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  • Review Article
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Coordination of gene expression between organellar and nuclear genomes

Key Points

  • Mitochondria and chloroplasts contain their own genomes, but most of their proteins are encoded in the nucleus.

  • The coordination of separate genomes is achieved by both anterograde mechanisms (nucleus to organelle) and retrograde signals (organelle to nucleus).

  • Transcriptional regulation in organelles is mostly used for global rather than subtle changes in gene expression.

  • Anterograde control of organelle gene expression is primarily post-transcriptional, involving nuclear-encoded regulators of organelle gene expression (ROGE) proteins that regulate the expression of specific organelle genes. In sugar-starved plant mitochondria, gene regulation occurs on a post-translational level and involves protein degradation and assembly.

  • Retrograde signals from organelles are numerous, complex, fulfil different requirements for the cell and use mechanisms that are not conserved among the kingdoms.

  • Tetrapyrroles act as retrograde signals in yeast mitochondria and in plant and algae chloroplasts, but with different effects.

  • In plants, several retrograde signals converge in chloroplasts, where they are mediated by the genomes uncoupled 1 (GUN1) protein.

  • In plants, cell death caused by singlet oxygen is a genetically programmed response to a retrograde signal mediated by the EXECUTER 1 protein.

  • Chloroplast-to-mitochondrion cross-talk involves retrograde signals from one organelle to the nucleus, which then modules anterograde control of the other organelle.

Abstract

Following the acquisition of chloroplasts and mitochondria by eukaryotic cells during endosymbiotic evolution, most of the genes in these organelles were either lost or transferred to the nucleus. Encoding organelle-destined proteins in the nucleus allows for host control of the organelle. In return, organelles send signals to the nucleus to coordinate nuclear and organellar activities. In photosynthetic eukaryotes, additional interactions exist between mitochondria and chloroplasts. Here we review recent advances in elucidating the intracellular signalling pathways that coordinate gene expression between organelles and the nucleus, with a focus on photosynthetic plants.

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Figure 1: An overview of genome co-ordination between the nucleus and intracellular organelles.
Figure 2: Nuclear anterograde control of organelle gene expression.
Figure 3: Retrograde signalling pathways and chloroplast–mitochondrion cross-talk in higher plant cells.

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Acknowledgements

Our work on genome coordination is supported by grants from the US Department of Energy (J. C.), and the Howard Hughes Medical Institute (J. C.). J. W. is supported by the Ruth L. Kirschstein National Research Service Awards post-doctoral fellowship from the National Institutes of Health. The authors wish to thank S. S. Orchard, G. H. Anderson, A. Nott, and J. M. Pérez-Ruiz for their reading and discussion of the manuscript.

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Glossary

Amyloplasts

A non-pigmented heterotrophic type of plastid that is used for starch storage, mostly found in underground tissues such as roots and tubers. When the plant requires energy, amyloplasts can convert the stored starch into usable sugars.

Chromoplasts

Plastids that are dedicated to pigment synthesis and storage. Chromoplast colours vary according to the type of pigment they contain, and they are responsible for the distinctive colours of fruits and of flower petals.

Pioneer protein

A protein that has no known homologue in other species. Therefore, pioneer proteins often lack any identifiable sequence motifs other than those that are used for protein localization.

De-etiolation

In plants, de-etiolation is the irreversible process of shifting from a heterotrophic dark-grown (etiolated) lifestyle to a phototrophic light-grown lifestyle. De-etiolation involves both morphological and physiological changes that are needed to acclimatize to light and to harvest its energy.

Greening

The shift of non-green plant seedlings grown in the dark (etiolated) to a green colour as a result of chloroplast biogenesis and chlorophyll accumulation during the process of de-etiolation.

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Woodson, J., Chory, J. Coordination of gene expression between organellar and nuclear genomes. Nat Rev Genet 9, 383–395 (2008). https://doi.org/10.1038/nrg2348

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