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  • Review Article
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Biogenesis and homeostasis of chloroplasts and other plastids

Nature Reviews Molecular Cell Biology volume 14, pages 787–802 (2013)Cite this article

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An Erratum to this article was published on 14 January 2014

This article has been updated

Key Points

  • Chloroplasts are the ancestral members of a structurally diverse family of organelles known as plastids (which also includes proplastids, amyloplasts and chromoplasts). Plastids are responsible for photosynthesis and various metabolic and signalling functions (among others), and they are the organelles that define plants.

  • Plastids evolved through endosymbiosis from an ancient relative of extant cyanobacteria. They are semi-autonomous by virtue of the fact that they retain a functional genetic system of their own. As a result, an important component of the biogenesis and homeostasis of plastids is the coordination of the organellar genome (plastome) with the nuclear genome.

  • During evolution, many organellar genes were transferred from the plastome to the nuclear genome, with the consequence that the bulk-flow of information during organellar development proceeds from the nucleus to plastids. Nonetheless, plastid-to-nucleus signals emitted by plastids (termed retrograde signals) have a significant influence on the expression of many nuclear genes.

  • Most plastid proteins are encoded in the nucleus and synthesized in the cytosol (each contains a cleavable targeting signal (or transit peptide)), and are imported post-translationally by plastids through the TOC (translocon at the outer envelope membrane of chloroplasts)–TIC (translocon at the inner envelope membrane of chloroplasts) translocation machinery in the envelope membranes. Client-specific protein import pathways (enabled by a diversity of TOC receptor components) influence the composition of the organellar proteome, and the balance of these pathways is controlled by the cytosolic ubiquitin–proteasome system.

  • Intraorganellar sorting of plastid proteins is achieved through a range of translocation systems (including the cpSEC (chloroplast SEC), cpTAT (CHLOROPLAST TWIN ARG TRANSLOCASE) and cpSRP (CHLOROPLAST SIGNAL RECOGNITION PARTICLE) pathways) that have been conserved through evolution and are thus similar to protein sorting pathways found in bacteria. Similarly, proteolytic systems operating inside plastids (CLP, FTSH, DEG and LON) are of prokaryotic origin.

  • Plastids are propagated by the division of pre-existing organelles though a binary fission mechanism that uses components that have been inherited from the prokaryotic endosymbiont (for example, FTSZ (FILAMENTOUS TEMPERATURE SENSITIVE Z)), as well as additional factors of eukaryotic origin (for example, dynamin-related ARC5 (ACCUMULATION AND REPLICATION OF CHLOROPLASTS 5)). The structurally dynamic nature of plastids is further indicated by their ability to produce stroma-filled protrusions called stromules and by observations of vesicle budding from the plastid body.

  • Plastid biogenesis and homeostasis are closely coordinated with cell and organ development to ensure that an appropriate number of plastids of the correct type are present in cells at each stage of plant development. Transcription factors responsible for chloroplast differentiation may have roles in chloroplast-to-nucleus communication and in the response to environmental (such as light) or hormonal signals.

Abstract

Chloroplasts are the organelles that define plants, and they are responsible for photosynthesis as well as numerous other functions. They are the ancestral members of a family of organelles known as plastids. Plastids are remarkably dynamic, existing in strikingly different forms that interconvert in response to developmental or environmental cues. The genetic system of this organelle and its coordination with the nucleocytosolic system, the import and routing of nucleus-encoded proteins, as well as organellar division all contribute to the biogenesis and homeostasis of plastids. They are controlled by the ubiquitin–proteasome system, which is part of a network of regulatory mechanisms that integrate plastid development into broader programmes of cellular and organismal development.

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Figure 1: Diversity of plastid forms and their interconversions.
Figure 2: Light-mediated anterograde control of chloroplast development.
Figure 3: Plastid-to-nucleus or retrograde signalling pathways.
Figure 4: The protein import and routing pathways of plastids.
Figure 5: The TOC–TIC machinery mediates client-specific protein import and is controlled by the ubiquitin–proteasome system.
Figure 6: The plastid division machinery.

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Change history

  • 14 January 2014

    In the above article, figure 4 (page 794) had an incorrect label, which indicated that plastid DNA-encoded proteins are co-transcriptionally targeted to thylakoids, whereas targeting actually occurs co-translationally. Also, on pages 796-798 of the article, there were spelling mistakes in the definitions of PDV1 and COP1, which should be PLASTID DIVISION 1 and CONSTITUTIVE PHOTOMORPHOGENESIS 1, respectively. Finally, in the reference list, the highlighted description for reference 67 was incorrectly positioned below reference 63, and the highlighted description for reference 128 was incorrectly positioned below reference 26. These corrections have been made to the online version of the article. Nature Reviews Molecular Cell Biology apologizes for any confusion caused to readers.

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Acknowledgements

Work in the authors' laboratories was supported by the Biotechnology and Biological Sciences Research Council and the Gatsby Charitable Foundation. They thank K. Osteryoung for assistance with the preparation of Figure 6 and M. Terry, Q. Ling and R. Trösch for helpful comments on the manuscript. They apologize to the authors of the many important publications that could not be cited owing to space limitations.

