Planta

, Volume 237, Issue 2, pp 463–470 | Cite as

A mechanism implicating plastoglobules in thylakoid disassembly during senescence and nitrogen starvation

Review

Abstract

Plastoglobules are lipid droplets present in all plastid types. In chloroplasts, they are connected to the thylakoid membrane by the outer lipid half-bilayer. The plastoglobule core is composed of neutral lipids most prominently the prenylquinones, triacylglycerols, fatty acid phytyl esters but likely also unknown compounds. During stress and various developmental stages such as senescence, plastoglobule size and number increase due to the accumulation of lipids. However, their role is not limited to lipid storage. Indeed, the characterization of the plastoglobule proteome revealed the presence of enzymes. Importantly it has been demonstrated that these participate in isoprenoid lipid metabolic pathways at the plastoglobule, notably in the metabolism of prenylquinones. Recently, the characterization of two phytyl ester synthases has established a firm metabolic link between PG enzymatic activity and thylakoid disassembly during chloroplast senescence and nitrogen starvation.

Keywords

Chloroplast Fatty acid phytyl ester Plastoglobule lipid droplets Prenylquinones Senescence Thylakoid membranes 

Abbreviations

ABC1

Activity of BC1

AOS

Allene oxide synthase

DGAT

Diacylglycerol acyltransferase

DMPBQ

2,3-Dimethyl-5-phytyl-1,4-benzoquinol

FAPEs

Fatty acids phytyl esters

FBN

Fibrillin

JA

Jasmonate

NDC1

Nicotinamide adenine dinucleotide phosphate (NADPH) dehydrogenase C1

OPDA

12-Oxophytodienoic acid

PG

Plastoglobule

PAP

Plastid-lipid-associated protein

PES

Phytyl ester synthases

PGL

Plastoglobulin

PQH2

Plastoquinol

ROS

Reactive oxygen species

SAG

Senescence associated gene

TAGs

Triacylglycerols

VTE1

Vitamin E cyclase

WT

Wild type

Introduction

Plastoglobules (PG) were discovered ~50 years ago by electron microscopy in plant tissues. Present in photosynthetic organisms (Greenwood et al. 1963; Leggett Bailey and Whyborn 1963), PG constitute a specific sub-organellar compartment in various types of plastids such as chloroplasts, chromoplasts and leucoplasts. Easily isolated by floatation on a sucrose gradient, these low density particles contain small amounts of protein, while the interior is filled with neutral lipids, often unsaturated (Vidi et al. 2006; Besagni et al. 2011). For this reason, PG readily react with osmium tetroxide which lead to their “osmiophile” characteristics in electron microscopy.

Structurally related to the oil droplets originating from the endoplasmic reticulum and storing triacylglycerol in their core (Huang 1992), PG arise at the margin of the stromal thylakoid membrane by a “blistering” mechanism and remain contiguous with the outer leaflet of thylakoid lipid bilayer (Austin et al. 2006).

Whereas in green chloroplasts, 95 % of the plastoglobules are single with diameters varying from 45 to 60 nm; in senescing and light stressed chloroplasts, PG tend to be much larger and form interconnected grape-like clusters (Austin et al. 2006). These interconnected PG clusters probably result from secondary blistering events at the surface of an existing PG. The observation of structural connections between the thylakoid membrane and PG and among PG suggests that bidirectional lipid trafficking occurs at the places of contact.

The PG core contains a varying range of neutral lipids including prenylquinones, triacylglycerols (TAGs), fatty acids phytyl esters (FAPEs), carotenoids and others. Plastoquinol (PQH2) and tocopherol (vitamin E) are the major constituents of the prenylquinone lipid family in plastoglobules, whereas phylloquinone (vitamin K) is also present but in minor concentrations (Lichtenthaler and Peveling 1966; Steinmuller and Tevini 1985; Austin et al. 2006; Lohmann et al. 2006; Gaude et al. 2007; Zbierzak et al. 2010; Lippold et al. 2012).

Conditions provoking oxidative stress such as high light, nitrate starvation, drought, high saline concentration, viral infection, chilling and ozone (Nordby and Yelenosky 1985; Locy et al. 1996; Rey et al. 2000; Oksanen et al. 2001; Gaude et al. 2007; Lichtenthaler 2007) or developmental stages such as senescence and fruit development (Kaup et al. 2002) result in the dismantling of thylakoid membrane. In parallel, the number and the size of lipid droplets increase, due to the accumulation of lipids in their hydrophobic core. However, the precise mechanisms here are not understood.

For many years, the observation that PG accumulate antioxidant molecules as well as catabolic products contributed to the idea that they represent a passive lipid storage site. However, since the characterization of the plastoglobule proteome from Arabidopsis chloroplasts and red-pepper chromoplasts, this idea has changed. The proteomics studies revealed the presence of proteins that can be attributed to three different groups: (1) structural proteins called fibrillins (FBN) or plastoglobulins (PGL), (2) enzymes involved in various lipid metabolic pathways and (3) uncharacterized proteins (Vidi et al. 2006; Ytterberg et al. 2006; Lundquist et al. 2012b).

Fibrillins

Fibrillins received their name from fibrils, the carotenoid-containing suborganellar structures of red-pepper chromoplasts that are derived from plastoglobules. The chromoplast fibrils not only contain apolar (carotenoids, tocopherol) and polar (galactolipids, phospholipids) lipids but also a dominant protein of 32 kD protein appropriately termed fibrillin (Deruere et al. 1994). Proteins similar in size were previously identified in the fibrils of Japanese rose (Wuttke 1976), Nasturtium (Winkenbach et al. 1976) and Palisota barteri (Knoth et al. 1986). The same group of proteins was later termed plastid–lipid associated protein (PAP), because of its localization not only both in chromoplasts but also in chloroplast plastoglobules and its association with lipid-containing structures (Pozueta-Romero et al. 1997). Independently, the fibrillin/PAP protein family localized in plastoglobules was referred to as plastoglobulins (Vidi et al. 2006).

