Dynamics of protein and polar lipid recruitment during lipid droplet assembly in Chlamydomonas reinhardtii

Plant Journal

Volumn 83, Issue 4, 2015, Pages 650-660

  Tsai, Chia Hong ^a   Zienkiewicz, Krzysztof ^b,c   Amstutz, Cynthia L ^b,e   Brink, Benedikt G ^d   Warakanont, Jaruswan ^a   Roston, Rebecca ^b,f   Benning, Christoph ^b  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b Michigan State University   (United States)

^c UNIVERSITY OF GÖTTINGEN   (Germany)

^d BIELEFELD UNIVERSITY   (Germany)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

algae; Chlamydomonas reinhardtii; lipid droplet; lipid metabolism; MLDP; plant

Indexed keywords

ALGAE; CELL PROLIFERATION; DROPS; FATTY ACIDS; HYDROPHOBICITY; LIPIDS; MEMBRANES; NITROGEN; SEED;

CHLAMYDOMONAS REINHARDTII; LIPID DROPLETS; LIPID METABOLISMS; MLDP; PLANT;

PROTEINS;

ALGAE; CHLAMYDOMONAS REINHARDTII; CHLOROPHYTA;

TRIACYLGLYCEROL; VEGETABLE PROTEIN;

CHLAMYDOMONAS REINHARDTII; CHLOROPLAST; LIPID METABOLISM; METABOLISM; PHYSIOLOGY;

CHLAMYDOMONAS REINHARDTII; CHLOROPLASTS; LIPID METABOLISM; PLANT PROTEINS; TRIGLYCERIDES;

EID: 84938990560     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12917     Document Type: Article

References (36)

