Tapetal oleosins play an essential role in tapetosome formation and protein relocation to the pollen coat

New Phytologist

Volumn 209, Issue 2, 2016, Pages 691-704

  Lévesque Lemay, Madeleine ^a   Chabot, Denise ^a   Hubbard, Keith ^a   Chan, John K ^a   Miller, Shea ^a   Robert, Laurian S ^a  

^a AGRICULTURE AND AGRI FOOD CANADA   (Canada)

Author keywords

Arabidopsis; Brassica; GFP; GUS; Oleosin; Tapetum

Indexed keywords

ALKANE; APOPTOSIS; CANOLA; CELL ORGANELLE; DICOTYLEDON; FLUORESCENCE; LIPID; PIGMENT; POLLEN; PROTEIN; TRANSLOCATION;

ARABIDOPSIS; ARABIDOPSIS THALIANA; BRASSICA; BRASSICACEAE;

ARABIDOPSIS PROTEIN; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; LIPID; OLEOSIN PROTEIN, ARABIDOPSIS; TRYPHINE;

ARABIDOPSIS; CELL ORGANELLE; CHEMISTRY; CYTOLOGY; GENETICS; METABOLISM; PLANT CELL; POLLEN; PROTEIN TRANSPORT; RAPESEED; TRANSGENIC PLANT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BRASSICA NAPUS; GREEN FLUORESCENT PROTEINS; LIPIDS; ORGANELLES; PLANT CELLS; PLANTS, GENETICALLY MODIFIED; POLLEN; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS;

EID: 84955204550     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.13611     Document Type: Article

References (49)