In vitro reconstitution of fibrils by the addition of fibrillin to a mixture of carotenoids and polar lipids experiments suggested a structural function of fibrillin in fibril assembly (Deruere et al. 1994). However, the functions of fibrillins may also directly or indirectly extend to roles in hormonal responses, protection of the photosystem from oxidative stress, resistance to biotic and abiotic stresses or chromoplast pigment accumulation and even a role in lipid transport has been suggested (Singh and McNellis 2011).

Recently, a quantitative proteomics study of PG, identifying 30 proteins, indicated that the FBN are the most abundant PG proteins in Arabidopsis leaf rosettes (Lundquist et al. 2012b). Six FBN, including the four major FBN1a, 1b, 2 and 4 (At4g04020, At4g22240, At2g35490, and At3g23400, respectively) accounted for 53 % of the PG protein mass in Arabidopsis. Together with six ABC1 (activity of BC1)-like kinases (At5g05200, At4g31390, At1g79600, At1g71810, At3g24190, At3g07700), they make up more than 70 % of the PG protein. In addition, the plastoglobule proteome contains several other major components: CCD4 (carotenoid cleavage dioxygenase-At4g19170), VTE1 (tocopherol cyclase-At4g32770) and NDC1 (NAD(P)H dehydrogenase C1-At5g08740), which account for 3.3, 2.6 and 2.5 % of the protein mass, respectively. PES1 (At1g54570) and PES2 (At3g26840), two phytyl ester synthases represent 2.6 and 1.4 % of the proteome, respectively (Lippold et al. 2012). The remaining proteins account for <20 % of the protein mass. These include notably UbiE1 and UbiE2, two methyltransferases (At1g78140 and At2g41040, respectively), M48 protease (At3g27110), as well as a third esterase (At5g41120) related to PES1 and 2, which is described later in this review.

ABC1-like kinases

Among the proteins of the Arabidopsis PG proteome, ABC1-like kinases are among the most abundant (Vidi et al. 2006; Ytterberg et al. 2006; Lundquist et al. 2012b). Even though little is known about functions of the plastoglobule ABC1-like kinases in plants, the prototypical function of this family is the regulation of ubiquinone metabolism in bacteria and mitochondria (Lundquist et al. 2012a). Their mutation leads to accumulation of a ubiquinone precursor and to a shortage of ubiquinone (Cardazzo et al. 1998; Leonard et al. 1998; Poon et al. 2000). In S. cerevisiae, abc1 mutants have a mitochondrial respiratory defect that can be rescued by the addition of exogenous quinones (Bousquet et al. 1991; Brasseur et al. 1997). Moreover, ABC1 is able to complement the coq8 mutant that is defective in ubiquinone synthesis (Do et al. 2001). In bacteria, the ubiB gene homolog of ABC1 is required for the first monooxygenase step in ubiquinone synthesis (Poon et al. 2000). In humans, mutation of an ABC1-like homolog leads to neuromuscular defects such as ataxia (Mollet et al. 2008). Recently, two putative kinases have been characterized in Arabidopsis: AtOSA1 (Arabidopsis oxidative stress related ABC1-like protein, At5g64940) localized at the chloroplast inner envelope membrane (Jasinski et al. 2008) and AtACDO1 (ABC1-like kinase related to chlorophyll degradation and oxidative stress, At4g31390) (Yang et al. 2012). Both were linked to oxidative stress under high light conditions. Thus, the chloroplast localization together with the phenotypes and the analogy to mitochondrial and bacterial ABC1-like kinases suggests that plastoglobule ABC1-like kinase proteins regulate prenylquinone metabolism and that they may do so via phosphorylation of enzymes in the pathway (Ytterberg et al. 2006; Lundquist et al. 2012a). Indeed, in yeast, it has been demonstrated that ABC1/Coq8 is required for the phosphorylation of Coq3, Coq5 and Coq7, three enzymes involved in ubiquinone pathway. Moreover, the human Coq8 ortholog ADCK3 rescues the phosphorylation of several Coq proteins in the yeast coq8 mutant as well as the defective phenotype of the strain (Xie et al. 2011).

The following group of proteins, with regard to their abundance in the PG proteome, includes CCD4, which has been implicated in carotenoid degradation (Ahrazem et al. 2010). Further indications for the implication of plastoglobules in carotenoid metabolism stems come from the identification of z-carotene desaturase (ZDS), lycopene b-cyclase (LYC-b or CYC-b), and two b-carotene b-hydroxylases (CrtR-b) in the PG chromoplast proteome of tomato (Ytterberg et al. 2006) (Fig. 1c).
Fig. 1

Implication of plastoglobule enzymes in lipid metabolic pathways. a During high light stress, NDC1 and VTE1 are implicated in the synthesis and the recycling of prenylquinones (phylloquinones, plastoquinol (PQH2-9), plastochromanol (PC8), tocopherol). b During senescence, PES1 and PES2 synthesize fatty acid phytyl esters (FAPEs) from fatty acids (FA) and phytol, leading to plastoglobule enlargement and disassembly of the thylakoid membrane. c PG-localized enzymes are involved in carotenoid synthesis principally in chromoplasts

Implication of plastoglobules in isoprenoid synthesis

Immunoelectron tomographic studies performed on two Arabidopsis PG proteins, the plastoglobulin PGL35 (At4g04020) and the tocopherol cyclase VTE1 revealed that PG proteins are located at the surface of the PG, presumably in contact with the head group of the polar lipids (Austin et al. 2006). VTE1, even penetrated the polar lipid monolayer, and extended into the core of the PG potentially allowing it to access its hydrophobic substrates (Austin et al. 2006; Kobayashi and DellaPenna 2008; Mene-Saffrane et al. 2010).

