The structure and biogenesis of plant oil bodies: the role of the ER membrane and the oleosin class of proteins

Napier, Johnathan A.; Ak, Stobart; Pr, Shewry

doi:10.1007/bf00040714

Cited by 150 publications

(110 citation statements)

References 71 publications

(101 reference statements)

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“…(5) Unlike mature seeds, the Physcomitrella gametophyte possesses oleosin-coated OBs in highly hydrated vegetative cells; this situation is similar to the lipid droplets in yeast and mammalian cells. Oleosins on seed OBs may protect the OBs from dehydration (Napier et al, 1996;Murphy, 2001;Hsieh and Huang, 2004). This idea could be applied to the oleosins on OBs in the vegetative nondehydrated Physcomitrella gametophyte because many moss tissues can undergo extreme and prolonged dehydration and still resuscitate upon water uptake.…”

Section: Discussionmentioning

confidence: 99%

“…These lipid droplets are present in seeds, pollens, fruits, and flowers of higher plants; the vegetative and reproductive organs of lower plants, algae, fungi, and nematodes; mammalian organs/tissues, such as mammalian glands and adipose tissues; and bacteria. Among all these lipid droplets, oil bodies (OBs) in seeds are the most prominent and have been extensively studied.Seeds of diverse plant species store oils (triacylglycerols [TAGs]) as food reserves for germination and postgermination growth (Napier et al, 1996;Frandsen et al, 2001;Murphy, 2001;Hsieh and Huang, 2004).The TAGs are present in small subcellular, spherical OBs of approximately 0.5 to 2 mm in diameter. Each OB has a matrix of TAGs surrounded by a layer of phospholipids (PLs) and the structural protein oleosins.…”

mentioning

confidence: 99%

“…Seeds of diverse plant species store oils (triacylglycerols [TAGs]) as food reserves for germination and postgermination growth (Napier et al, 1996;Frandsen et al, 2001;Murphy, 2001;Hsieh and Huang, 2004).…”

mentioning

confidence: 99%

“…Whereas the nascent oleosins are attached to the ER surface via the long hydrophobic hairpin stretch, TAGs are sequestered between the two PL layers of the ER membrane. These oleosins and TAGs migrate to and are eventually concentrated in confined ER regions, which are detached to form mature OBs (Napier et al, 1996;Murphy, 2001;Abell et al, 2004;Hsieh and Huang, 2004). What is uncertain is the location of the ER on which oleosins and TAGs are synthesized.…”

mentioning

confidence: 99%

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Oil Bodies and Oleosins in Physcomitrella Possess Characteristics Representative of Early Trends in Evolution

Huang

Chung²,

Lin³

et al. 2009

Plant Physiology

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Searches of sequenced genomes of diverse organisms revealed that the moss Physcomitrella patens is the most primitive organism possessing oleosin genes. Microscopy examination of Physcomitrella revealed that oil bodies (OBs) were abundant in the photosynthetic vegetative gametophyte and the reproductive spore. Chromatography illustrated the neutral lipids in OBs isolated from the gametophyte to be largely steryl esters and triacylglycerols, and SDS-PAGE showed the major proteins to be oleosins. Reverse transcription-PCR revealed the expression of all three oleosin genes to be tissue specific. This tissue specificity was greatly altered via alternative splicing, a control mechanism of oleosin gene expression unknown in higher plants. During the production of sex organs at the tips of gametophyte branches, the number of OBs in the top gametophyte tissue decreased concomitant with increases in the number of peroxisomes and level of transcripts encoding the glyoxylate cycle enzymes; thus, the OBs are food reserves for gluconeogenesis. In spores during germination, peroxisomes adjacent to OBs, along with transcripts encoding the glyoxylate cycle enzymes, appeared; thus, the spore OBs are food reserves for gluconeogenesis and equivalent to seed OBs. The one-cell-layer gametophyte could be observed easily with confocal microscopy for the subcellular OBs and other structures. Transient expression of various gene constructs transformed into gametophyte cells revealed that all OBs were linked to the endoplasmic reticulum (ER), that oleosins were synthesized in extended regions of the ER, and that two different oleosins were colocated in all OBs.Eukaryotes and prokaryotes contain neutral lipids in subcellular droplets as food reserves and/or for other purposes (Hsieh and Huang, 2004;Martin and Parton, 2006;Goodman, 2008;Rajakumari et al., 2008). These lipid droplets are present in seeds, pollens, fruits, and flowers of higher plants; the vegetative and reproductive organs of lower plants, algae, fungi, and nematodes; mammalian organs/tissues, such as mammalian glands and adipose tissues; and bacteria. Among all these lipid droplets, oil bodies (OBs) in seeds are the most prominent and have been extensively studied.Seeds of diverse plant species store oils (triacylglycerols [TAGs]) as food reserves for germination and postgermination growth (Napier et al., 1996;Frandsen et al., 2001;Murphy, 2001;Hsieh and Huang, 2004).The TAGs are present in small subcellular, spherical OBs of approximately 0.5 to 2 mm in diameter. Each OB has a matrix of TAGs surrounded by a layer of phospholipids (PLs) and the structural protein oleosins. The massive oleosins completely cover the surface of the OBs and prevent them from coalescence; so, a large surface area per unit TAG is available for lipase binding and catalysis during germination. Each oleosin molecule has a characteristic long central hydrophobic stretch, which forms a hairpin penetrating into the matrix TAGs for stable anchorage.Other than being present in the seeds of plants, oleos...

