plastids are major regulators of light signaling in arabidopsis

Available online at www.sciencedirect.com

Integration of light and plastid signalsRobert M Larkin1,2 and Michael E Ruckle1,2

Light and plastid signals promote chloroplast biogenesis and

are among the most potent inducers and repressors of

photosynthesis-related gene expression, respectively. These

signals can be likened to a ‘gas and brake system’ that

promotes efficient chloroplast biogenesis and function. Recent

findings indicate that a particular plastid signal can ‘rewire’ a

light signaling network, converting it from an inducer into a

repressor of particular photosynthesis-related genes.

Therefore, a plastid signal appears to be an endogenous

regulator of light signaling rather than a signal acting

independently from light. This integration of light and plastid

signals may allow plants to proactively manage chloroplast

dysfunction when performing chloroplast biogenesis and

maintenance in adverse light conditions.

Addresses1 Michigan State University, Department of Energy Plant Research

Laboratory, United States2 Department of Biochemistry and Molecular Biology, Michigan State

University, East Lansing, MI 48824, United States

Corresponding author: Larkin, Robert M ([email protected]) and Ruckle,

Michael E ([email protected])

Current Opinion in Plant Biology 2008, 11:593–599

This review comes from a themed issue on

Cell Biology

Edited by David Ehrhardt and Federica Brandizzi

Available online 22nd October 2008

1369-5266/$ – see front matter

# 2008 Elsevier Ltd. All rights reserved.

DOI 10.1016/j.pbi.2008.10.004

IntroductionProteins that perform functions related to photosynthesis

are encoded by both nuclear and chloroplast genomes.

The chloroplast contains a small genome that encodes

less than 100 proteins, most of which contribute to

photosynthesis and the expression of the chloroplast

genome. By contrast, approximately 3000 nuclear genes

are predicted to encode chloroplast proteins in Arabidop-

sis and rice [1]. Coordinating the expression of photosyn-

thesis-associated nuclear genes (PhANGs) with the

expression of photosynthesis-associated plastidic genes

is essential for proper chloroplast biogenesis and main-

tenance, because photosynthesis depends on large multi-

subunit protein complexes that are composed of both

chloroplast-encoded and nuclear-encoded proteins.

Environmental and endogenous cues such as light, the

circadian clock, tissue-specific signals, carbohydrates, and

www.sciencedirect.com

hormones control the expression of nuclear genes that

encode chloroplast proteins [2–4], including those that

control the expression of the plastid genome [5,6]. There-

fore, the regulation of nuclear gene expression by these

signals has a major role in coordinating the expression of

both genomes and controlling chloroplast biogenesis and

function.

Although far from autonomous, chloroplasts are not com-

pletely subordinate to the nucleus. In fact, signals that are

triggered by plastid dysfunction are major regulators of

nuclear gene expression, especially of a number of genes

that encode proteins active in photosynthesis. Plastids

were first shown to affect the extraplastidic synthesis of

plastidic enzymes thirty years ago [7]. Subsequent studies

showed that plastid factors can repress the transcription of

nuclear genes and that this plastid-mediated repression

depends on particular cis-acting elements in the promo-

ters of nuclear genes. Up to several thousand genes can be

regulated by plastid dysfunction in Arabidopsis. Several

plastid signals have been identified, such as buildup of

the chlorophyll precursor Mg-protoporphyrin IX, signals

that are transduced when the expression of the plastid

genome is inhibited, signals derived from the photosyn-

thetic electron transport chain, and reactive oxygen

species such as singlet oxygen and hydrogen peroxide.

The molecular nature of signals that are derived from the

expression of the plastid genome and the photosynthetic

electron transport chain have not been defined. Many of

the proteins that are required for plastid signal biosyn-

thesis and transduction remain unknown. Also, although

plastid signals affect growth and development, their full

impact of plastid signals on growth and development has

not been completely established. These aspects of plas-

tid-to-nucleus signaling have been reviewed recently [8–12]. Here, we will review recent findings on the integ-

ration of light and plastid signals, topics not covered by

these other reviews.