The role of PG in isoprenoid metabolism is highlighted by two PG enzymes (Piller et al. 2012) (Fig. 1a): VTE1 and NDC1. Under oxidative stress, prenylquinone synthesis represents an important plant response to protect the thylakoid membranes against reactive oxygen species (ROS) (Gruszka et al. 2008). PG have now been implicated in the synthesis, storage and regeneration of these antioxidant molecules that include tocopherols, plastoquinone, plastochromanol and phylloquinone. PG may release and exchange prenylquinones with the thylakoid membranes through the attachment sites (Austin et al. 2006).

Tocopherol accumulates in plastoglobules under high light stress (Havaux et al. 2005; Brehelin et al. 2007) and may in part explain the enlargement of PG under such conditions. VTE1 mediates the conversion of 2,3-dimethyl-5-phytyl-1,4-benzoquinol (DMPBQ) into γ-tocopherol. While most of the VTE1 appears to be present in PG, the three enzymes (VTE2, 3, 4) catalyzing the other biosynthetic reactions have been localized to the chloroplast inner envelope membrane (Soll et al. 1985; Cheng et al. 2003; Vidi et al. 2006; Kobayashi and DellaPenna 2008; Zbierzak et al. 2010). VTE1 has also been implicated in the recycling of the tocopherol oxidation product, α-tocopherol quinone, that accumulates in response to oxidative stress (Kobayashi and DellaPenna 2008).

The NADPH dehydrogenase NDC1, localized at plastoglobules, has been implicated in the re-oxidation of the reduced pool of plastoquinol (PQH2-9) accumulated in plastoglobules during high light stress (Szymanska and Kruk 2010; Zbierzak et al. 2010; Piller et al. 2011). This pool can also serve as a substrate for VTE1 to produce plastochromanol-8 (Mene-Saffrane et al. 2010; Szymanska and Kruk 2010; Zbierzak et al. 2010). A role of NDC1 in the biosynthesis of phylloquinone has also been demonstrated using a non-targeted lipidomic analysis of the ndc1 mutant. The ndc1 mutant completely lacked phylloquinone but accumulated its immediate precursor, demethyl-phylloquinone instead (Piller et al. 2011). The enzyme AtMENG, which catalyzes this methylation, had been identified previously (Lohmann et al. 2006) and was normally expressed in the ndc1 mutant. The mechanism of NDC1 in phylloquinone synthesis currently remains unknown.

Role of plastoglobules during leaf senescence

The implication of PG in the storage of catabolic molecules produced during senescence and nitrogen starvation has been described previously (Kaup et al. 2002; Gaude et al. 2007). However, the characterization of two PG acyl transferases has led to an advance in mechanistic understanding of the accumulation of fatty acid phytyl esters and triacylglycerols (Fig. 1b).

Senescence is essentially a highly coordinated cascade of events leading to cell death. During this process, leaf cells undergo series of changes in gene expression, metabolism and structure, which lead to a decline in photosynthetic activity and loss of chlorophyll. However, variations in the symptoms of senescence exist and leaves may remain green longer than normal in certain mutants. Functional stay-greens genotypes or mutants retain both chlorophyll and photosynthetic competence, whereas cosmetic stay-greens retain their chlorophyll but loose photosynthetic activity (Hortensteiner 2009).

Senescence is controlled by environmental and autonomous factors (Gan and Amasino 1997; Quirino et al. 2000). Internal factors include age, phytohormones and reproductive development, whereas external cues include stress conditions such as nutrient deficiency, pathogen infection, drought, low and high temperature and shading. Thus, the expression patterns of numerous genes are common between such stress responses and leaf senescence (Lim et al. 2007).

Hormones provide a means for plants to signal and control leaf senescence. Indeed, cytokinines, ethylene, auxin, jasmonic acid (JA), abscisic acid and salicylic acid are key plant hormones mediating senescence in different ways. Stresses which affect the synthesis of these phytohormones or their exogenous application lead to a modification in gene expression underlying senescence (Weaver et al. 1998). For example, cytokinines delay senescence by a negative regulation of the promoter of the senescence-associated gene SAG12 (Gan and Amasino 1995). In contrary, exogenously applied ethylene induces premature leaf senescence in Arabidopsis, and ethylene insensitive mutants etr1-1 and ein2/ore3 showed increased leaf longevity (Guiboileau et al. 2010). Similarly, methyl jasmonate as well as its precursor JA lead to an increased expression of SAG genes including SAG14, SEN4, SEN5 and rVPE. Moreover, the JA-insensitive mutant coi1 (coronatine insensitive 1) is defective in JA-dependant senescence (He et al. 2002).