1. Awai, K., Xu, C., Tamot, B., and, Benning, C., (2006) A phosphatidic acid-binding protein of the chloroplast inner envelope membrane involved in lipid trafficking. Proc. Natl Acad. Sci. U S A, 103, 10817-10822.
2. Benning, C., Huang, Z.H., and, Gage, D.A., (1995) Accumulation of a novel glycolipid and a betaine lipid in cells of Rhodobacter sphaeroides grown under phosphate limitation. Arch. Biochem. Biophys. 317, 103-111.
3. Brasaemle, D.L., (2007) Thematic review series: adipocyte biology. The perilipin family of structural lipid droplet proteins: stabilization of lipid droplets and control of lipolysis. J. Lipid Res. 48, 2547-2559.
4. Chapman, K.D., Dyer, J.M., and, Mullen, R.T., (2012) Biogenesis and functions of lipid droplets in plants: thematic review series: lipid droplet synthesis and metabolism: from yeast to man. J. Lipid Res. 53, 215-226.
5. Davidi, L., Katz, A., and, Pick, U., (2012) Characterization of major lipid droplet proteins from Dunaliella. Planta, 236, 19-33.
6. Fan, J., Andre, C., and, Xu, C., (2011) A chloroplast pathway for the de novo biosynthesis of triacylglycerol in Chlamydomonas reinhardtii. FEBS Lett., 585, 1985-1991.
7. Horn, P.J., James, C.N., Gidda, S.K., Kilaru, A., Dyer, J.M., Mullen, R.T., Ohlrogge, J.B., and, Chapman, K.D., (2013) Identification of a new class of lipid droplet-associated proteins in plants. Plant Physiol. 162, 1926-1936.
8. Hsieh, K., and, Huang, A.H., (2007) Tapetosomes in Brassica tapetum accumulate endoplasmic reticulum-derived flavonoids and alkanes for delivery to the pollen surface. Plant Cell, 19, 582-596.
9. Huang, A.H., (1996) Oleosins and oil bodies in seeds and other organs. Plant Physiol. 110, 1055-1061.
10. Huang, N.L., Huang, M.D., Chen, T.L., and, Huang, A.H., (2013) Oleosin of subcellular lipid droplets evolved in green algae. Plant Physiol. 161, 1862-1874.
11. James, C.N., Horn, P.J., Case, C.R., Gidda, S.K., Zhang, D., Mullen, R.T., Dyer, J.M., Anderson, R.G., and, Chapman, K.D., (2010) Disruption of the Arabidopsis CGI-58 homologue produces Chanarin-Dorfman-like lipid droplet accumulation in plants. Proc. Natl Acad. Sci. U S A, 107, 17833-17838.
12. James, G.O., Hocart, C.H., Hillier, W., Chen, H., Kordbacheh, F., Price, G.D., and, Djordjevic, M.A., (2011) Fatty acid profiling of Chlamydomonas reinhardtii under nitrogen deprivation. Bioresour. Technol. 102, 3343-3351.
13. Kikuchi, S., Hirohashi, T., and, Nakai, M., (2006) Characterization of the preprotein translocon at the outer envelope membrane of chloroplasts by blue native PAGE. Plant Cell Physiol. 47, 363-371.
14. Kim, H.U., Hsieh, K., Ratnayake, C., and, Huang, A.H., (2002) A novel group of oleosins is present inside the pollen of Arabidopsis. J. Biol. Chem. 277, 22677-22684.
15. Kimmel, A.R., Brasaemle, D.L., McAndrews-Hill, M., Sztalryd, C., and, Londos, C., (2010) Adoption of PERILIPIN as a unifying nomenclature for the mammalian PAT-family of intracellular lipid storage droplet proteins. J. Lipid Res. 51, 468-471.
16. Kunz, H.H., Scharnewski, M., Feussner, K., Feussner, I., Flugge, U.I., Fulda, M., and, Gierth, M., (2009) The ABC transporter PXA1 and peroxisomal beta-oxidation are vital for metabolism in mature leaves of Arabidopsis during extended darkness. Plant Cell, 21, 2733-2749.
17. Ladig, R., Sommer, M.S., Hahn, A., et al. (2011) A high-definition native polyacrylamide gel electrophoresis system for the analysis of membrane complexes. Plant J. 67, 181-194.
18. LeDizet, M., and, Piperno, G., (1986) Cytoplasmic microtubules containing acetylated alpha-tubulin in Chlamydomonas reinhardtii: spatial arrangement and properties. J. Cell Biol. 103, 13-22.
19. Lippold, F., vom Dorp, K., Abraham, M., et al. (2012) Fatty acid phytyl ester synthesis in chloroplasts of Arabidopsis. Plant Cell, 24, 2001-2014.
20. Miller, R., Wu, G., Deshpande, R.R., et al. (2010) Changes in transcript abundance in Chlamydomonas reinhardtii following nitrogen deprivation predict diversion of metabolism. Plant Physiol. 154, 1737-1752.
21. Moellering, E.R., and, Benning, C., (2010) RNA interference silencing of a major lipid droplet protein affects lipid droplet size in Chlamydomonas reinhardtii. Eukaryot. Cell, 9, 97-106.
22. Mussgnug, J.H., Wobbe, L., Elles, I., et al. (2005) NAB1 is an RNA binding protein involved in the light-regulated differential expression of the light-harvesting antenna of Chlamydomonas reinhardtii. Plant Cell, 17, 3409-3421.
23. Nguyen, H.M., Baudet, M., Cuine, S., et al. (2011) Proteomic profiling of oil bodies isolated from the unicellular green microalga Chlamydomonas reinhardtii: with focus on proteins involved in lipid metabolism. Proteomics, 11, 4266-4273.
24. Peled, E., Leu, S., Zarka, A., Weiss, M., Pick, U., Khozin-Goldberg, I., and, Boussiba, S., (2011) Isolation of a novel oil globule protein from the green alga Haematococcus pluvialis (Chlorophyceae). Lipids, 46, 851-861.
25. Rossak, M., Schafer, A., Xu, N., Gage, D.A., and, Benning, C., (1997) Accumulation of sulfoquinovosyl-1-O-dihydroxyacetone in a sulfolipid-deficient mutant of Rhodobacter sphaeroides inactivated in sqdC. Arch. Biochem. Biophys. 340, 219-230.
26. Rottet, S., Besagni, C., and, Kessler, F., (2015) The role of plastoglobules in thylakoid lipid remodeling during plant development. Biochim. Biophys. Acta, 1847, 889-899.
27. Schmollinger, S., Muhlhaus, T., Boyle, N.R., et al. (2014) Nitrogen-sparing mechanisms in Chlamydomonas affect the transcriptome, the proteome, and photosynthetic metabolism. Plant Cell, 26, 1410-1435.
28. Shevchenko, A., Wilm, M., Vorm, O., and, Mann, M., (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858.
29. Siloto, R.M., Findlay, K., Lopez-Villalobos, A., Yeung, E.C., Nykiforuk, C.L., and, Moloney, M.M., (2006) The accumulation of oleosins determines the size of seed oilbodies in Arabidopsis. Plant Cell, 18, 1961-1974.
30. Tauchi-Sato, K., Ozeki, S., Houjou, T., Taguchi, R., and, Fujimoto, T., (2002) The surface of lipid droplets is a phospholipid monolayer with a unique fatty acid composition. J. Biol. Chem. 277, 44507-44512.
31. Tsai, C.H., Warakanont, J., Takeuchi, T., Sears, B.B., Moellering, E.R., and, Benning, C., (2014) The protein compromised Hydrolysis of Triacylglycerols 7 (CHT7) acts as a repressor of cellular quiescence in Chlamydomonas. Proc. Natl Acad. Sci. U S A, 111, 15833-15838.
32. Walther, T.C., and, Farese, R.V. Jr, (2012) Lipid droplets and cellular lipid metabolism. Annu. Rev. Biochem. 81, 687-714.
33. Wang, Z.T., Ullrich, N., Joo, S., Waffenschmidt, S., and, Goodenough, U., (2009) Algal lipid bodies: stress induction, purification, and biochemical characterization in wild-type and starchless Chlamydomonas reinhardtii. Eukaryot. Cell, 8, 1856-1868.
34. Welte, M.A., (2007) Proteins under new management: lipid droplets deliver. Trends Cell Biol. 17, 363-369.
35. Welte, M.A., Gross, S.P., Postner, M., Block, S.M., and, Wieschaus, E.F., (1998) Developmental regulation of vesicle transport in Drosophila embryos: forces and kinetics. Cell, 92, 547-557.
36. Yang, Y., Yu, X., Song, L., and, An, C., (2011) ABI4 activates DGAT1 expression in Arabidopsis seedlings during nitrogen deficiency. Plant Physiol. 156, 873-883.