Plastid signals and plastid-to-nucleussignaling mechanismsBlocking chloroplast biogenesis was one of the first

approaches for studying plastid-to-nucleus signaling.

Chloroplast biogenesis can be blocked using particular

genetic backgrounds (e.g., variegated mutants, plastid

ribosome-deficient, or carotenoid-deficient mutants).

Alternatively, chloroplast biogenesis can be blocked using

photobleaching herbicides or antibiotics that inhibit the

expression of the plastid genome. Seedlings treated with

these inhibitors of chloroplast biogenesis are viable when

they are provided sucrose, and become green when

transferred to media that does not contain one of these


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mailto:[email protected]

http://dx.doi.org/10.1016/j.pbi.2008.10.004

594 Cell Biology

Figure 1

Analysis of PhANG expression in seedlings treated with an inhibitor of

chloroplast biogenesis. (a) Lincomycin-treated and untreated

Arabidopsis seedlings. Arabidopsis seedlings were grown on media

containing lincomycin (+) or no inhibitor of chloroplast biogenesis (�), as

previously described [13��]. Lincomycin inhibits plastid translation. Like

the photobleaching herbicide norflurazon, lincomycin blocks chloroplast

biogenesis and severely represses PhANG expression [10]. Neither

lincomycin-treated nor norflurazon-treated seedlings accumulate

chlorophyll, but both accumulate anthocyanins [14,16] [Ruckle ME and

Larkin RM, unpublished data]. Bar = 2 mm. (b) Lhcb and RbcS

expression in lincomycin-treated and untreated Arabidopsis seedlings.

Total RNA was extracted from seedlings that were either lincomycin-

treated (+) or not treated (�), as previously described [13��]. Lhcb and

RbcS mRNA levels were analyzed by northern blotting as previously

described [13��]. These mRNAs accumulate at approximately 50-fold

lower levels in treated compared to untreated seedlings.

Figure 2

A previous model for the regulation of PhANG expression by light and plasti

chloroplasts. Light induces PhANG expression. Plastid signals that are trigge

Under these conditions, PhANG expression is robust, supporting chloroplas

chloroplasts. Light induces PhANG expression, but plastid signals that inhibit


inhibitors. Seedlings treated with an inhibitor of chlor-

oplast biogenesis contain nonphotosynthetic plastids that

resemble proplastids and exhibit very low levels of

PhANG expression, even in the presence of potent

inductive signals such as light (Figure 1). On the basis

of these data, these dysfunctional plastids were proposed

to emit signals that affect PhANG expression [9,10]

(Figure 2). The plastid-to-nucleus signaling triggered

by these treatments can be a major regulator of PhANG

expression. For example, light is one of the most potent

inducer of PhANGs, but when chloroplast biogenesis is

blocked in light conditions that otherwise induce high

levels of PhANG expression, PhANGs are expressed at

even lower levels than are observed in the dark [13��,14].

These plastid signals help coordinate the expression of

nuclear and chloroplast genomes, couple the expression

of PhANGs with the functional state of the chloroplast,

and are required for efficient chloroplast biogenesis

[9,10,13��].

Our understanding of plastid-to-nucleus signaling that is

triggered when chloroplast biogenesis is blocked has been

enhanced by the genomes uncoupled (gun) mutants. These

mutants uncouple the expression of genes that encode

proteins active in photosynthesis from chloroplast func-

tion. For example, when wild-type seedlings are treated

with inhibitors of chloroplast biogenesis, genes that

encode proteins active in photosynthesis are repressed,

but when gun mutants are treated with these same inhibi-

tors, PhANGs are partially derepressed. PhANGs that

encode the light-harvesting chlorophyll a/b-binding

protein of photosystem II (Lhcb or CAB, hereafter

referred to as Lhcb) and the small subunit of Rubisco

(RbcS) have been routinely used in these studies.

In Arabidopsis seedlings grown on media that contain

d signals. (a) PhANG expression in seedlings containing well-functioning

red by plastid dysfunction and repress PhANG expression are not active.

t function. (b) PhANG expression in seedlings containing dysfunctional

PhANG expression are active. PhANG expression is severely repressed.


