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

Tsai C-H, Zienkiewicz K, Amstutz CL, Brink B, Warakanont J, Roston R, Benning C (2015)
The Plant Journal 83(4): 650-660.

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Zeitschriftenaufsatz | Veröffentlicht | Englisch
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Abstract / Bemerkung
In plants, neutral lipids are frequently synthesized and stored in seed tissues, where the assembly of lipid droplets (LDs) coincides with the accumulation of triacylglycerols (TAGs). In addition, photosynthetic, vegetative cells can form cytosolic LDs and much less information is known about the makeup and biogenesis of these LDs. Here we focus on Chlamydomonas reinhardtii as a reference model for LDs in a photosynthetic cell, because in this unicellular green alga LD dynamics can be readily manipulated by nitrogen availability. Nitrogen deprivation leads to cellular quiescence during which cell divisions cease and TAGs accumulate. The major lipid droplet protein (MLDP) forms a proteinaceous coat surrounding mature LDs. Reducing the amount of MLDP affects LD size and number, TAG breakdown and timely progression out of cellular quiescence following nitrogen resupply. Depending on nitrogen availability, MLDP recruits different proteins to LDs, tubulins in particular. Conversely, depolymerization of microtubules drastically alters the association of MLDP with LDs. LDs also contain select chloroplast envelope membrane proteins hinting at an origin of LDs, at least in part, from chloroplast membranes. Moreover, LD surface lipids are rich in de novo synthesized fatty acids, and are mainly composed of galactolipids which are typical components of chloroplast membranes. The composition of the LD membrane is altered in the absence of MLDP. Collectively, our results suggest a mechanism for LD formation in C.reinhardtii involving chloroplast envelope membranes by which specific proteins are recruited to LDs and a specialized polar lipid monolayer surrounding the LD is formed. Significance Statement Lipid droplets (LDs) are dynamic organelles of virtually every cell type and are involved in numerous metabolic and physiological processes. Many aspects of LD biology, particularly in photosynthetic cells remain obscure. Using Chlamydomonas reinhardtii as a model, we uncovered an interaction of microtubules with the major lipid droplet protein affecting protein targeting to LDs. We also provide evidence for a specialized polar lipid composition of LDs suggesting an origin of LDs from chloroplast envelope membranes.
Erscheinungsjahr
Zeitschriftentitel
The Plant Journal
Band
83
Ausgabe
4
Seite(n)
650-660
ISSN
PUB-ID

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Tsai C-H, Zienkiewicz K, Amstutz CL, et al. Dynamics of protein and polar lipid recruitment during lipid droplet assembly in Chlamydomonas reinhardtii. The Plant Journal. 2015;83(4):650-660.
Tsai, C. - H., Zienkiewicz, K., Amstutz, C. L., Brink, B., Warakanont, J., Roston, R., & Benning, C. (2015). Dynamics of protein and polar lipid recruitment during lipid droplet assembly in Chlamydomonas reinhardtii. The Plant Journal, 83(4), 650-660. doi:10.1111/tpj.12917
Tsai, C. - H., Zienkiewicz, K., Amstutz, C. L., Brink, B., Warakanont, J., Roston, R., and Benning, C. (2015). Dynamics of protein and polar lipid recruitment during lipid droplet assembly in Chlamydomonas reinhardtii. The Plant Journal 83, 650-660.
Tsai, C.-H., et al., 2015. Dynamics of protein and polar lipid recruitment during lipid droplet assembly in Chlamydomonas reinhardtii. The Plant Journal, 83(4), p 650-660.
C.-H. Tsai, et al., “Dynamics of protein and polar lipid recruitment during lipid droplet assembly in Chlamydomonas reinhardtii”, The Plant Journal, vol. 83, 2015, pp. 650-660.
Tsai, C.-H., Zienkiewicz, K., Amstutz, C.L., Brink, B., Warakanont, J., Roston, R., Benning, C.: Dynamics of protein and polar lipid recruitment during lipid droplet assembly in Chlamydomonas reinhardtii. The Plant Journal. 83, 650-660 (2015).
Tsai, Chia-Hong, Zienkiewicz, Krzysztof, Amstutz, Cynthia L., Brink, Benedikt, Warakanont, Jaruswan, Roston, Rebecca, and Benning, Christoph. “Dynamics of protein and polar lipid recruitment during lipid droplet assembly in Chlamydomonas reinhardtii”. The Plant Journal 83.4 (2015): 650-660.