A large set of regulatory SAGs has been isolated from various plant species. Up-regulated during senescence, they trigger leaf senescence by signal perception and transduction such as receptor-like kinases and transcription factors (Quirino et al. 2000; Lim et al. 2007). Among at least 800 SAGs identified in Arabidopsis, 20 different families of transcription factors are significantly overexpressed during senescence. The largest groups being NAC, WRKY, C2H2-type zing finger and MYB proteins (Hinderhofer and Zentgraf 2001; Guo and Gan 2006). These transcription factors control the expression of many genes of senescence (Buchanan-Wollaston and Ainsworth 1997; Lin and Wu 2004). Among them, WRKY53 was shown to play a central role in early leaf-senescence and has various targets such as SAGs, PR genes, and additional WRKY factors. Indeed, the wrky53 mutant manifested a delay in senescence whereas overexpression caused precocious senescence (Miao et al. 2004).

During senescence, many of the SAGs regulate the catabolic events such as protein, lipid and nucleic acid degradation that ultimately lead to cell death (Thompson et al. 1998). However, this programmed cell death also coincides with a remobilization of nutrients (e.g. nitrogen and phosphorus) that are relocated from the senescing tissue to the developing seeds (Quirino et al. 2000). Thus, leaf senescence also has aspects of a recycling process important for re-production and plant fitness.

Probably the first visible manifestations of leaf senescence occur at the level of the chloroplast. The dismantling of the thylakoid membrane, which consists to 80 % of galactolipids, results in the release of free fatty acids. In parallel, chlorophyll is catabolized and free phytol is released by the pheophytin pheophorbide hydrolase (PPH) (Harris and Arnott 1973; Hortensteiner 2006). These hydrolytic products are considered toxic and can be metabolized to form fatty acid phytyl esters, tocopherols and triacylglycerols. All three of these accumulate in plastoglobules during senescence and nitrogen starvation (Kaup et al. 2002; Ischebeck et al. 2006; Vidi et al. 2006; Gaude et al. 2007).

The chlorophyll catabolic pathway (Hortensteiner 2006) as well as the incorporation of phytol into tocopherol via phosphorylation by the phytol kinase VTE5 (Valentin et al. 2006) are well documented. However, the conversion mechanism of phytol to fatty acid phytyl esters was unclear until the recent characterization of two PG enzymes, phytyl ester synthase, PES1 and PES2. These two acyltransferase proteins, up-regulated during senescence and nitrogen starvation, belong to the ELT (esterase/lipase/thioesterase) family that includes six members in Arabidopsis. They can esterify either diacylglycerol or the phytol (stemming from degradation of the thylakoid membrane and the chlorophyll) with free fatty acids, resulting in the formation of triacylglycerols and FAPEs, respectively (Lippold et al. 2012). According to the nature of the acyl groups in phytyl ester and triacylglycerols, fatty acids may be derived from de novo synthesis or galactolipid degradation which provides a pool enriched in fatty acids C16:3 and C18:3 (Browse et al. 1986).

In the pes1pes2 double mutant under nitrogen starvation, the amount of FAPEs was reduced by 85 % suggesting that these two enzymes play a major role (Lippold et al. 2012). In contrary, the amount of TAGs in the mutant leaves is only 30 % lower, certainly due to the implication of other diacylglycerol acyltransferase enzymes such as DGAT1 (Zou et al. 1999; Dahlqvist et al. 2000; Lardizabal et al. 2001; Kaup et al. 2002). Moreover, in the updated and quantitative plastoglobule proteome study published recently by Lundquist and colleagues, in addition to PES1 and 2, a third esterase (At5g41120) was identified that may also participate in the synthesis of FAPEs and TAGs in plastoglobules (Lundquist et al. 2012b).

Phenotypically, a delay in senescence, but not a stay green phenotype, is observed in pes1pes2 double mutant. It is characterized by the persistence of a pale green phenotype for a longer period of time than in the wild type. This pale green phenotype correlates with the retention of a thylakoid membrane network, which could explain the presence of residual chlorophyll (Lippold et al. 2012). The presence of a predicted hydrolase domain of the α/β-superfamily in PES1 and 2 proteins in addition to the esterase domain suggests that these two proteins may also have lipase activity and be directly involved in galactolipid catabolism.

Fatty acids C18:3 and C16:3 originate from galactolipid degradation and are precursors for jasmonate biosynthesis (Gfeller et al. 2010). This phytohormone is not only involved in stress resistance (e.g. wounding, pathogen attack) but also in senescence induction (Shan et al. 2011). Allene oxide synthase (AOS), a key enzyme in jasmonate biosynthesis was originally identified in two proteome studies (Vidi et al. 2006; Ytterberg et al. 2006), but had already been reported to associate with chloroplast inner envelope membrane in tomato (Froehlich et al. 2001) and in Arabidopsis (Ferro et al. 2010). Thus, despite the clear presence of AOS in plastoglobules, it can not consider a bona fide plastoglobule protein due its presence in other chloroplast membrane compartments (Lundquist et al. 2012a). Nevertheless, the presence of AOS in plastoglobules, which catalyzes the formation of jasmonate precursor 12-oxophytodienoic acid (OPDA), suggests that plastoglobules may also participate in the production of jasmonate during senescence.

Moreover, under high light and low temperature, it has been demonstrated that the production of jasmonate is linked to the presence of fibrillins in PG. Indeed, the addition of jasmonate rescues the mutant phenotype of fib12 RNAi plants, characterized by a retarded shoot growth, a deficit in anthocyanin accumulation and increased oxidative stress symptoms. In addition, the number of PG is lower in fib12 RNAi plants than in wild type plants, concomitant with a reduction of TAGs in PG that makes less C18:3 fatty acid, the precursor of jasmonate, available in plastids. Indeed, the fibrillins in PG could influence early steps of jasmonate synthesis during stress (Youssef et al. 2010).

