are synthesized in the chloroplast and must

exit the chloroplast to act as plastid signals. In Arabidopsis,


512 Cell Signalling and Gene Regulation

Mg-ProtoIX could be visualized in the cells using confocal

laser-scanning spectroscopy and the fluorescence images

obtained demonstrated that Mg-ProtoIX accumulated in

the cytosol during stress conditions [36�]. The relative

cytoplasmic accumulation of Mg-ProtoIX was greater in

cotyledons, compared to hypocotyls, suggesting that the

export mechanisms is more active in leaf tissue and that the

export of tetrapyrroles is an active and regulated process.

Supporting this conclusion, Beck and colleagues demon-

strated in Chlamydomonas that expression of HSP70 was not

induced when the cells were fed the precursor ProtoIX in

the dark, with resulting accumulation of Mg-ProtoIX in the

plastids [41]. These data suggest that the plastid export

mechanism for Mg-ProtoIX is light regulated. However,

describing the mechanism used for transport of tetrapyr-

roles across the envelope membrane is a challenge for the

future.

Plastid signals converge upstream of GUN1and ABI4The last of the GUN genes, GUN1, was recently cloned and

found to encode a chloroplast-localized pentatricopeptide-

repeat (PPR) containing protein [32��]. In contrast to the

other gun mutants, gun1 is affected in the redox-mediated,

the Mg-ProtoIX-mediated, and the organellar gene expres-

sion mediated pathways. The genome-uncoupled pheno-

type observed under such a wide range of stress conditions

in the gun1 mutant indicated that several plastid signals are

integrated within the plastids, and GUN1 is required to

either generate or transmit a second, common signal to the

nucleus [32��]. However, treatment with norflurazon and

resulting accumulation of Mg-ProtoIX was demonstrated

to also affect the transcription of PEP-dependent plastid-

encoded genes [36�]. Thus, Mg-ProtoIX may also trigger

the organellar gene expression mediated pathway as a

secondary effect. However, GUN1 would at least integrate

the redox-mediated and the organellar gene expression

mediated pathways.

The abi4 mutant was demonstrated to exhibit a gunphenotype when grown on inhibitors of plastid translation

and the AP2-type transcription factor, ABI4, was found to

bind in close proximity of the CUF1 element of the

LHCB promoter required for retrograde signaling

[32��,33]. Several lines of evidence presented by Kous-

sevitzky et al. [32��] suggest that GUN1 and ABI4 act in

the same signaling pathway. Thus, in response to the

GUN1-derived signal, ABI4 binds the promoter of LHCB,

which then prevents the binding of G-box-binding factors

required for light-induced expression of nuclear-encoded

photosynthesis genes [32��]. To reveal the nature of the

GUN1-derived common plastid signal that activates ABI4

is one of the key questions for the field.

ConclusionsAlthough it is true that the chloroplast is dependent on

the nucleus to supply much of the genetic information


necessary for their function, it is also becoming clear that

the plastids produce multiple signals in response to

changes in the environment that orchestrate major

changes in nuclear gene expression. Plastid signals assist

the cell during stress responses and for the plant to

respond optimally to environmental stress, information

must be integrated from both cytosolic and plastid-sig-

naling networks. The sources of many plastid signals

and cis-elements with transacting factors through which

the signals are mediated have been identified. However,

the cytosolic components transducing the signal to the

nucleus remain elusive and identifying these players is an

exciting task for the future.

AcknowledgementsWe thank Dr Vaughan Hurry and Peter Kindgren for helpful comments onthe manuscript. Financial support through the Swedish Research Counciland the INGVAR-grant from Foundation for Strategic Research, SSF (AS) isgratefully acknowledged.

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Retrograde signaling and plant stress: plastid signals initiate cellular stress responses