Interorganellar communication

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Signals originating from chloroplasts and mitochondria modulate nuclear gene expression (retrograde signalling). Relevant signals are derived from the pool of reactive oxygen species or generated by changes in redox state, flux through the tetrapyrrole biosynthetic pathway, or rates of organelle protein synthesis. In addition, multiple interactions of these four pathways with sugar and hormone signalling occur. Although the nature of the molecules that relay information through the cytosol to the nucleus is still unknown, the first putative signalling components in the chloroplast have recently been identified, and give tentative hints of overlaps between the different pathways. Retrograde signalling-dependent modulation of nuclear gene expression seems to involve multilayered transcriptional control and the transcription factor ABI4.

Introduction

Although often used for all structurally discrete cell components, the term ‘organelle’ is here limited to DNA-containing compartments bounded by double membranes. Chloroplasts and mitochondria each contain several thousand different proteins. Most of these are encoded by nuclear genes, whereas the few resident genes mainly encode components of the gene expression system itself, and the respiratory chain (in mitochondria) or photosynthesis (in chloroplasts). Hence, chloroplast ribosomes or photosystems are mosaics—multiprotein complexes made up of nucleus-encoded and plastid-encoded subunits. This implies the existence of mechanisms that coordinate gene expression in the different compartments. Multiple levels of nuclear control of organellar properties – summarized as ‘anterograde control’ – operate to regulate nuclear [1•, 2•] and organellar gene expression, as well as posttranslational events. ‘Retrograde’ mechanisms have evolved to communicate the functional and developmental state of chloroplasts and mitochondria to the nucleus, so as to modulate the anterograde control according to cellular needs. Four main retrograde pathways have been defined, depending on the signal source: (i) tetrapyrrole biosynthesis, (ii) organellar gene expression (OGE) (see Glossary); (iii) organellar redox state, and (iv) reactive oxygen species (ROS) (see Glossary) (Figure 1). Although not a classical retrograde signal, sugar sensing is also discussed here because it overlaps and interacts – at least in certain tissues – with canonical retrograde signalling pathways.

Section snippets

Tetrapyrrole signalling

The first evidence for an involvement of tetrapyrroles in the regulation of nuclear gene expression came from studies on green algae, with the discovery that Chlamydomonas reinhardtii cells failed to accumulate light-induced LHCB (see Glossary) transcripts when treated with inhibitors of late steps in tetrapyrrole biosynthesis, but not when treated with inhibitors acting on early steps. This finding immediately suggested that certain intermediates in tetrapyrrole synthesis trigger inhibition of

OGE signalling

Treatment with inhibitors of organellar protein synthesis decreases the expression of nuclear photosynthesis genes in a light-independent manner during early stages of plant development [10, 11]. The Arabidopsis prors1 mutant, which is defective in a prolyl-tRNA synthetase found in both plastids and mitochondria and exhibits a decrease in protein synthesis in both organelles, was recently characterized [12]. The prors1 mutation induces a specific, light-independent, downregulation of nuclear

Redox and ROS signalling

Two different sources have been proposed for redox signals that activate retrograde communication: (i) intersystem electron transport in the chloroplast, particularly the plastoquinone pool (PQ), and (ii) the PSI (see Glossary) acceptor site with a variety of redox-active components (e.g. NADPH, thioredoxin, glutathione and glutaredoxin) (Figure 3). In the green alga Dunaliella tertiolecta, the redox state of PQ is thought to be coupled to the regulation of nuclear photosynthesis genes by light

Sugar signalling

In flowering plants, sugars affect growth and development throughout the life cycle and act as signalling molecules to control the expression of nuclear genes involved in photosynthesis, glyoxylate metabolism, respiration, starch and sucrose synthesis, and many other essential processes. Increased levels of glucose or sucrose, the end-products of photosynthesis, repress photosynthetic gene expression [32]. Hexokinase (HXK) (see Glossary) is critical for sensing and responding to hexose signals

Communication between chloroplasts and mitochondria?

Chloroplasts and mitochondria are metabolically interdependent at multiple levels. Despite this close interdependence, little is known about communication between them or coordination of the activities of the two organelles by signals other than carbon metabolites. Although nitric oxide, ascorbate and ROS have been suggested to act as signals between mitochondria and chloroplasts [43], no solid experimental evidence has been provided so far. Nevertheless, mitochondria and chloroplasts work in

Conclusions

Following the generation of a signal in the cytosolic organelles, the information must be transmitted to the nucleus. The cytosolic and nuclear components of interorganellar signalling remain more or less elusive. Transcriptome analyses in A. thaliana revealed the existence of different layers of transcriptional control over nuclear chloroplast genes, including a ‘master switch’ that acts in a binary mode by either inducing or repressing the same large set of genes [1•, 15•]. Recently, the

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

We thank the Deutsche Forschungsgemeinschaft (DFG) for financial support (grants SFB-TR1 TPB7, FOR804 TP5, LE1265/9) and Klaus Apel, Karl-Josef Dietz, Bernhard Grimm, Thomas Pfannschmidt and Paul Hardy for critical comments on the manuscript.

Glossary

ABI4
abscisic acid-insensitive 4
APX2
ASCORBATE PEROXIDASE 2
ChlH
H subunit of Mg chelatase
2CPA
2-CYS PEROXIREDOXIN-A
gin2
glucose insensitive 2
gun
genomes uncoupled
H2O2
hydrogen peroxide
HXK
hexokinase
LHCB
nuclear genes encoding the chlorophyll a/b binding proteins of photosystem II
Lincomycin
inhibitor of organelle translation
Norflurazon
inhibitor of phytoene desaturase, a carotenoid biosynthesis enzyme
1O2
singlet oxygen
O2radical dot
superoxide anion
OGE
organelle gene expression
PPR protein
pentatricopeptide repeat

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