19 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Revisiting the Algal "Chloroplast Lipid Droplet": The Absence of an Entity That Is Unlikely to Exist.
Moriyama T, Toyoshima M, Saito M, Wada H, Sato N., Plant Physiol 176(2), 2018
PMID: 29061905
Recovery from N Deprivation Is a Transcriptionally and Functionally Distinct State in Chlamydomonas.
Tsai CH, Uygun S, Roston R, Shiu SH, Benning C., Plant Physiol 176(3), 2018
PMID: 29288234
Endoplasmic reticulum acyltransferase with prokaryotic substrate preference contributes to triacylglycerol assembly in Chlamydomonas.
Kim Y, Terng EL, Riekhof WR, Cahoon EB, Cerutti H., Proc Natl Acad Sci U S A 115(7), 2018
PMID: 29382746
Autophagic flux is required for the synthesis of triacylglycerols and ribosomal protein turnover in Chlamydomonas.
Couso I, Pérez-Pérez ME, Martínez-Force E, Kim HS, He Y, Umen JG, Crespo JL., J Exp Bot 69(6), 2018
PMID: 29053817
3D Reconstruction of Lipid Droplets in the Seed of Brassica napus.
Yin Y, Guo L, Chen K, Guo Z, Chao H, Wang B, Li M., Sci Rep 8(1), 2018
PMID: 29700334
Tobacco pollen tubes - a fast and easy tool for studying lipid droplet association of plant proteins.
Müller AO, Blersch KF, Gippert AL, Ischebeck T., Plant J 89(5), 2017
PMID: 27943529
Proteomic Analysis of Lipid Droplets from Arabidopsis Aging Leaves Brings New Insight into Their Biogenesis and Functions.
Brocard L, Immel F, Coulon D, Esnay N, Tuphile K, Pascal S, Claverol S, Fouillen L, Bessoule JJ, Bréhélin C., Front Plant Sci 8(), 2017
PMID: 28611809
Analysis of the lipid body proteome of the oleaginous alga Lobosphaera incisa.
Siegler H, Valerius O, Ischebeck T, Popko J, Tourasse NJ, Vallon O, Khozin-Goldberg I, Braus GH, Feussner I., BMC Plant Biol 17(1), 2017
PMID: 28587627
Arabidopsis lipid droplet-associated protein (LDAP) - interacting protein (LDIP) influences lipid droplet size and neutral lipid homeostasis in both leaves and seeds.
Pyc M, Cai Y, Gidda SK, Yurchenko O, Park S, Kretzschmar FK, Ischebeck T, Valerius O, Braus GH, Chapman KD, Dyer JM, Mullen RT., Plant J 92(6), 2017
PMID: 29083105
Fatty Acid and Lipid Transport in Plant Cells.
Li N, Xu C, Li-Beisson Y, Philippar K., Trends Plant Sci 21(2), 2016
PMID: 26616197
Lipid Droplet-Associated Proteins (LDAPs) Are Required for the Dynamic Regulation of Neutral Lipid Compartmentation in Plant Cells.
Gidda SK, Park S, Pyc M, Yurchenko O, Cai Y, Wu P, Andrews DW, Chapman KD, Dyer JM, Mullen RT., Plant Physiol 170(4), 2016
PMID: 26896396
Antimicrobial cocktails to control bacterial and fungal contamination in Chlamydomonas reinhardtii cultures.
Wang L, Yang F, Chen H, Fan Z, Zhou Y, Lu J, Zheng Y., Biotechniques 60(3), 2016
PMID: 26956093
Saturating Light Induces Sustained Accumulation of Oil in Plastidal Lipid Droplets in Chlamydomonas reinhardtii.
Goold HD, Cuiné S, Légeret B, Liang Y, Brugière S, Auroy P, Javot H, Tardif M, Jones B, Beisson F, Peltier G, Li-Beisson Y., Plant Physiol 171(4), 2016
PMID: 27297678
The plant lipidome in human and environmental health.
Horn PJ, Benning C., Science 353(6305), 2016
PMID: 27634522
Label-free in vivo analysis of intracellular lipid droplets in the oleaginous microalga Monoraphidium neglectum by coherent Raman scattering microscopy.
Jaeger D, Pilger C, Hachmeister H, Oberländer E, Wördenweber R, Wichmann J, Mussgnug JH, Huser T, Kruse O., Sci Rep 6(), 2016
PMID: 27767024