Finally, the identification of an unknown SAG protein in the plastoglobule proteome and a M48 protease in the same co-expression network as PES1 and 2 (termed “senescence module” by Lundquist et al.) firmly anchors plastoglobules in the senescence program (Lundquist et al. 2012b).

Conclusions

PG are lipoprotein particles that serve as an active lipid reservoir during stresses such as high light or during senescence. The characterization of the PG proteome revealed the presence of enzymes that provide PG with enzymatic capability for lipid synthesis (Vidi et al. 2006; Ytterberg et al. 2006; Lundquist et al. 2012b).

The Arabidopsis PG proteome contains three groups of proteins: fibrillins, enzymes involved in various lipid metabolic pathways and uncharacterized proteins. Among these PG proteins, fibrillins and ABC-like kinases constitute the most abundant families (Lundquist et al. 2012b).

In particular, the important role of PG proteins in prenylquinone metabolism is now well established notably via the characterization of NDC1 and the discovery of new aspects of VTE1 function (Vidi et al. 2006; Szymanska and Kruk 2010; Zbierzak et al. 2010; Piller et al. 2011, 2012).

Furthermore, the concomitant presence of proteins overexpressed during senescence (e.g. SAG, PES1/-2, M48) and implicated in jasmonate synthesis (AOS, FIB1-2) as well as co-expression networks strongly support a role for PG in the senescence process (Lundquist et al. 2012b). The mechanisms by which these actors influence senescence are still far from fully known. However, it is has now become clear that the PES1 and PES2 activities through their role in the biosynthesis of fatty acid phytyl esters and triacylglycerols are major contributors to thylakoid disassembly and plastoglobule enlargement during senescence and nitrogen deprivation.

