The Dynamics of Oil Bodies in A. thaliana Seeds: A Mathematical Model of Biogenesis and Coalescence
The subcellular organelles called oil bodies (OBs) are lipid-filled quasi-spherical droplets produced from the endoplasmic reticulum (ER) and then released into the cytoplasm during seed development. It is believed that an OB grows by coalescence with other OBs and that its stability depends on the composition of oleosins, major proteins inserted in the hemi membrane that covers OBs. In this study, we measured the OB-volume distribution from different genotypes of A. thaliana after 7, 8, 9, 10 and 11 days of seed development. In order to test the hypothesis of OBs dynamics, we developed a simple mathematical model using non-linear differential equations inspired from the theory of coagulation. The model describes the evolution of OB-volume distribution during the first steps of seed development by taking into consideration the production of OBs, the increase of triacylglycerol volume to be stored, and the growth by coalescence of OBs. Fitted parameters values show an increase in the OB production and coalescence rates in A. thaliana oleosin mutants compared to wild type.
[1] A. H. Huang, "Oleosins and oil bodies in seeds and other organs.,"
Plant Physiology, vol. 110, pp. 1055-1061, Apr. 1996. PMID: 8934621
PMCID: 160879.
[2] J. Tzen, Y. Cao, P. Laurent, C. Ratnayake, and A. Huang, "Lipids,
proteins, and structure of seed oil bodies from diverse species," Plant
Physiology, vol. 101, pp. 267 -276, Jan. 1993.
[3] J. C. Chen, C. C. Tsai, and J. T. Tzen, "Cloning and secondary structure
analysis of caleosin, a unique Calcium-Binding protein in oil bodies of
plant seeds," Plant and Cell Physiology, vol. 40, pp. 1079 -1086, Jan.
1999.
[4] D. J. Murphy, "Storage lipid bodies in plants and other organisms,"
Progress in Lipid Research, vol. 29, no. 4, pp. 299-324, 1990. PMID:
2135719.
[5] J. Tzen and A. Huang, "Surface structure and properties of plant seed
oil bodies," The Journal of Cell Biology, vol. 117, pp. 327 -335, Apr.
1992.
[6] D. J. Murphy and J. Vance, "Mechanisms of lipid-body formation,"
Trends in Biochemical Sciences, vol. 24, pp. 109-115, Mar. 1999.
[7] G.Wanner and R. R. Theimer, "Membranous appendices of spherosomes
(oleosomes)," Planta, vol. 140, pp. 163-169, 1978.
[8] D. J. Murphy and I. Cummins, "Seed oil-bodies: Isolation, composition
and role of oil-body apolipoproteins," Phytochemistry, vol. 28, no. 8,
pp. 2063-2069, 1989.
[9] I. Cummins, M. J. Hills, J. H. E. Ross, D. H. Hobbs, M. D. Watson,
and D. J. Murphy, "Differential, temporal and spatial expression of genes
involved in storage oil and oleosin accumulation in developing rapeseed
embryos: implications for the role of oleosins and the mechanisms of
oil-body formation," Plant Molecular Biology, vol. 23, pp. 1015-1027,
Dec. 1993.
[10] F. Beaudoin and J. A. Napier, "The targeting and accumulation of ectopically
expressed oleosin in non-seed tissues of arabidopsis thaliana,"
Planta, vol. 210, pp. 439-445, Feb. 2000.
[11] A. Bana, A. Dahlqvist, H. Debski, P. O. Gummeson, and S. Stymne,
"Accumulation of storage products in oat during kernel development,"
Biochemical Society Transactions, vol. 28, pp. 705-707, Dec. 2000.
PMID: 11171178.
[12] C. Sarmiento, J. H. E. Ross, E. Herman, and D. J. Murphy, "Expression
and subcellular targeting of a soybean oleosin in transgenic rapeseed.
implications for the mechanism of oil body formation in seeds," The
Plant Journal, vol. 11, pp. 783-796, Apr. 1997.
[13] D. J. Murphy, "Production of novel oils in plants," Current Opinion in
Biotechnology, vol. 10, pp. 175-180, Apr. 1999. PMID: 10209131.
[14] D. J. Lacey, F. Beaudoin, C. E. Dempsey, P. R. Shewry, and J. A. Napier,
"The accumulation of triacylglycerols within the endoplasmic reticulum
of developing seeds of Helianthus annuus," The Plant Journal, vol. 17,
pp. 397-405, Feb. 1999.
