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Oleosins and Endoplasmic Reticulum in Seeds and Anthers

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The Plant Endoplasmic Reticulum

Part of the book series: Plant Cell Monographs ((CELLMONO,volume 4))

Abstract

Three types of related subcellular oil-rich particles are present in plants: storage oil bodies inseeds for gluconeogenesis during germination, storage oil bodies in pollen providing acyl moieties for membranesynthesis in the pollen tube, and tapetosomes in the anther tapetum for delivering lipids and proteins tothe maturing pollen surface. Each of these oil-rich particles has a basic structure of an oil body,which consists of a triacylglycerol matrix enclosed by a layer of phospholipids and the structuralprotein oleosins. All components of an oil body are synthesized and assembled in endoplasmic reticulum(ER), from which a budding oil body is released. An oleosin molecule has a highly conserved centraldomain of 72 uninterrupted hydrophobic residues flanked by variable amphipathic N-and C-terminal segments. Its unique central domain is presumed to haveevolved from a transmembrane segment of an ER protein. An oleosin molecule does not have an N-terminal ER-targeting signal and is targeted to the signal recognition particleand then ER via its central hydrophobic domain. Targeting studies of oleosin molecules that have been modifiedby adding a N-terminal ER-targeting signal, shortening the centralhydrophobic stretch and eliminating the N- or C-terminalamphipathic stretch, have provided a model delineating the mechanism of oleosin targeting to ER andoil bodies. A tapetosome possesses numerous oleosin-coated oil bodies associated ionically with abundantmembranous vesicles, both of which are assembled in and then detached from ER.

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References

  1. Abell BM, Holbrook LA, Abenes M, Murphy DJ, Hills MJ, Moloney MM (1997) Role of the proline knot motif in oleosin endoplasmic reticulum topology and oil body targeting. Plant Cell 9:1481–1493

    PubMed  CAS  Google Scholar 

  2. Abell BM, High S, Moloney MM (2002) Membrane protein topology of oleosin is constrained by its long hydrophobic domain. J Biol Chem 277:8602–8610

    Article  PubMed  CAS  Google Scholar 

  3. Abell BM, Hahn M, Holbrook LA, Moloney MM (2004) Membrane topology and sequence requirements for oil body targeting of oleosin. Plant J 37:461–470

    Article  PubMed  CAS  Google Scholar 

  4. Alexander LG, Sessions RB, Clarke AR, Tatham AS, Shewry PR, Napier JA (2002) Characterization and modelling of the hydrophobic domain of a sunflower oleosin. Planta 214:546–551

    Article  PubMed  CAS  Google Scholar 

  5. Beaudoin F, Napier JA (2002) Targeting and membrane-insertion of a sunflower oleosin in vitro and in Saccharomyces cervisiae: the central hydrophobic domain contains more than one signal sequence, and directs oleosin insertion into the endoplasmic reticulum membrane using a signal anchor sequence mechanism. Planta 215:293–303

    Article  PubMed  CAS  Google Scholar 

  6. Beaudoin F, Wilkinson BM, Stirling C, Napier JA (2000) In vivo targeting of a sunflower oil body protein in yeast secretory (sec) mutants. Plant J 23:159–170

    Article  PubMed  CAS  Google Scholar 

  7. Cae YZ, Huang AHC (1986) Diacylglycerol acyltransferase in maturing oil seeds of maize and other species. Plant Physiol 82:813–820

    Article  Google Scholar 

  8. Chen JCF, Tzen JTC (2001) An in vitro system to examine the effective phospholipids and structural domain for protein targeting to seed oil bodies. Plant Cell Physiol 42:1245–1252

    Article  PubMed  Google Scholar 

  9. deOliverira DE, Franco LO, Simoens C, Seurinck J, Coppieters J, Botterman J, van Montagu M (1993) Inflorescence-specific genes from Arabidopsis thaliana encoding glycine-rich proteins. Plant J 3:495–507

    Article  Google Scholar 

  10. Fiebig A, Kimport R, Preuss D (2004) Comparisons of pollen coat genes across Brassicaceae species reveal rapid evolution by repeat expansion and diversification. Proc Natl Acad Sci (US) 101:3286–3291