Notes

Acknowledgments

We wish to thank Charles Andrès for his help with the elaboration of the manuscript. F.E.K. thanks the Université de Neuchâtel, SystemsX PGCE and NCCR Plant Survival and the SNF Grants 31003A_127380 and 31003_141229.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Ahrazem O, Trapero A, Gomez MD, Rubio-Moraga A, Gomez–Gomez L (2010) Genomic analysis and gene structure of the plant carotenoid dioxygenase 4 family: a deeper study in Crocus sativus and its allies. Genomics 96:239–250PubMedCrossRefGoogle Scholar
  2. Austin JR 2nd, Frost E, Vidi PA, Kessler F, Staehelin LA (2006) Plastoglobules are lipoprotein subcompartments of the chloroplast that are permanently coupled to thylakoid membranes and contain biosynthetic enzymes. Plant Cell 18:1693–1703PubMedCrossRefGoogle Scholar
  3. Besagni C, Piller LE, Brehelin C (2011) Preparation of plastoglobules from Arabidopsis plastids for proteomic analysis and other studies. Methods Mol Biol 775:223–239PubMedCrossRefGoogle Scholar
  4. Bousquet I, Dujardin G, Slonimski PP (1991) ABC1, a novel yeast nuclear gene has a dual function in mitochondria: it suppresses a cytochrome b mRNA translation defect and is essential for the electron transfer in the bc 1 complex. EMBO J 10:2023–2031PubMedGoogle Scholar
  5. Brasseur G, Tron G, Dujardin G, Slonimski PP, Brivet-Chevillotte P (1997) The nuclear ABC1 gene is essential for the correct conformation and functioning of the cytochrome bc1 complex and the neighbouring complexes II and IV in the mitochondrial respiratory chain. Eur J Biochem 246:103–111PubMedCrossRefGoogle Scholar
  6. Brehelin C, Kessler F, van Wijk KJ (2007) Plastoglobules: versatile lipoprotein particles in plastids. Trends Plant Sci 12:260–266PubMedCrossRefGoogle Scholar
  7. Browse J, Warwick N, Somerville CR, Slack CR (1986) Fluxes through the prokaryotic and eukaryotic pathways of lipid synthesis in the ‘16:3’ plant Arabidopsis thaliana. Biochem J 235:25–31PubMedGoogle Scholar
  8. Buchanan-Wollaston V, Ainsworth C (1997) Leaf senescence in Brassica napus: cloning of senescence related genes by subtractive hybridisation. Plant Mol Biol 33:821–834PubMedCrossRefGoogle Scholar
  9. Cardazzo B, Hamel P, Sakamoto W, Wintz H, Dujardin G (1998) Isolation of an Arabidopsis thaliana cDNA by complementation of a yeast abc1 deletion mutant deficient in complex III respiratory activity. Gene 221:117–125PubMedCrossRefGoogle Scholar
  10. Cheng Z, Sattler S, Maeda H, Sakuragi Y, Bryant DA, DellaPenna D (2003) Highly divergent methyltransferases catalyze a conserved reaction in tocopherol and plastoquinone synthesis in cyanobacteria and photosynthetic eukaryotes. Plant Cell 15:2343–2356PubMedCrossRefGoogle Scholar
  11. Dahlqvist A, Stahl U, Lenman M, Banas A, Lee M, Sandager L, Ronne H, Stymne S (2000) Phospholipid:diacylglycerol acyltransferase: an enzyme that catalyzes the acyl-CoA-independent formation of triacylglycerol in yeast and plants. Proc Natl Acad Sci USA 97:6487–6492PubMedCrossRefGoogle Scholar
  12. Deruere J, Romer S, d’Harlingue A, Backhaus RA, Kuntz M, Camara B (1994) Fibril assembly and carotenoid overaccumulation in chromoplasts: a model for supramolecular lipoprotein structures. Plant Cell 6:119–133PubMedGoogle Scholar
  13. Do TQ, Hsu AY, Jonassen T, Lee PT, Clarke CF (2001) A defect in coenzyme Q biosynthesis is responsible for the respiratory deficiency in Saccharomyces cerevisiae abc1 mutants. J Biol Chem 276:18161–18168PubMedCrossRefGoogle Scholar
  14. Ferro M, Brugiere S, Salvi D, Seigneurin-Berny D, Court M, Moyet L, Ramus C, Miras S, Mellal M, Le Gall S, Kieffer-Jaquinod S, Bruley C, Garin J, Joyard J, Masselon C, Rolland N (2010) AT_CHLORO, a comprehensive chloroplast proteome database with subplastidial localization and curated information on envelope proteins. Mol Cell Proteomics 9:1063–1084PubMedCrossRefGoogle Scholar
  15. Froehlich JE, Itoh A, Howe GA (2001) Tomato allene oxide synthase and fatty acid hydroperoxide lyase, two cytochrome P450s involved in oxylipin metabolism, are targeted to different membranes of chloroplast envelope. Plant Physiol 125:306–317PubMedCrossRefGoogle Scholar
  16. Gan S, Amasino RM (1995) Inhibition of leaf senescence by autoregulated production of cytokinin. Science 270:1986–1988PubMedCrossRefGoogle Scholar
  17. Gan S, Amasino RM (1997) Making sense of senescence (Molecular genetic regulation and manipulation of leaf senescence). Plant Physiol 113:313–319PubMedGoogle Scholar
  18. Gaude N, Brehelin C, Tischendorf G, Kessler F, Dormann P (2007) Nitrogen deficiency in Arabidopsis affects galactolipid composition and gene expression and results in accumulation of fatty acid phytyl esters. Plant J 49:729–739PubMedCrossRefGoogle Scholar
  19. Gfeller A, Dubugnon L, Liechti R, Farmer EE (2010) Jasmonate biochemical pathway. Sci Signal 3: cm3Google Scholar
  20. Greenwood AD, Leech RM, Williams JP (1963) Osmiophilic globules of chloroplasts. 1. Osmiophilic globules as a normal component of chloroplasts and their isolation and composition in Vicia faba L. Biochim Biophys Acta 78:148–162CrossRefGoogle Scholar
  21. Gruszka J, Pawlak A, Kruk J (2008) Tocochromanols, plastoquinol, and other biological prenyllipids as singlet oxygen quenchers-determination of singlet oxygen quenching rate constants and oxidation products. Free Radical Biol Med 45:920–928CrossRefGoogle Scholar
  22. Guiboileau A, Sormani R, Meyer C, Masclaux-Daubresse C (2010) Senescence and death of plant organs: nutrient recycling and developmental regulation. C R Biol 333:382–391PubMedCrossRefGoogle Scholar
