Review
Plastoglobules: versatile lipoprotein particles in plastids

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Plastoglobules are plastid-localized lipoprotein particles that contain tocopherols and other lipid isoprenoid-derived metabolites, as well as structural proteins named plastoglobulins. Surprisingly, recent publications show that plastoglobules contain enzymes involved in the metabolism of these secondary metabolites, as well as enzymes of unknown function. The size and number of plastoglobules vary during plastid development and differentiation, and strongly increase during light stress, senescence and in mutants blocked in thylakoid formation. Given that plastoglobules are contiguous with the outer lipid leaflet of the thylakoid membrane, it is highly plausible that a function of plastoglobules is the active channeling of lipid molecules and lipid breakdown products. Understanding the function of plastoglobules should provide a foundation for improving the nutritional value and yield of plants.

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History of plastoglobule research and discovery

Early electron microscopic studies revealed the presence of ‘osmiophilic globuli’ inside chloroplasts (Figure 1) and chromoplasts, as well as other plastid types [1]. The diameter of these bodies, later termed plastoglobules, ranges from 30 nm to 5 μm. These plastoglobules could be conveniently isolated by flotation density centrifugation because of their relatively high lipid content 1, 2. The lipid composition of plastoglobules has been determined in several plant species – it consists mainly

Plastoglobule composition

Plastoglobules isolated from chloroplasts are known to contain the prenyl quinones, including plastoquinone and phylloquinone and α-tocopherol 1, 2, 9, 17. Data from a recent study have shown that a significant fraction of phylloquinone (vitamin K1) in chloroplasts is not associated with photosystem I, but locates to plastoglobules [18]. This suggests that plastoglobules are a sink for the deposit of excess phylloquinone and its precursors. Whereas galactolipids have been detected in

Plastoglobule proteome

The advancement of proteomics and biological mass spectrometry greatly helped in the identification of plastoglobule proteins and functions. Thirty-four proteins are considered candidates for genuine plastoglobule proteins based on their experimental identification in purified plastoglobules isolated from Arabidopsis thaliana chloroplasts 24, 25. Twenty-three of the proteins were found in both of the two independent studies. The identified proteins fall into three categories:

Plastoglobulins

The plastoglobulin/PAP/fibrillin family in Arabidopsis consists of thirteen genes [3]. Eight members of this family were identified in the plastoglobule proteome, suggesting that the majority of the plastoglobulins/PAPs/fibrillins function in plastoglobules. Moreover, expression of several of the identified plastoglobulins fused to GFP gave punctuate fluorescence patterns consistent with plastoglobule localization [24]. Several names have been used to describe these proteins and, for clarity,

Chloroplast metabolic enzymes

Although the presence of plastoglobulins was not unexpected, the identification of known metabolic enzymes was surprising given that plastoglobules were generally considered passive lipid storage bodies 9, 19. Three chloroplast enzymes involved in biosynthetic pathways related to stress responses were identified: the allene oxide synthase implicated in jasmonate synthesis, a 9-cis-epoxycarotenoid dioxygenase that might participate in carotenoid and ABA metabolism, and tocopherol cyclase (VTE1,

Metabolic enzymes in plastoglobules of chromoplasts in red pepper

Chromoplasts of ripe red peppers do not contain thylakoid membranes or chlorophylls, but instead accumulate large amounts of carotenoids that are mostly sequestered in fibrillar plastoglobules [16]. Proteome analysis of isolated plastoglobules from the chromoplasts of ripe red peppers identified ζ-carotene desaturase, lycopene β-cyclase, and two β-carotene β-hydroxylases operating in series in bicyclic carotenoid biosynthesis [25]. This suggests that plastoglobules in chromoplasts have a

Unclassified proteins in plastoglobules

Among the 20 unclassified plastoglobule proteins, six are putatively involved in quinone synthesis and two in general lipid metabolism on the basis of predicted functional domains (Table 1). The four ABC1 kinases might function in regulation of quinone synthesis, based on the role of their homologs in Escherichia coli and Saccharomyces cerevisiae (see Ref. [25] for discussion). Their substrates and products are currently not known. The key to understanding their enzymatic function could be the

Ultrastructure of plastoglobules

Given that plastoglobules participate in various metabolic pathways as well as in lipid storage, the question arises as to how these lipids can be transferred to and from the thylakoid membranes. Plastoglobules often appear in close proximity to thylakoid membranes and physical connections have been reported. Electron tomography has shown that virtually all plastoglobules are attached to thylakoids, some of them directly and others via a network of interconnected plastoglobules [30]. Moreover,