[15] G. van Rooijen and M. M. Moloney, "Structural requirements of oleosin
domains for subcellular targeting to the oil body," Plant Physiology,
vol. 109, pp. 1353 -1361, Dec. 1995.
[16] F. Beisson, Etude des ol'eosomes de plantes et de leur lipolyse : M'ethodes
de dosage de l-activit'e des lipases. PhD thesis, 1999.
[17] P. Jolivet, E. Roux, S. d-Andrea, M. Davanture, L. Negroni, M. Zivy, and
T. Chardot, "Protein composition of oil bodies in arabidopsis thaliana
ecotype WS," Plant Physiology and Biochemistry, vol. 42, pp. 501-509,
June 2004.
[18] J. Zimmerberg and M. M. Kozlov, "How proteins produce cellular
membrane curvature," Nat Rev Mol Cell Biol, vol. 7, pp. 9-19, Jan.
2006.
[19] L. J. Pike, "The challenge of lipid rafts," Journal of Lipid Research,
vol. 50, pp. S323-S328, Apr. 2009. PMID: 18955730 PMCID: 2674732.
[20] S. Beucher and C. Lantuejoul, "Use of watersheds in contour detection,"
in International Workshop on Image Processing: Real-time Edge and
Motion Detection/Estimation, Rennes, France., 1979.
[21] P. G. J. Dongen and M. H. Ernst, "On the occurrence of a gelation transition
in Smoluchowski-s coagulation equation," Journal of Statistical
Physics, vol. 44, pp. 785-792, Sept. 1986.
[22] R. C. Ball, C. Connaughton, T. H. M. Stein, and O. Zaboronski, "Instantaneous
gelation in Smoluchowski-s coagulation equation revisited,"
Physical Review. E, Statistical, Nonlinear, and Soft Matter Physics,
vol. 84 , July 2011. PMID: 21867117.
[23] H. Haario, M. Laine, A. Mira, and E. Saksman, "DRAM: efficient
adaptive MCMC," Statistics and Computing, vol. 16, pp. 339-354, Dec.
2006.
[1] A. H. Huang, "Oleosins and oil bodies in seeds and other organs.,"
Plant Physiology, vol. 110, pp. 1055-1061, Apr. 1996. PMID: 8934621
PMCID: 160879.
[2] J. Tzen, Y. Cao, P. Laurent, C. Ratnayake, and A. Huang, "Lipids,
proteins, and structure of seed oil bodies from diverse species," Plant
Physiology, vol. 101, pp. 267 -276, Jan. 1993.
[3] J. C. Chen, C. C. Tsai, and J. T. Tzen, "Cloning and secondary structure
analysis of caleosin, a unique Calcium-Binding protein in oil bodies of
plant seeds," Plant and Cell Physiology, vol. 40, pp. 1079 -1086, Jan.
1999.
[4] D. J. Murphy, "Storage lipid bodies in plants and other organisms,"
Progress in Lipid Research, vol. 29, no. 4, pp. 299-324, 1990. PMID:
2135719.
[5] J. Tzen and A. Huang, "Surface structure and properties of plant seed
oil bodies," The Journal of Cell Biology, vol. 117, pp. 327 -335, Apr.
1992.
[6] D. J. Murphy and J. Vance, "Mechanisms of lipid-body formation,"
Trends in Biochemical Sciences, vol. 24, pp. 109-115, Mar. 1999.
[7] G.Wanner and R. R. Theimer, "Membranous appendices of spherosomes
(oleosomes)," Planta, vol. 140, pp. 163-169, 1978.
[8] D. J. Murphy and I. Cummins, "Seed oil-bodies: Isolation, composition
and role of oil-body apolipoproteins," Phytochemistry, vol. 28, no. 8,
pp. 2063-2069, 1989.
[9] I. Cummins, M. J. Hills, J. H. E. Ross, D. H. Hobbs, M. D. Watson,
and D. J. Murphy, "Differential, temporal and spatial expression of genes
involved in storage oil and oleosin accumulation in developing rapeseed
embryos: implications for the role of oleosins and the mechanisms of
oil-body formation," Plant Molecular Biology, vol. 23, pp. 1015-1027,
Dec. 1993.
[10] F. Beaudoin and J. A. Napier, "The targeting and accumulation of ectopically
expressed oleosin in non-seed tissues of arabidopsis thaliana,"
Planta, vol. 210, pp. 439-445, Feb. 2000.