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Oil Bodies and Oleosins in Physcomitrella Possess Characteristics Representative of Early Trends in Evolution

Huang

Chung²,

Lin³

et al. 2009

Plant Physiology

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“…1B) and is predicted to reside completely within the phospholipid bilayer. Oleosins eventually accumulate on oil bodies within the cytosol of plant seed cells (15,16) and are anchored to oil bodies by their H domain (17). It is likely that membrane topology and the hydrophobicity of the H domain favors transition into a region of oil in the ER membrane from which oil body formation can occur (18 -20).…”

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Membrane Protein Topology of Oleosin Is Constrained by Its Long Hydrophobic Domain

Abell

High

Moloney

2002

Journal of Biological Chemistry

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Oleosin proteins from Arabidopsis assume a unique endoplasmic reticulum (ER) topology with a membraneintegrated hydrophobic (H) domain of 72 residues, flanked by two cytosolic hydrophilic domains. We have investigated the targeting and topological determinants present within the oleosin polypeptide sequence using ER-derived canine pancreatic microsomes. Our data indicate that oleosins are integrated into membranes by a cotranslational, translocon-mediated pathway. This is supported by the identification of two independent functional signal sequences in the H domain, and by demonstrating the involvement of the SRP receptor in membrane targeting. Oleosin topology was manipulated by the addition of an N-terminal cleavable signal sequence, resulting in translocation of the N terminus to the microsomal lumen. Surprisingly, the C terminus failed to translocate. Inhibition of C-terminal translocation was not dependent on either the sequence of hydrophobic segments in the H domain, the central proline knot motif or charges flanking the H domain. Therefore, the topological constraint results from the length and/or the hydrophobicity of the H domain, implying a general case that long hydrophobic spans are unable to translocate their C terminus to the ER lumen.Membrane proteins targeted to the ER 1 generally display a uniform and consistent topology, in which the orientation of membrane spans is determined by the interaction between nascent polypeptides and the translocon (1, 2). A set of general rules has been established that are useful for prediction of unknown topologies. These rules also further our understanding of the underlying mechanisms of membrane insertion. In the simplest case, individual membrane spans can be orientated by sequential insertion, resulting in adoption of the opposite orientation to the previous span (3). The presence of charged residues in flanking regions is a critical influence on the orientation of individual membrane spans; positively charged residues show a strong preference for retention in the cytosol, while negatively charged residues have a weak affinity for translocation to the ER lumen (4 -7). Variants of a yeast protein, Ste2p, a G protein-coupled pheromone receptor, strictly followed the "positive inside" rule for the first transmembrane span (8). The N terminus is translocated only if the charge difference is reversed by removal of all the N-terminal positive charges or addition of C-terminal negative charges. ER membrane does not support a transmembrane potential, suggesting that this preference may be due to charged residues interacting with phospholipids (9). In the case of signal-anchors, translocation of the N terminus can be blocked by the adoption of a fully folded conformation (10). Prediction of topology can also be aided by analyzing the membrane span itself. Transmembrane spans up to 25 leucine residues increasingly favored a topology with the N terminus in the lumen as the polyleucine chain was lengthened (11). The interaction between multiple topology determinants is ...

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Characterization of a 13-lipoxygenase from virgin olive oil and oil bodies of olive endosperms

Georgalaki¹,

Bachmann

Sotiroudis

et al. 1998

Fett/Lipid

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Olive oil is one of the oldest known vegetable oils, and it is almost unique in that it can be consumed without any refining treatment. One of its most important quality problems is oxidative rancidity due to the oxygenation of polyenoic fatty acids and formation of compounds that derive from these fatty acid hydroperoxides. Beside autoxidation, lipoxygenases (LOXs) were suggested to be involved in this process. Here we show, that approximately 1.6% of all linoleic acid (LA) molecules within olive oil samples had been converted into LOX‐derived (13S,9Z,11E)‐13‐hydroperoxy‐9,11‐octadecadienoic acid (13‐HPODE) as determined by 1H NMR‐ and HPLC analysis. LOX activity tests indicated the occurrence of an active 13‐LOX exhibiting a pH optimum between pH 5.5 and 6.0. Furthermore, this enzyme preferentially metabolized free fatty acids. In order to elucidate the origin of this LOX, we analyzed olive endosperms for LOX forms. Chromatography of total protein extracts of the tissue showed LOX activity almost exclusively associated with a high molecular mass fraction. Light microscopic inspection, as well as the calculated phosphate, neutral lipid, and protein content of this fraction, suggested that this fraction may contain oil bodies and that LOX activity was associated with their membrane. This LOX activity had a pH optimum of 6.0. Activity assays at various temperatures indicated a significant catalytic efficiency of the enzyme up to 55°C. HPLC analysis of LA oxygenation products within the lipid fraction and of activity tests of isolated oil bodies showed that the LOX present in mature olive endosperm oil bodies was, as the enzyme from olive oil, a linoleate 13‐LOX preferentially active on free LA. We suggest, that this oil body LOX from olive endosperm, is the one detected originally in olive oil and may survive at least in part olive oil production.

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The structure and biogenesis of plant oil bodies: the role of the ER membrane and the oleosin class of proteins

Cited by 150 publications

References 71 publications

Oil Bodies and Oleosins in Physcomitrella Possess Characteristics Representative of Early Trends in Evolution

Oil Bodies and Oleosins in Physcomitrella Possess Characteristics Representative of Early Trends in Evolution

Membrane Protein Topology of Oleosin Is Constrained by Its Long Hydrophobic Domain

Characterization of a 13-lipoxygenase from virgin olive oil and oil bodies of olive endosperms

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