Plastid-light interactions Larkin and Ruckle 595

Figure 3

The GUN1-dependent plastid signaling. When Arabidopsis seedlings are

treated with inhibitors of chloroplast biogenesis, the buildup of Mg-

protoporphyrin IX (Mg-Proto) or inhibition of plastid gene expression

(PGE) triggers the production of a second messenger (X) that requires

GUN1 for its biosynthesis or transduction (dashed arrows). High-

intensity light and glucose treatments can also induce the biosynthesis

or transduction of X. Light induces PhANG expression by inducing the

activity of G-box binding factors (GBFs) that induce PhANG

transcription, as described in the text. X induces the ABI4-dependent

repression of PhANGs. ABI4 has been proposed to repress PhANGs by

binding to CCAC and displacing GBFs, which bind the light-responsive

G-box (CACGTG). This model was adapted from Koussevitzky et al.

[18��].

various inhibitors of chloroplast biogenesis, Lhcb and

RbcS mRNAs accumulate at 2–3% of the levels observed

in untreated seedlings. By contrast, when strong gunalleles are treated with these same inhibitors, mRNAs

encoded by these PhANGs accumulate to 10–20% of the

levels observed in untreated seedlings [13��,15]. The

derepression of PhANG expression in gun mutants is

thought to result from defects in plastid-to-nucleus sig-

naling that repress PhANGs [9,10]. The coordination of

the nuclear and chloroplastic genomes is also impaired in

gun1 mutants [16].

Recent analysis of gun mutants indicates that accumu-

lation of the chlorophyll precursor Mg-protoporphyrin IX,

inhibition of chloroplast genome expression, high levels

of glucose, and exposure to high-intensity light all pro-

duce a second messenger that triggers plastid-to-nucleus

signaling that represses PhANG expression. This second

messenger remains undefined. GUN1 appears to be cru-

cial for the production or transduction of this second

messenger. GUN1 is a chloroplastic pentatricopeptide

repeat protein that colocalizes with nucleoids. Because

these proteins contribute to post-transcriptional processes

such as splicing, editing, processing, and translation of

RNA in chloroplasts and mitochondria [17], these findings

are consistent with the expression of the plastid genome

affecting nuclear gene expression when chloroplast bio-

genesis is blocked. ABSCISIC ACID-INSENSITIVE 4

(ABI4), an Apetala 2-type transcription factor, acts down-

stream of GUN1 and appears to repress PhANG tran-

scription by binding CCAC in PhANG promoters, a

sequence that is adjacent to or overlapping with the G-

box [18��]. Because G-boxes can contribute to the light

induction of PhANGs [2,19], these data suggest that ABI4

and a G-box binding factor(s) (GBF) might compete for a

binding site on PhANG promoters. However, not all

GUN1-regulated promoters have a CCAC motif overlap-

ping or in close proximity to a G-box [18��]. Moreover,

ABI4 has also been reported to have no effect on the

plastid regulation of reporter genes driven by particular

RbcS promoters [20]. These findings suggest that GUN1-

dependent plastid signals may regulate transcription fac-

tors other than ABI4. Nonetheless, GUN1 and ABI4

acting downstream of multiple plastid signals is consistent

with a model proposed several years ago in which a master

switch integrates diverse plastid signals [21]. These find-

ings also suggest that GUN1 and ABI4 function as part of

this master switch [18��] (Figure 3).

Regulation of PhANG expression by lightLight regulates at least 20% of the transcriptome in

Arabidopsis and rice. A number of photoreceptors and

downstream signaling components have been shown to

function in light-regulated transcriptional networks [2].

Photoreceptor signaling mechanisms are complex, invol-

ving the regulation of activity, subcellular localization,

and concentrations of particular photoreceptors and


downstream signaling components [2]. The expression

of Lhcb, RbcS, and other PhANGs is induced by phyto-

chromes and cryptochromes, which sense far-red, red, and

blue light [19,22,23]. Much of this induction results from

increased rates of transcription. A combination of at least

two promoter elements such as G-boxes, GT-elements, I-

boxes or GATA motifs, AT-rich motifs, and others have

been shown to function as light-responsive promoter

elements in PhANGs [2,19].