  23. Guo Y, Gan S (2006) AtNAP, a NAC family transcription factor, has an important role in leaf senescence. Plant J 46:601–612PubMedCrossRefGoogle Scholar
  24. Harris JB, Arnott HJ (1973) Effects of senescence on chloroplasts of the tobacco leaf. Tissue Cell 5:527–544PubMedCrossRefGoogle Scholar
  25. Havaux M, Eymery F, Porfirova S, Rey P, Dormann P (2005) Vitamin E protects against photoinhibition and photooxidative stress in Arabidopsis thaliana. Plant Cell 17:3451–3469PubMedCrossRefGoogle Scholar
  26. He Y, Fukushige H, Hildebrand DF, Gan S (2002) Evidence supporting a role of jasmonic acid in Arabidopsis leaf senescence. Plant Physiol 128:876–884PubMedCrossRefGoogle Scholar
  27. Hinderhofer K, Zentgraf U (2001) Identification of a transcription factor specifically expressed at the onset of leaf senescence. Planta 213:469–473PubMedCrossRefGoogle Scholar
  28. Hortensteiner S (2006) Chlorophyll degradation during senescence. Annu Rev Plant Biol 57:55–77PubMedCrossRefGoogle Scholar
  29. Hortensteiner S (2009) Stay-green regulates chlorophyll and chlorophyll-binding protein degradation during senescence. Trends Plant Sci 14:155–162PubMedCrossRefGoogle Scholar
  30. Huang AHC (1992) Oil bodies and oleosins in seeds. Annu Rev Plant Physiol Plant Mol Biol 43:177–200CrossRefGoogle Scholar
  31. Ischebeck T, Zbierzak AM, Kanwischer M, Dormann P (2006) A salvage pathway for phytol metabolism in Arabidopsis. J Biol Chem 281:2470–2477PubMedCrossRefGoogle Scholar
  32. Jasinski M, Sudre D, Schansker G, Schellenberg M, Constant S, Martinoia E, Bovet L (2008) AtOSA1, a member of the Abc1-like family, as a new factor in cadmium and oxidative stress response. Plant Physiol 147:719–731PubMedCrossRefGoogle Scholar
  33. Kaup MT, Froese CD, Thompson JE (2002) A role for diacylglycerol acyltransferase during leaf senescence. Plant Physiol 129:1616–1626PubMedCrossRefGoogle Scholar
  34. Knoth R, Hansmann P, Sitte P (1986) Chromoplasts of Palisota barteri, and the molecular structure of chromoplast tubules. Planta 168:167–174Google Scholar
  35. Kobayashi N, DellaPenna D (2008) Tocopherol metabolism, oxidation and recycling under high light stress in Arabidopsis. Plant J 55:607–618PubMedCrossRefGoogle Scholar
  36. Lardizabal KD, Mai JT, Wagner NW, Wyrick A, Voelker T, Hawkins DJ (2001) DGAT2 is a new diacylglycerol acyltransferase gene family: purification, cloning, and expression in insect cells of two polypeptides from Mortierella ramanniana with diacylglycerol acyltransferase activity. J Biol Chem 276:38862–38869PubMedCrossRefGoogle Scholar
  37. Leggett Bailey J, Whyborn AG (1963) Osmiophilic globules of chloroplasts II. Globules of spinach beet chloroplast. Biochim Biophys Acta 78:163–174CrossRefGoogle Scholar
  38. Leonard CJ, Aravind L, Koonin EV (1998) Novel families of putative protein kinases in bacteria and archaea: evolution of the “eukaryotic” protein kinase superfamily. Genome Res 8:1038–1047PubMedGoogle Scholar
  39. Lichtenthaler HK (2007) Biosynthesis, accumulation and emission of carotenoids, alpha-tocopherol, plastoquinone, and isoprene in leaves under high photosynthetic irradiance. Photosynth Res 92:163–179PubMedCrossRefGoogle Scholar
  40. Lichtenthaler HK, Peveling E (1966) Osmiophile Lipideinschlusse in den Chloroplasten und im Cytoplasma von Hoya carnosa R Br. Naturwissenschaften 53:534PubMedCrossRefGoogle Scholar
  41. Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 58:115–136PubMedCrossRefGoogle Scholar
  42. Lin JF, Wu SH (2004) Molecular events in senescing Arabidopsis leaves. Plant J 39:612–628PubMedCrossRefGoogle Scholar
  43. Lippold F, Vom Dorp K, Abraham M, Holzl G, Wewer V, Yilmaz JL, Lager I, Montandon C, Besagni C, Kessler F, Stymne S, Dormann P (2012) Fatty acid phytyl ester synthesis in chloroplasts of Arabidopsis. Plant Cell 24:2001–2014PubMedCrossRefGoogle Scholar
  44. Locy RD, Chang CC, Nielsen BL, Singh NK (1996) Photosynthesis in salt-adapted heterotrophic tobacco cells and regenerated plants. Plant Physiol 110:321–328PubMedGoogle Scholar
  45. Lohmann A, Schottler MA, Brehelin C, Kessler F, Bock R, Cahoon EB, Dormann P (2006) Deficiency in phylloquinone (vitamin K1) methylation affects prenyl quinone distribution, photosystem I abundance, and anthocyanin accumulation in the Arabidopsis AtmenG mutant. J Biol Chem 281:40461–40472PubMedCrossRefGoogle Scholar
  46. Lundquist PK, Davis JI, van Wijk KJ (2012a) ABC1K atypical kinases in plants: filling the organellar kinase void. Trends Plant Sci 17:546–555PubMedCrossRefGoogle Scholar
  47. Lundquist PK, Poliakov A, Bhuiyan NH, Zybailov B, Sun Q, van Wijk KJ (2012b) The functional network of the Arabidopsis plastoglobule proteome based on quantitative proteomics and genome-wide coexpression analysis. Plant Physiol 158:1172–1192PubMedCrossRefGoogle Scholar
  48. Mene-Saffrane L, Jones AD, DellaPenna D (2010) Plastochromanol-8 and tocopherols are essential lipid-soluble antioxidants during seed desiccation and quiescence in Arabidopsis. Proc Natl Acad Sci USA 107:17815–17820PubMedCrossRefGoogle Scholar
  49. Miao Y, Laun T, Zimmermann P, Zentgraf U (2004) Targets of the WRKY53 transcription factor and its role during leaf senescence in Arabidopsis. Plant Mol Biol 55:853–867PubMedGoogle Scholar
  50. Mollet J, Delahodde A, Serre V, Chretien D, Schlemmer D, Lombes A, Boddaert N, Desguerre I, de Lonlay P, de Baulny HO, Munnich A, Rotig A (2008) CABC1 gene mutations cause ubiquinone deficiency with cerebellar ataxia and seizures. Am J Hum Genet 82:623–630PubMedCrossRefGoogle Scholar
  51. Nordby HE, Yelenosky G (1985) Change in citrus leaf lipids during freeze-thaw stress. Phytochemistry 24:1675–1679CrossRefGoogle Scholar