    Article  CAS  Google Scholar 

  11. Frandsen GI, Mundy J, Tzen JT (2001) Oil bodies and their associated proteins, oleosin and caleosin. Physiol Plant 112:301–307

    Article  PubMed  CAS  Google Scholar 

  12. Galili G, Sengupta-Gopalan C, Ceriotti A (1998) The endoplasmic reticulum of plant cells and its role in protein maturation and biogenesis of oil bodies. Plant Mol Biol 38:1–29

    Article  PubMed  CAS  Google Scholar 

  13. Guilloteau M, Laloi M, Blais D, Crouzillat D, McCarthy J (2003) Oil bodies in Theobroma cacao seeds: cloning and characterization of cDNA encoding the 15.8 and 16.9 kDaoleosins. Plant Science 164:597–606

    Article  CAS  Google Scholar 

  14. Herman EM (1987) Immunogold-localization and synthesis of an oil-body membrane protein in developing soybean seeds. Planta 172:336–345

    Article  CAS  Google Scholar 

  15. Hsieh K, Huang AHC (2005) Lipid-rich tapetosomes in Brassica tapetum are composed of oleosin-coated oil droplets and vesicles, both assembled in and then detached from the endoplasmic reticulum. Plant J 43:889–899

    Article  PubMed  CAS  Google Scholar 

  16. Hills MJ, Watson MD, Murphy DJ (1993) Targeting of oleosins to the oil bodies of oilseed rape (Brassica napus L.). Planta 189:24–29

    Article  PubMed  CAS  Google Scholar 

  17. Huang AHC (1992) Oil bodies and oleosins in seeds. Annu Rev Plant Physiol Mol Biol 43:177–200

    Article  CAS  Google Scholar 

  18. Huang AHC (1996) Evolution of oleosins. In: William JP et al. (ed) Physiology, biochemistry and molecular biology of plant lipids. Kluwer, Dordrecht, pp 292–294

    Google Scholar 

  19. Kim HU, Hsieh K, Ratnayake C, Huang AHC (2002) Expression of Arabidopsis oleosin genes and characterization of their encoded oleosins. J Biol Chem 277:22677–22684

    Article  PubMed  CAS  Google Scholar 

  20. Lacey DJ, Beaudoin F, Dempsey CE, Shewry PR, Napier JA (1999) The accumulation of triacylglycerols within the endoplasmic reticulum of developing seeds of Helianthus annuus. Plant J 17:397–405

    Article  CAS  Google Scholar 

  21. Lee K, Ratnayake C, Huang AHC (1995) Genetic dissection of the co-expression of genes encoding the two isoforms of oleosins in the oil bodies of maize kernel. Plant J 7:603–611

    Article  PubMed  CAS  Google Scholar 

  22. Li M, Murphy DJ, Lee KHK, Wilson R, Smith LJ, Clark DC, Sung JY (2002) Purification and structural characterization of the central hydrophobic domain of oleosin. J Biol Chem 277:37888–37895

    Article  PubMed  CAS  Google Scholar 

  23. Loer DS, Herman EM (1993) Cotranslational integration of soybean (Glycine max) oil body membrane protein oleosin into microsomal membranes. Plant Physiol 101:993–998

    PubMed  CAS  Google Scholar 

  24. Mayfield JA, Preuss D (2000) Rapid initiation of Arabidopsis pollination requires the oleosin-domain protein GRP17. Nature Cell Biol 2:128–130

    Article  PubMed  CAS  Google Scholar 

  25. Murphy DJ (2001) The biogenesis and functions of lipid bodies in animals, plants and microorganisms. Plant J 13:1–16

    CAS  Google Scholar 

  26. Napier JA, Stobart AK, Shewry PR (1996) The structure and biogenesis of plant oil bodies: the role of the ER membrane and the oleosin class of proteins. Plant Mol Biol 31:945–956

    Article  PubMed  CAS  Google Scholar 

  27. Owen HA, Makeroff CA (1995) Ultrastructure of microsporogenesis and microgametogenesis in Arabidopsis thaliana (L.) Heynh. ecotype Wassilewskija (Brassicaceae). Protoplasma 185:7–21