1. Abell BM, Hahn M, Holbrook LA, Moloney MM. 2004. Membrane topology and sequence requirements for oil body targeting of oleosin. Plant Journal 37: 461-470.
2. Abell BM, High S, Moloney MM. 2002. Membrane protein topology of oleosin is constrained by its long hydrophobic domain. Journal of Biological Chemistry 277: 8602-8610.
3. 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.
4. Alves Ferreira M, De Almeida Engler J, Costa Miguens F, Van Montagu M, Engler G, De Oliveira DE. 1997. Oleosin gene expression in Arabidopsis thaliana tapetum coincides with accumulation of lipids in plastids and cytoplasmic bodies. Plant Physiology and Biochemistry 35: 729-739.
5. Beaudoin F, Napier JA. 2000. The targeting and accumulation of ectopically expressed oleosin in non-seed tissues of Arabidopsis thaliana. Planta 210: 439-445.
6. Benghezal M, Wasteneys GO, Jones DA. 2000. The C-terminal dilysine motif confers endoplasmic reticulum localization to type I membrane proteins in plants. Plant Cell 12: 1179-1201.
7. Blackmore S, Wortley AH, Skvarla JJ, Rowley JR. 2007. Pollen wall development in flowering plants. New Phytologist 174: 483-498.
8. Clough SJ, Bent AF. 1998. Floral dip: a simplified method for Agrobacterium mediated transformation of Arabidopsis thaliana. Plant Journal 16: 735-743.
9. DaSilva LLP, Taylor JP, Hadlington JL, Hanton SL, Snowden CJ, Fox SJ, Foresti O, Brandizzi F, Denecke J. 2005. Receptor salvage from the prevacuolar compartment is essential for efficient vacuolar protein targeting. Plant Cell 17: 132-148.
10. De Oliveira 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 Journal 3: 495-507.
11. Foster E, Schneiderman D, Cloutier M, Gleddie S, Robert LS. 2002. Modifying the pollen coat protein composition in Brassica. Plant Journal 31: 477-486.
12. Gabarayeva N, Hemsley AR. 2006. Merging concepts: the role of self-assembly in the development of pollen wall structure. Review of Paleobotany and Palynology 138: 121-139.
13. Hernández-Pinzón I, Ross JHE, Barnes KA, Damant AP, Murphy DJ. 1999. Composition and role of tapetal lipid bodies in the biogenesis of the pollen coat of Brassica napus. Planta 208: 588-598.
14. Hong HP, Gerster JL, Datla RSS, Albani D, Scoles G, Keller W, Robert LS. 1997. The promoter of a Brassica napus polygalacturonase gene directs pollen expression of β-glucuronidase in transgenic Brassica plants. Plant Cell Reports 16: 373-378.
15. Hsieh K, Huang AHC. 2004. Endoplasmic reticulum, oleosins, and oils in seeds and tapetum cells. Plant Physiology 136: 3427-3434.
16. 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 Journal 43: 889-899.
17. Hsieh K, Huang AHC. 2007. Tapetosomes in Brassica tapetum accumulate endoplasmic reticulum-derived flavonoids and alkanes for delivery to the pollen surface. Plant Cell 19: 582-596.
18. Huang CY, Chen P, Huang M, Tsou C, Jane W, Huang AHC. 2013a. Tandem oleosin genes in a cluster acquired in Brassicaceae created tapetosomes and conferred additive benefit of pollen vigor. Proceedings of the National Academy of Sciences, USA 110: 14480-14485.
19. Huang M, Chen TL, Huang AHC. 2013b. Abundant type III lipid transfer proteins in Arabidopsis tapetum are secreted to the locule and become a constituent of the pollen coat exine. Plant Physiology 163: 1218-1229.
20. Huang AHC. 1992. Oil bodies and oleosins in seeds. Annual Review of Plant Physiology and Plant Molecular Biology 43: 177-200.
21. Huang AHC. 2006. Oleosins and endoplasmic reticulum in seeds and anthers. In: Robinson DG, ed. The plant endoplasmic reticulum. Heidelberg, Germany: Springer-Verlag, 187-204.
22. Johnson-Brousseau SA, McCormick S. 2004. A compendium of methods useful for characterizing Arabidopsis pollen mutants and gametophytically-expressed genes. Plant Journal 39: 761-775.
23. Kim HU, Hsieh K, Ratnayake C, Huang AHC. 2002. A novel group of oleosins is present inside the pollen of Arabidopsis. Journal of Biological Chemistry 277: 22677-22684.
24. Li M, Murphy DJ, Lee KK, Wilson R, Smith LJ, Clark DC, Sung J. 2002. Purification and structural characterization of the central hydrophobic domain of oleosin. Journal of Biological Chemistry 277: 37888-37895.
25. Mayfield JA, Fiebig A, Johnstone SE, Preuss D. 2001. Gene families from the Arabidopsis thaliana pollen coat proteome. Science 292: 2482-2485.
26. Mayfield JA, Preuss D. 2000. Rapid initiation of Arabidopsis pollination requires the oleosin-domain protein GRP17. Nature Cell Biology 2: 128-130.
27. Miquel M, Trigui G, d'Andréa S, Kelemen Z, Baud S, Berger A, Deruyffelaere C, Trubuil A, Lepiniec L, Dubreucq B. 2014. Specialization of oleosins in oil body dynamics during seed development in Arabidopsis seeds. Plant Physiology 164: 1866-1878.
28. Murphy DJ. 2001. The biogenesis and functions of lipid bodies in animals, plants and microorganisms. Progress in Lipid Research 40: 325-438.
29. Murphy DJ. 2006. The extracellular pollen coat in members of the Brassicaceae: composition, biosynthesis, and functions in pollination. Protoplasma 228: 31-39.
30. Murphy DJ, Ross JHE. 1998. Biosynthesis, targeting and processing of oleosin like proteins, which are major pollen coat components in Brassica napus. Plant Journal 13: 1-16.
31. Parish RW, Li SF. 2010. Death of a tapetum: a programme of developmental altruism. Plant Science 178: 73-89.
32. Platt KA, Huang AHC, Thomson WW. 1998. Ultrastructural study of lipid accumulation in tapetal cells of Brassica napus L. cv. Westar during microsporogenesis. International Journal of Plant Science 159: 724-737.
33. Pons L, Olszewski A, Guéant J. 1998. Characterization of the oligomeric behaviour of a 16.5 kD peanut oleosin by chromatography and electrophoresis of the iodinated form. Journal of Chromatography B: Biomedical Sciences and Applications 706: 131-140.
34. Quattrocchio FM, Spelt C, Koes R. 2013. Transgenes and protein localization: myths and legends. Trends in Plant Science 18: 473-476.
35. Quilichini TD, Douglas CJ, Samuels AL. 2014. New views of tapetum ultrastructure and pollen exine development in Arabidopsis thaliana. Annals of Botany 114: 1189-1201.
36. Robert 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 Journal 6: 927-933.
37. Ross JHE, Milanesi C, Murphy DJ, Cresti M. 2000. Rapid-freeze fixation and substitution improves tissue preservation of microspores and tapetum in Brassica napus. Sexual Plant Reproduction 12: 237-240.
38. 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 Journal 9: 625-637.
39. Ruiter RK, Van Eldik GJ, Van Herpen RMA, Schrauwen JAM, Wullems GJ. 1997. Characterization of oleosins in the pollen coat of Brassica oleracea. Plant Cell 9: 1621-1631.
40. Russin WA, Trivett CL. 2001. Vacuum-microwave combination for processing plant tissues for electron microscopy. In: Giberson RT, Demaree RS Jr, eds. Microwave techniques and protocols. Totowa, NJ, USA: Humana Press, 25-35.
41. Sarmiento C, Ross JHE, Herman E, Murphy DJ. 1997. Expression and subcellular targeting of a soybean oleosin in transgenic rapeseed. Implications for the mechanism of oil-body formation in seeds. Plant Journal 11: 783-796.
42. Suzuki T, Tsunekawa S, Koizuka C, Yamamoto K, Imamura J, Nakamura K, Ishiguro S. 2013. Development and disintegration of tapetum-specific lipid- accumulating organelles, elaioplasts and tapetosomes, in Arabidopsis thaliana and Brassica napus. Plant Science 207: 25-36.
43. Ting JTL, Wu SSH, Ratnayake C, Huang AHC. 1998. Constituents of the tapetosomes and elaioplasts in Brassica campestris tapetum and their degradation and retention during microsporogenesis. Plant Journal 16: 541-551.
44. Updegraff EP, Zhao F, Preuss D. 2009. The extracellular lipase EXL4 is required for efficient hydration of Arabidopsis pollen. Sexual Plant Reproduction 22: 197-204.
45. Van Rooijen GJH, Moloney MM. 1995. Structural requirements of oleosin domains for subcellular targeting to the oil body. Plant Physiology 109: 1353-1361.
46. Vargo KB, Sood N, Moeller TD, Heiney PA, Hammer DA. 2014. Spherical micelles assembled from variants of recombinant oleosin. Langmuir 30: 11292-11300.
47. Wang T, Balsamo RA, Ratnayake C, Platt KA, Ting JTL, Huang AHC. 1997. Identification, subcellular localization, and developmental studies of oleosins in the anther of Brassica napus. Plant Journal 11: 475-487.
48. 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.
49. Wu SSH, Platt KA, Ratnayake C, Wang T, Ting JTL, Huang AHC. 1997. Isolation and characterization of neutral-lipid-containing organelles and globuli-filled plastids from Brassica napus tapetum. Proceedings of the National Academy of Sciences, USA 94: 12711-12716.