Interaction between plastid signaling and lightsignalingNo light signaling mutants were obtained from the

original gun screen, with the exceptions of gun2 and

gun3, which are allelic to hy1 and hy2 [15]. These genes

encode heme oxygenase and phytochromobilin synthase


596 Cell Biology

and are required for the biosynthesis of the chromophore

for phytochromes [24]. The gun phenotypes of these

mutants are thought to arise from reduced levels of

Mg-protoporphyrin IX rather than as a result of defective

phytochrome signaling [15,25,26]. However, although

photoreceptors such as cry1 induce Lhcb expression in

greening and green seedlings [19,23], cry1 alleles were

recently isolated from a new gun mutant screen. These

data indicate that cry1 represses Lhcb when chloroplast

biogenesis is blocked. cry1 mutants that are treated with

inhibitors of chloroplast biogenesis accumulate approxi-

mately 5–10% of the Lhcb mRNA that accumulates in

wild-type seedlings that are not treated with inhibitors of

chloroplast biogenesis, compared to the 2–3% that

accumulates in treated wild type. This subtle gun phe-

notype understates the significance of cry1 in this context.

Double mutant studies show that Lhcb is synergistically

derepressed in cry1 gun1 double mutants and that cry1 and

GUN1 are responsible for most if not all of the repression

of Lhcb in blue light. These data indicate that a plastid

signal can convert cry1 into a negative regulator of Lhcband suggest that the fluence rate should control the

amount of Lhcb repression. Indeed, when seedlings are

treated with inhibitors of chloroplast biogenesis, the

repression of Lhcb is increased 10-fold in bright light

compared to dim light [13��].

Figure 4

Working model for the rewiring of cry1 signaling by plastid signals. (a) Regu

chloroplasts. Because HY5 binding is necessary but not sufficient to regulate

by a factor (W) that associates with the Lhcb promoter using a HY5-depend

described in the text, HY5 appears to bind the G-box (CACGTG). (b) Regul

chloroplasts. When seedlings are treated with an inhibitor of chloroplast bio

described in Figure 3. Simultaneously, a distinct plastid signal (Y) converts c

[13��]. We propose that Y activates a factor (Z) that replaces factor W describ

fluence rate of light also increases the repression of Lhcb when chloroplast b

are present [13��]. Therefore, we propose that the activity of factor Z may a


The mechanism by which cry1 regulates PhANG expres-

sion appears the same regardless of whether seedlings are

treated with inhibitors of chloroplast biogenesis. cry1

appears to regulate gene expression by inhibiting

COP1, an E3 ubiquitin ligase that targets positive reg-

ulators of photomorphogenesis and PhANG expression

for degradation through the proteasome [13��], as has

been previously shown [2,27]. These studies also showed

that the conversion of cry1 from a positive to a negative

regulator of Lhcb largely results from the conversion of

long hypocotyl 5 (HY5) from a positive to a negative

regulator of Lhcb [13��]. HY5 is a basic leucine zipper

transcription factor that acts downstream of cry1 and other

photoreceptors to induce the expression of PhANGs like

Lhcb and photomorphogenesis [2,28��]. Because HY5

both induces and represses the expression of Lhcb, and

because promoter binding appears necessary but not

sufficient for HY5 to regulate transcription [28��], we

suggest that HY5 requires other factors to induce and

repress Lhcb transcription. For example, we suggest that

when chloroplast biogenesis proceeds and chloroplasts

are not stressed, the activity of a factor that induces Lhcbusing a HY5-dependent mechanism dominates, but when

chloroplasts are dysfunctional, a plastid signal induces the

activity of a factor that represses Lhcb using a HY5-de-

pendent mechanism. Under each set of conditions, cry1

lation of Lhcb transcription by HY5 in cells that contain well-functioning

gene expression [28��], we propose that Lhcb transcription is activated

ent mechanism when cells contain well-functioning chloroplasts. As

ation of Lhcb transcription by HY5 in cells that contain dysfunctional

genesis, the GUN1-dependent signals (shown in gray) are activated as

ry1 into a repressor of Lhcb by converting HY5 into a repressor of Lhcb

ed in (a), thereby converting HY5 into a repressor of Lhcb. Increasing the

iogenesis is blocked, regardless of whether the GUN1-dependent signals

lso be induced by light, as has been reported for HY5 [2].