36 References

Daten bereitgestellt von Europe PubMed Central.

A phosphatidic acid-binding protein of the chloroplast inner envelope membrane involved in lipid trafficking.
Awai K, Xu C, Tamot B, Benning C., Proc. Natl. Acad. Sci. U.S.A. 103(28), 2006
PMID: 16818883
Characterization of major lipid droplet proteins from Dunaliella.
Davidi L, Katz A, Pick U., Planta 236(1), 2012
PMID: 22231009
Identification of a new class of lipid droplet-associated proteins in plants.
Horn PJ, James CN, Gidda SK, Kilaru A, Dyer JM, Mullen RT, Ohlrogge JB, Chapman KD., Plant Physiol. 162(4), 2013
PMID: 23821652
Oleosins and oil bodies in seeds and other organs.
Huang AH., Plant Physiol. 110(4), 1996
PMID: 8934621
Oleosin of subcellular lipid droplets evolved in green algae.
Huang NL, Huang MD, Chen TL, Huang AH., Plant Physiol. 161(4), 2013
PMID: 23391579
Disruption of the Arabidopsis CGI-58 homologue produces Chanarin-Dorfman-like lipid droplet accumulation in plants.
James CN, Horn PJ, Case CR, Gidda SK, Zhang D, Mullen RT, Dyer JM, Anderson RG, Chapman KD., Proc. Natl. Acad. Sci. U.S.A. 107(41), 2010
PMID: 20876112
Fatty acid profiling of Chlamydomonas reinhardtii under nitrogen deprivation.
James GO, Hocart CH, Hillier W, Chen H, Kordbacheh F, Price GD, Djordjevic MA., Bioresour. Technol. 102(3), 2010
PMID: 21146403
A novel group of oleosins is present inside the pollen of Arabidopsis.
Kim HU, Hsieh K, Ratnayake C, Huang AH., J. Biol. Chem. 277(25), 2002
PMID: 11929861
Adoption of PERILIPIN as a unifying nomenclature for the mammalian PAT-family of intracellular lipid storage droplet proteins.
Kimmel AR, Brasaemle DL, McAndrews-Hill M, Sztalryd C, Londos C., J. Lipid Res. 51(3), 2009
PMID: 19638644
The ABC transporter PXA1 and peroxisomal beta-oxidation are vital for metabolism in mature leaves of Arabidopsis during extended darkness.
Kunz HH, Scharnewski M, Feussner K, Feussner I, Flugge UI, Fulda M, Gierth M., Plant Cell 21(9), 2009
PMID: 19794119
A high-definition native polyacrylamide gel electrophoresis system for the analysis of membrane complexes.
Ladig R, Sommer MS, Hahn A, Leisegang MS, Papasotiriou DG, Ibrahim M, Elkehal R, Karas M, Zickermann V, Gutensohn M, Brandt U, Klosgen RB, Schleiff E., Plant J. 67(1), 2011
PMID: 21418111
Fatty acid phytyl ester synthesis in chloroplasts of Arabidopsis.
Lippold F, vom Dorp K, Abraham M, Holzl G, Wewer V, Yilmaz JL, Lager I, Montandon C, Besagni C, Kessler F, Stymne S, Dormann P., Plant Cell 24(5), 2012
PMID: 22623494
Changes in transcript abundance in Chlamydomonas reinhardtii following nitrogen deprivation predict diversion of metabolism.
Miller R, Wu G, Deshpande RR, Vieler A, Gartner K, Li X, Moellering ER, Zauner S, Cornish AJ, Liu B, Bullard B, Sears BB, Kuo MH, Hegg EL, Shachar-Hill Y, Shiu SH, Benning C., Plant Physiol. 154(4), 2010
PMID: 20935180