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Authors and Affiliations

  1. Department of Plant Sciences, University of Oxford, South Parks Road, OX1 3RB, Oxford, UK

    Paul Jarvis

  2. School of Biological Sciences, Royal Holloway University of London, Egham, TW20 0EX, Surrey, UK

    Enrique López-Juez

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  1. Paul Jarvis
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  2. Enrique López-Juez
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Correspondence to Paul Jarvis.

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Competing interests

Paul Jarvis' work on SP1 is the subject of a patent application, which is related to the control of plastid development. Enrique López-Juez declares no competing financial interests.

PowerPoint slides

Glossary

Meristems

Groups of stem cell-like, undifferentiated cells, that are found particularly at the tips of shoots and roots. All other plant cells derive from the meristems.

Reaction centres

Complexes of proteins and photosynthetic pigments that are located at the centre of a photosystem. In these complexes, charge separation occurs to commence the photochemical reactions of photosynthesis.

Antenna complexes

Groups of proteins and photosynthetic pigments that collect photons and deliver their excitation energy to the reaction centre of a photosystem.

Thylakoid

Thylakoids are flattened membranous sacks inside plastids that are responsible for photosynthetic light reactions. They are distinct from the envelope membranes and typically stack to form grana in mature chloroplasts.

Mesophyll

Tissue in the interior of leaves, between the epidermal layers but not in contact with vascular bundle tissue, which contains most leaf chloroplasts and is the principal site of photosynthesis.

σ-factor

A subunit of multimeric, prokaryotic-type RNA polymerase that is responsible for DNA binding and promoter recognition; it thus determines which genes are transcribed.

Pentatricopeptide repeat proteins

(PPR proteins). Proteins that possess tandemly repeated copies of a degenerate, 35-residue motif that enables sequence-specific nucleic acid binding. These proteins are involved in RNA stability or editing in organelles.

Horizontal gene transfer

The transfer of genes between two contemporaneous individuals of the same or different species or between two genetic systems of one individual.

Photoautotrophic

An organism that derives its energy from light and that uses CO2 as a carbon source. The aerial tissues of plants are photoautotrophic when kept in the light.

Cryptochrome

A family of plant photoreceptors that are sensitive to blue light and, together with phytochromes, control developmental responses.

Translocon

A protein complex that is embedded within a membrane and acts in the translocation of client proteins into the membrane, or from one side of the membrane to the other.

β-barrel

A structural arrangement found in proteins of the outer membranes of Gram-negative bacteria, mitochondria and plastids, in which a number of transmembrane β-strands cooperate to form a cylindrical structure with a central pore.

Stroma

The aqueous internal matrix of plastids enclosed by the inner envelope membrane, where, in chloroplasts, the Calvin cycle enzymes mediate photosynthetic carbon fixation.

Omp85

A protein superfamily that comprises a range of β-barrel proteins that are all involved in protein transport or assembly; BamA is a prototypical member of the family and is responsible for the biogenesis of bacterial β-barrel proteins.

YidC and Oxa1

YidC and Oxa1 are homologous, polytopic membrane proteins found in bacteria and mitochondria, respectively. They mediate client insertion during membrane protein biogenesis.

Plastoglobules

Lipid bodies that are found within plastids. They are responsible for the storage and biosynthesis of lipids, and in chloroplasts they are associated with the thylakoids.

Ubiquitin E3 ligase

One of a large group of enzymes that catalyse the final step in the ubiquitylation cascade and that are responsible for determining target specificity.

AAA+ family

(ATPases associated with various cellular activities). A protein family comprising a diverse set of factors that mediate conformational changes in client proteins. They are characterized by the possession of Walker-type ATPase motifs and the ability to assemble into oligomeric rings.

Binary fission

The chief mode of cellular division in prokaryotes, by which a cell divides symmetrically to form two equal daughter cells that each contain genetic material.

Dynamin

A large GTPase that assembles into helical arrays at membrane constriction zones in order to catalyse membrane fission during various membrane remodelling processes.

RuBisCo

(Ribulose-1,5-bisphosphate carboxylase–oxygenase). The enzyme of the photosynthetic Calvin cycle that is responsible for CO2 fixation and may be the most abundant protein on earth.

Syngamy

The complete fusion of two gametes to form a zygote, which develops into a new organism.

Phytochromes

A family of plant and bacterial photoreceptors that are sensitive in particular to red and far-red light and are responsible for the control of developmental responses such as photomorphogenesis.

Photomorphogenesis

A developmental programme in higher plant seedlings that occurs in the light and is characterized by elongation inhibition, leaf expansion and chloroplast development. It is distinct from an alternative programme (skotomorphogenesis or etiolation) that occurs in the dark.

Bundle sheath cells

Cells in the interior of leaves that are closely associated with the vasculature and have specialized functions in photosynthate loading of the vasculature. In C4 photosynthesis plants such as maize, they are the exclusive site of CO2 fixation by RuBisCo.

Auxin

A plant growth hormone that, although necessary for leaf development, counteracts cytokinin action in aerial tissues and therefore represses greening and chloroplast development.

Cytokinin

A plant hormone that, in aerial tissues, is associated with cell proliferation but also promotes greening and chloroplast development.

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Jarvis, P., López-Juez, E. Biogenesis and homeostasis of chloroplasts and other plastids. Nat Rev Mol Cell Biol 14, 787–802 (2013). https://doi.org/10.1038/nrm3702

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