  52. Oksanen E, Sober J, Karnosky DF (2001) Impacts of elevated CO2 and/or O3 on leaf ultrastructure of aspen (Populus tremuloides) and birch (Betula papyrifera) in the aspen FACE experiment. Environ Pollut 115:437–446PubMedCrossRefGoogle Scholar
  53. Piller LE, Besagni C, Ksas B, Rumeau D, Brehelin C, Glauser G, Kessler F, Havaux M (2011) Chloroplast lipid droplet type II NAD(P)H quinone oxidoreductase is essential for prenylquinone metabolism and vitamin K1 accumulation. Proc Natl Acad Sci USA 108:14354–14359CrossRefGoogle Scholar
  54. Piller LE, Abraham M, Dormann P, Kessler F, Besagni C (2012) Plastid lipid droplets at the crossroads of prenylquinone metabolism. J Exp Bot 63:1609–1618CrossRefGoogle Scholar
  55. Poon WW, Davis DE, Ha HT, Jonassen T, Rather PN, Clarke CF (2000) Identification of Escherichia coli ubiB, a gene required for the first monooxygenase step in ubiquinone biosynthesis. J Bacteriol 182:5139–5146PubMedCrossRefGoogle Scholar
  56. Pozueta-Romero J, Rafia F, Houlne G, Cheniclet C, Carde JP, Schantz ML, Schantz R (1997) A ubiquitous plant housekeeping gene, PAP, encodes a major protein component of bell pepper chromoplasts. Plant Physiol 115:1185–1194PubMedCrossRefGoogle Scholar
  57. Quirino BF, Noh YS, Himelblau E, Amasino RM (2000) Molecular aspects of leaf senescence. Trends Plant Sci 5:278–282PubMedCrossRefGoogle Scholar
  58. Rey P, Gillet B, Romer S, Eymery F, Massimino J, Peltier G, Kuntz M (2000) Overexpression of a pepper plastid lipid-associated protein in tobacco leads to changes in plastid ultrastructure and plant development upon stress. Plant J 21:483–494PubMedCrossRefGoogle Scholar
  59. Shan X, Li C, Peng W, Gao B (2011) New perspective of jasmonate function in leaf senescence. Plant Signal Behav 6:575–577PubMedCrossRefGoogle Scholar
  60. Singh DK, McNellis TW (2011) Fibrillin protein function: the tip of the iceberg? Trends Plant Sci 16:432–441PubMedCrossRefGoogle Scholar
  61. Soll J, Schultz G, Joyard J, Douce R, Block MA (1985) Localization and synthesis of prenylquinones in isolated outer and inner envelope membranes from spinach chloroplasts. Arch Biochem Biophys 238:290–299PubMedCrossRefGoogle Scholar
  62. Steinmuller D, Tevini M (1985) Composition and function of plastoglobuli. 1. Isolation and purification from chloroplasts and chromoplasts. Planta 163:201–207CrossRefGoogle Scholar
  63. Szymanska R, Kruk J (2010) Plastoquinol is the main prenyllipid synthesized during acclimation to high light conditions in Arabidopsis and is converted to plastochromanol by tocopherol cyclase. Plant Cell Physiol 51:537–545PubMedCrossRefGoogle Scholar
  64. Thompson JE, Froese CD, Madey E, Smith MD, Hong Y (1998) Lipid metabolism during plant senescence. Prog Lipid Res 37:119–141PubMedCrossRefGoogle Scholar
  65. Valentin HE, Lincoln K, Moshiri F, Jensen PK, Qi Q, Venkatesh TV, Karunanandaa B, Baszis SR, Norris SR, Savidge B, Gruys KJ, Last RL (2006) The Arabidopsis vitamin E pathway gene5-1 mutant reveals a critical role for phytol kinase in seed tocopherol biosynthesis. Plant Cell 18:212–224PubMedCrossRefGoogle Scholar
  66. Vidi PA, Kanwischer M, Baginsky S, Austin JR, Csucs G, Dormann P, Kessler F, Brehelin C (2006) Tocopherol cyclase (VTE1) localization and vitamin E accumulation in chloroplast plastoglobule lipoprotein particles. J Biol Chem 281:11225–11234PubMedCrossRefGoogle Scholar
  67. Weaver LM, Gan S, Quirino B, Amasino RM (1998) A comparison of the expression patterns of several senescence-associated genes in response to stress and hormone treatment. Plant Mol Biol 37:455–469PubMedCrossRefGoogle Scholar
  68. Winkenbach F, Falk H, Liedvogel B, Sitte P (1976) Chromoplasts of Tropaeolum majus L.: isolation and characterization of lipoprotein elements. Planta 128:23–28CrossRefGoogle Scholar
  69. Wuttke HG (1976) Chromoplasts in Rosa rugosa: Development and chemical characterization of tubular elements. Z Naturforsch 31c:456–460Google Scholar
  70. Xie LX, Hsieh EJ, Watanabe S, Allan CM, Chen JY, Tran UC, Clarke CF (2011) Expression of the human atypical kinase ADCK3 rescues coenzyme Q biosynthesis and phosphorylation of Coq polypeptides in yeast coq8 mutants. Biochim Biophys Acta 1811:348–360PubMedCrossRefGoogle Scholar
  71. Yang S, Zeng X, Li T, Liu M, Zhang S, Gao S, Wang Y, Peng C, Li L, Yang C (2012) AtACDO1, an ABC1-like kinase gene, is involved in chlorophyll degradation and the response to photooxidative stress in Arabidopsis. J Exp Bot 63:3959–3973PubMedCrossRefGoogle Scholar
  72. Youssef A, Laizet Y, Block MA, Marechal E, Alcaraz JP, Larson TR, Pontier D, Gaffe J, Kuntz M (2010) Plant lipid-associated fibrillin proteins condition jasmonate production under photosynthetic stress. Plant J 61:436–445PubMedCrossRefGoogle Scholar
  73. Ytterberg AJ, Peltier JB, van Wijk KJ (2006) Protein profiling of plastoglobules in chloroplasts and chromoplasts. A surprising site for differential accumulation of metabolic enzymes. Plant Physiol 140:984–997PubMedCrossRefGoogle Scholar
  74. Zbierzak AM, Kanwischer M, Wille C, Vidi PA, Giavalisco P, Lohmann A, Briesen I, Porfirova S, Brehelin C, Kessler F, Dormann P (2010) Intersection of the tocopherol and plastoquinol metabolic pathways at the plastoglobule. Biochem J 425:389–399CrossRefGoogle Scholar
  75. Zou J, Wei Y, Jako C, Kumar A, Selvaraj G, Taylor DC (1999) The Arabidopsis thaliana TAG1 mutant has a mutation in a diacylglycerol acyltransferase gene. Plant J 19:645–653PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Laboratoire de Physiologie VégétaleUniversité de NeuchâtelNeuchâtelSwitzerland

Personalised recommendations