Figure 5

Interaction between plastid signaling and light signaling that affects Lhcb

and RbcS expression. (a) Regulation of Lhcb and RbcS expression in

seedlings containing chloroplasts that are not stressed. During de-

etiolation or in green seedlings photoreceptors that perceive red and

blue light induce the expression of Lhcb and RbcS, as described in the

text. Chloroplasts that are not stressed have not been shown to

influence the regulation of these PhANGs by affecting light-regulated

transcriptional networks. (b) The rewiring of light signaling networks by

plastid signals. When chloroplast biogenesis is blocked, a plastid signal

(X) triggers the GUN1-dependent signaling, as described in Figure 3

(shown in gray). Under these same conditions, a distinct plastid signal(s)

(Y) converts the blue and/or red light signaling network, which have

otherwise been reported to induce both Lhcb and RbcS, into repressors

of Lhcb and RbcS. Plastid–phytochrome interactions are not as well

understood as plastid–cry1 interactions. The repression of RbcS by Y

may result from a light-dependent or a light-independent signal (dotted

arrow and dotted T-bar, respectively). Y may be more than one signal.

Subpart (b) was adapted from Ruckle et al. [13��].

promotes the activity of the regulatory complex by bind-

ing and inhibiting COP1, thereby protecting HY5 from

degradation (Figure 4). The conversion of particular

transcription factors from positive to negative regulators

and vice versa has been reported in other systems. For

example, nuclear receptors and Myc are known to either

positively or negatively regulate transcription, depending

on the coregulators or transcription factors they bind [29–31]. Other mechanisms are possible.

The findings of Koussevitzky et al. [18��] and Ruckle et al.[13��] indicate that ABI4 and HY5 are simultaneously

required for plastid-dependent repression of Lhcb. There-

fore, a model that is more complex than ABI4 displacing

GBFs such as HY5 [32,33] from Lhcb promoters seems

likely. These findings lead us to suggest that either both

factors simultaneously bind Lhcb promoters when chlor-

oplast biogenesis is blocked or that at least one of these

factors represses Lhcb by an indirect mechanism.

Although HY5 has been shown to bind Lhcb promoters

in light-grown and etiolated tissue by chromatin immu-

noprecipitation [28��], neither ABI4 nor HY5 has been

tested for binding Lhcb or other PhANG promoters in

seedlings treated with inhibitors of chloroplast bio-

genesis.

Several observations suggest that plastid–light inter-

actions are probably more complex than described above.

For example, although cry1 and GUN1 are responsible for

most if not all repression of Lhcb when chloroplast bio-

genesis is blocked in blue light, repression in white light

appears more complex. This additional complexity may

be contributed by other photoreceptors. Indeed, phyB

contributes to the repression of Lhcb when chloroplast

biogenesis is blocked in white light, but whether all

repression of Lhcb in white light depends on GUN1,

cry1, and phyB remains to be tested. The complexity

of plastid–light interactions is also apparent from an

analysis of RbcS expression. Although Lhcb and RbcSare similarly repressed when Arabidopsis seedlings are

treated with inhibitors of chloroplast biogenesis in white

light, cry1 remains a positive regulator of RbcS regardless

of the functional and developmental state of the chlor-

oplast. Analysis of RbcS mRNA levels in seedlings trea-

ted with inhibitors of chloroplast biogenesis and

untreated seedlings in different light qualities are con-

sistent with (1) a light quality besides blue or (2) a light-

independent signal that is distinct from GUN1-depend-

ent signals repressing RbcS when chloroplast biogenesis is

blocked [13��] (Figure 5).