    Article  Google Scholar 

  28. Platt KA, Huang AHC, Thomson WW (1998) Ultrastructural study of lipid accumulation in tapetal cells of Brassica napus L. cv. Westar during microsporogenesis. Int J Plant Sci 159:724–737

    Article  CAS  Google Scholar 

  29. Polowick PL, Sawhney VK (1990) Microsporogenesis in a normal line and in the ogu cytoplasmic male sterile line of Brassica napus. I. The influence of high temperature. Sex Plant Reprod 3:263–276

    Article  Google Scholar 

  30. Roberts LS, Gerster J, Allard S, Cass L, Simmonds J (1994) Molecular characterization of two Brassica napus genes related to oleosins which are highly expressed in the tapetum. Plant J 6:927–933

    Article  Google Scholar 

  31. Ross JHE, Murphy DJ (1996) Characterization of anther-expressed genes encoding a major class of extracellular oleosin-like proteins in the pollen coat of Brassicaceae. Plant J 9:625–637

    Article  PubMed  CAS  Google Scholar 

  32. Ruiter RK, Vaneldik GJ, Vanherpen RMA, Schrauwen JAM, Wullems GJ (1997) Characterization of oleosins in the pollen coat of Brassica oleracea. Plant Cell 9:1621–1631

    PubMed  CAS  Google Scholar 

  33. Schein M, Yang ZH, Mitchell-Olds T, Schmid KJ (2004) Rapid evolution of a pollen-specific oleosin-like gene family from Arabidopsis thaliana and closely related species. Mol Biol Evolution 21:659–669

    Article  CAS  Google Scholar 

  34. Thoyts PJ, Millichip MI, Stobart AK, Griffiths WT, Shewry PR, Napier JA (1995) Expression and in vitro targeting of a sunflower oleosin. Plant Mol Biol 29:403–410

    Article  PubMed  CAS  Google Scholar 

  35. Ting JTL, Balsamo RA, Ratnayake C, Huang AHC (1997) Oleosin of plant seed oil bodies is correctly targeted to the lipid bodies in transformed yeast. J Biol Chem 272:3699–3706

    Article  PubMed  CAS  Google Scholar 

  36. Ting JTL, Lee K, Ratnayake C, Platt KA, Balsamo RA, Huang AHC (1996) Oleosin genes in maize kernels having diverse oil contents are constitutively expressed independent of oil contents: size and shape of intracellular oil bodies are determined by the oleosin/oils ratio. Planta 199:158–165

    Article  PubMed  CAS  Google Scholar 

  37. Ting JTL, Wu SSH, Ratnayake C, Huang AHC (1998) Constituents of the tapetosomes and elaioplasts in Brassica campestris and their degradation and retention during microsporogenesis. Plant J 16:541–551

    Article  PubMed  CAS  Google Scholar 

  38. Wanner G, Formanek H, Theimer RR (1981) The ontogeny of lipid bodies in plant cells. Planta 151:109–123

    Article  Google Scholar 

  39. Wu SSH, Moreau RA, Whitaker BD, Huang AHC (1999) Steryl esters in the elaioplasts of the tapetum in developing Brassica anthers and their recovery on the pollen surface. Lipids 34:517–523

    Article  PubMed  CAS  Google Scholar 

  40. Wu SSH, Platt KA, Ratnayake C, Wang TW, Ting JTL, Huang AHC (1997) Isolation and characterization of novel neutral-lipid-containing organelles and globuli-filled plastids from Brassica napus tapetum. Proc Natl Acad Sci (US) 94:12711–12716

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The research was supported by the National Science Foundation (MCB-0131358) and the US Department of Agriculture (National Research Initiative Competitive Grant No. 2004-02429).

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Correspondence to Anthony H. C. Huang .

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David G. Robinson

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© 2006 Springer-Verlag Berlin Heidelberg

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Huang, A.H.C. (2006). Oleosins and Endoplasmic Reticulum in Seeds and Anthers. In: Robinson, D.G. (eds) The Plant Endoplasmic Reticulum. Plant Cell Monographs, vol 4. Springer, Berlin, Heidelberg. https://doi.org/10.1007/7089_057

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