Involvement of plastoglobules in stress response

The first indications that plastoglobules are involved in stress responses came from ultra-structural observations. Indeed, several studies have reported the presence of larger and more numerous plastoglobules in chloroplasts from plants grown under diverse stress conditions 39, 40, 41, 42, 43, 44, 45, 46, 47. In addition, the expression of PGL genes has been shown to be modulated by diverse stress stimuli such as exposure to reactive oxygen species 48, 49 or ozone [50], ABA induction 51, 52,

Integration of plastoglobule functions with chloroplast metabolism and stress responses

The recent publications have laid a foundation for the molecular understanding of plastoglobule functions in chloroplast and chromoplast secondary metabolism and stress responses. These discoveries strongly suggest that plastoglobules actively participate in diverse secondary metabolism pathways and stress responses and, thus, are not merely a ‘passive storage’ compartment but rather versatile particles. However, the plastoglobule-localized metabolic activities are part of larger networks of

Acknowledgements

We thank Michèle Vlimant (Laboratory of Animal Physiology, Neuchâtel) for her skilled help in electron microscopy. Funding was provided to K.J.V.W. by the US Department of Agriculture (USDA-Plants and Environment #0195698). C.B. and F.K. thank the Swiss National Center for Competence in Research (NCCR Plant Survival) and the University of Neuchâtel for financial support.

References (62)

  • F. Eymery et al.

    Immunocytolocalization of CDSP 32 and CDSP 34, two chloroplastic drought-induced stress proteins in Solanum tuberosum plants

    Plant Physiol. Biochem.

    (1999)
  • E. Paakkonen

    Differences in growth, leaf senescence and injury, and stomatal density in birch (Betula pendula Roth.) in relation to ambient levels of ozone in Finland

    Environ. Pollut.

    (1997)
  • S. Duret

    Cadmium-induced ultrastructural changes in Euglena cells

    Environ. Res.

    (1986)
  • N. Manac’h et al.

    Stress induction of a nuclear gene encoding for a plastid protein is mediated by photo-oxidative events

    Plant Physiol. Biochem.

    (1999)
  • J. Hirschberg

    Carotenoid biosynthesis in flowering plants

    Curr. Opin. Plant Biol.

    (2001)
  • J.L. Bailey et al.

    The osmiophilic globules of chloroplasts. II. Globules of the spinach-beet chloroplast

    Biochim. Biophys. Acta

    (1963)
  • Y. Laizet

    Subfamily organization and phylogenetic origin of genes encoding plastid lipid-associated proteins of the fibrillin type

    J. Genome Sci. Tech.

    (2004)
  • R. Rinnan et al.

    Ozone effects on the ultrastructure of peatland plants: Sphagnum mosses, Vaccinium oxycoccus, Andromeda polifolia and Eriophorum vaginatum

    Ann. Bot. (Lond.)

    (2004)
  • A. Katz

    Isolation and characterization of a protein associated with carotene globules in the alga Dunaliella bardawil

    Plant Physiol.

    (1995)
  • M. Schmidt

    Proteomic analysis of the eyespot of Chlamydomonas reinhardtii provides novel insights into its components and tactic movements

    Plant Cell

    (2006)
  • G. Stanier

    Fine structure of cyanobacteria

  • H.K. Lichtenthaler et al.

    Plastoglobuli in Verschiedenen Differenzierungsstadien der Plastiden bei Allium cepa L

    Planta (Berl.)

    (1967)
  • H.K. Lichtenthaler

    Plastoglobuli and the fine structure of plastids

    Endeavor

    (1968)
  • B. Sprey et al.

    Zur Frage der Beziehungen zwischen Plastoglobuli und Thylakoidgenese in Gerstenkeimlingen

    Z. Naturforschg

    (1966)
  • J.J. Guiamét

    Mass exodus from senescing soybean chloroplasts

    Plant Cell Physiol.

    (1999)
  • A. Rudella

    Downregulation of ClpR2 leads to reduced accumulation of the ClpPRS protease complex and defects in chloroplast biogenesis in Arabidopsis

    Plant Cell

    (2006)
  • D. Kroll

    VIPP1, a nuclear gene of Arabidopsis thaliana essential for thylakoid membrane formation

    Proc. Natl. Acad. Sci. U. S. A.

    (2001)
  • J. Deruere

    Fibril assembly and carotenoid overaccumulation in chromoplasts: a model for supramolecular lipoprotein structures

    Plant Cell

    (1994)
  • D. Steinmüller et al.

    Composition and function of plastoglobuli. I. Isolation and purification from chloroplasts and chromoplasts

    Planta

    (1985)
  • M. Tevini et al.

    Composition and function of plastoglobuli. II. Lipid composition of leaves and plastoglobuli during beech leaf senescence

    Planta

    (1985)
  • N. Gaude

    Nitrogen deficiency in Arabidopsis affects galactolipid composition and gene expression and results in accumulation of fatty acid phytyl esters

    Plant J.

    (2007)

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