[11] A. Bana, A. Dahlqvist, H. Debski, P. O. Gummeson, and S. Stymne,
"Accumulation of storage products in oat during kernel development,"
Biochemical Society Transactions, vol. 28, pp. 705-707, Dec. 2000.
PMID: 11171178.
[12] C. Sarmiento, J. H. E. Ross, E. Herman, and D. J. Murphy, "Expression
and subcellular targeting of a soybean oleosin in transgenic rapeseed.
implications for the mechanism of oil body formation in seeds," The
Plant Journal, vol. 11, pp. 783-796, Apr. 1997.
[13] D. J. Murphy, "Production of novel oils in plants," Current Opinion in
Biotechnology, vol. 10, pp. 175-180, Apr. 1999. PMID: 10209131.
[14] D. J. Lacey, F. Beaudoin, C. E. Dempsey, P. R. Shewry, and J. A. Napier,
"The accumulation of triacylglycerols within the endoplasmic reticulum
of developing seeds of Helianthus annuus," The Plant Journal, vol. 17,
pp. 397-405, Feb. 1999.
[15] G. van Rooijen and M. M. Moloney, "Structural requirements of oleosin
domains for subcellular targeting to the oil body," Plant Physiology,
vol. 109, pp. 1353 -1361, Dec. 1995.
[16] F. Beisson, Etude des ol'eosomes de plantes et de leur lipolyse : M'ethodes
de dosage de l-activit'e des lipases. PhD thesis, 1999.
[17] P. Jolivet, E. Roux, S. d-Andrea, M. Davanture, L. Negroni, M. Zivy, and
T. Chardot, "Protein composition of oil bodies in arabidopsis thaliana
ecotype WS," Plant Physiology and Biochemistry, vol. 42, pp. 501-509,
June 2004.
[18] J. Zimmerberg and M. M. Kozlov, "How proteins produce cellular
membrane curvature," Nat Rev Mol Cell Biol, vol. 7, pp. 9-19, Jan.
2006.
[19] L. J. Pike, "The challenge of lipid rafts," Journal of Lipid Research,
vol. 50, pp. S323-S328, Apr. 2009. PMID: 18955730 PMCID: 2674732.
[20] S. Beucher and C. Lantuejoul, "Use of watersheds in contour detection,"
in International Workshop on Image Processing: Real-time Edge and
Motion Detection/Estimation, Rennes, France., 1979.
[21] P. G. J. Dongen and M. H. Ernst, "On the occurrence of a gelation transition
in Smoluchowski-s coagulation equation," Journal of Statistical
Physics, vol. 44, pp. 785-792, Sept. 1986.
[22] R. C. Ball, C. Connaughton, T. H. M. Stein, and O. Zaboronski, "Instantaneous
gelation in Smoluchowski-s coagulation equation revisited,"
Physical Review. E, Statistical, Nonlinear, and Soft Matter Physics,
vol. 84 , July 2011. PMID: 21867117.
[23] H. Haario, M. Laine, A. Mira, and E. Saksman, "DRAM: efficient
adaptive MCMC," Statistics and Computing, vol. 16, pp. 339-354, Dec.
2006.
@article{"International Journal of Biological, Life and Agricultural Sciences:54210", author = "G. Trigui and B. Laroche and M. Miquel and B. Dubreucq and A. Trubuil", title = "The Dynamics of Oil Bodies in A. thaliana Seeds: A Mathematical Model of Biogenesis and Coalescence", abstract = "The subcellular organelles called oil bodies (OBs) are lipid-filled quasi-spherical droplets produced from the endoplasmic reticulum (ER) and then released into the cytoplasm during seed development. It is believed that an OB grows by coalescence with other OBs and that its stability depends on the composition of oleosins, major proteins inserted in the hemi membrane that covers OBs. In this study, we measured the OB-volume distribution from different genotypes of A. thaliana after 7, 8, 9, 10 and 11 days of seed development. In order to test the hypothesis of OBs dynamics, we developed a simple mathematical model using non-linear differential equations inspired from the theory of coagulation. The model describes the evolution of OB-volume distribution during the first steps of seed development by taking into consideration the production of OBs, the increase of triacylglycerol volume to be stored, and the growth by coalescence of OBs. Fitted parameters values show an increase in the OB production and coalescence rates in A. thaliana oleosin mutants compared to wild type.
", keywords = "Biogenesis, coalescence, oil body, oleosin, population dynamics.", volume = "6", number = "4", pages = "149-6", }