Interactions between plastid and light signals are not

surprising. Because light promotes chloroplast biogenesis

and photosynthesis, light also induces chloroplast stress

[34]. Although plastid signals such as the light-indepen-

dent signals that require GUN1 allow plants to react to

chloroplast stress, plants may need to do more than simply


react. By ‘rewiring’ light signaling, plastid signals could

enable plants to be proactive rather than simply reactive,

and to respond not only to chloroplast dysfunction but

also to the potential for continued photooxidative damage

when regulating nuclear gene expression. Consistent with

these plastid–light interactions contributing to photooxi-

dative stress tolerance, cry1 and hy5 single mutants are more

sensitive to high-intensity light than wild type [13��,35].

Additionally, a striking increase in the sensitivity to


598 Cell Biology

high-intensity light was observed in the cry1 gun1 and hy5gun1 double mutants compared to the corresponding single

mutants and wild type [13��]. Another example of plastid–light interactions that is consistent with this model was

recently reported by Danon et al. [36��]. These authors

showed that singlet oxygen stress within the chloroplast

requires cry1 to regulate nuclear gene expression and

trigger a programmed cell death response.

ConclusionsAt least two genetically distinct plastid signals have been

defined that are triggered by treatments with inhibitors of

chloroplast biogenesis: the signal that remodels a light

signaling network and the light-independent plastid sig-

nals that depend on GUN1. Lhcb mRNA has been

reported to accumulate at similar levels in particular

gun mutants treated with inhibitors of chloroplast bio-

genesis and untreated wild-type seedlings only in blue or

far-red light and not when seedlings are grown in dark-

ness, white light, red light, or in any light condition that

induces RbcS mRNA [13��]. These findings suggest that

we are unable to completely knock out plastid-to-nucleus

signaling and may not know the full impact of plastid-to-

nucleus signaling during growth and development of

plants at this time. We do know that the GUN1-depend-

ent signals and plastid signals that remodel light signaling

networks regulate nuclear gene expression and promote

efficient chloroplast biogenesis [9,10,13��]. Recent

analyses of gun1 cry1 double mutants indicate that plastid

signals can also affect the accumulation of anthocyanins

and the photomorphogenesis of cotyledons and hypoco-

tyls (Ruckle ME and Larkin RM, unpublished data).

Additionally, plastid signals were recently shown to affect

the circadian clock [37�]. These recent findings suggest

that the significance of signals emanating from the plastid

may be underappreciated, not only in regulating chlor-

oplast biogenesis and function but also in other processes.

AcknowledgementsThis work was supported by DOE grant no. DE–FG02–91ER20021 andNSF grant no. IOB 0517841 to RML.

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34. Niyogi KK: Photoprotection revisited: genetic and molecularapproaches. Annu Rev Plant Physiol Plant Mol Biol 1999,50:333-359.

35. Kleine T, Kindgren P, Benedict C, Hendrickson L, Strand A:Genome-wide gene expression analysis reveals a critical rolefor CRYPTOCHROME1 in the response of Arabidopsis to highirradiance. Plant Physiol 2007, 144:1391-1406.

36.��

Danon A, Coll NS, Apel K: Cryptochrome-1-dependentexecution of programmed cell death induced by singletoxygen in Arabidopsis thaliana. Proc Natl Acad Sci U S A 2006,103:17036-17041.

These authors show that a plastid-to-nucleus signaling pathway that istriggered by singlet oxygen stress within the chloroplast requires photo-activated cry1 to induce programmed cell death.

37.�

Hassidim M, Yakir E, Fradkin D, Hilman D, Kron I, Keren N, Harir Y,Yerushalmi S, Green RM: Mutations in chloroplast RNA bindingprovide evidence for the involvement of the chloroplast in theregulation of the circadian clock in Arabidopsis. Plant J 2007,51:551-562.

These authors demonstrate that a chloroplast-localized RNA-bindingprotein can affect the circadian clock. They also demonstrate thatGUN1 and STN7, which were previously shown to participate in plas-tid-to-nucleus signaling, can also affect the circadian clock.


plastids are major regulators of light signaling in arabidopsis

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