NAB1 is an RNA binding protein involved in the light-regulated differential expression of the light-harvesting antenna of Chlamydomonas reinhardtii.
Mussgnug JH, Wobbe L, Elles I, Claus C, Hamilton M, Fink A, Kahmann U, Kapazoglou A, Mullineaux CW, Hippler M, Nickelsen J, Nixon PJ, Kruse O., Plant Cell 17(12), 2005
PMID: 16284312
Proteomic profiling of oil bodies isolated from the unicellular green microalga Chlamydomonas reinhardtii: with focus on proteins involved in lipid metabolism.
Nguyen HM, Baudet M, Cuine S, Adriano JM, Barthe D, Billon E, Bruley C, Beisson F, Peltier G, Ferro M, Li-Beisson Y., Proteomics 11(21), 2011
PMID: 21928291
Isolation of a novel oil globule protein from the green alga Haematococcus pluvialis (Chlorophyceae).
Peled E, Leu S, Zarka A, Weiss M, Pick U, Khozin-Goldberg I, Boussiba S., Lipids 46(9), 2011
PMID: 21732215
Accumulation of sulfoquinovosyl-1-O-dihydroxyacetone in a sulfolipid-deficient mutant of Rhodobacter sphaeroides inactivated in sqdC.
Rossak M, Schafer A, Xu N, Gage DA, Benning C., Arch. Biochem. Biophys. 340(2), 1997
PMID: 9143325
The role of plastoglobules in thylakoid lipid remodeling during plant development.
Rottet S, Besagni C, Kessler F., Biochim. Biophys. Acta 1847(9), 2015
PMID: 25667966
Nitrogen-Sparing Mechanisms in Chlamydomonas Affect the Transcriptome, the Proteome, and Photosynthetic Metabolism.
Schmollinger S, Muhlhaus T, Boyle NR, Blaby IK, Casero D, Mettler T, Moseley JL, Kropat J, Sommer F, Strenkert D, Hemme D, Pellegrini M, Grossman AR, Stitt M, Schroda M, Merchant SS., Plant Cell 26(4), 2014
PMID: 24748044
Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels.
Shevchenko A, Wilm M, Vorm O, Mann M., Anal. Chem. 68(5), 1996
PMID: 8779443
The accumulation of oleosins determines the size of seed oilbodies in Arabidopsis.
Siloto RM, Findlay K, Lopez-Villalobos A, Yeung EC, Nykiforuk CL, Moloney MM., Plant Cell 18(8), 2006
PMID: 16877495
The surface of lipid droplets is a phospholipid monolayer with a unique Fatty Acid composition.
Tauchi-Sato K, Ozeki S, Houjou T, Taguchi R, Fujimoto T., J. Biol. Chem. 277(46), 2002
PMID: 12221100
The protein Compromised Hydrolysis of Triacylglycerols 7 (CHT7) acts as a repressor of cellular quiescence in Chlamydomonas.
Tsai CH, Warakanont J, Takeuchi T, Sears BB, Moellering ER, Benning C., Proc. Natl. Acad. Sci. U.S.A. 111(44), 2014
PMID: 25313078
Lipid droplets and cellular lipid metabolism.
Walther TC, Farese RV Jr., Annu. Rev. Biochem. 81(), 2012
PMID: 22524315
Proteins under new management: lipid droplets deliver.
Welte MA., Trends Cell Biol. 17(8), 2007
PMID: 17766117
Developmental regulation of vesicle transport in Drosophila embryos: forces and kinetics.
Welte MA, Gross SP, Postner M, Block SM, Wieschaus EF., Cell 92(4), 1998
PMID: 9491895
ABI4 activates DGAT1 expression in Arabidopsis seedlings during nitrogen deficiency.
Yang Y, Yu X, Song L, An C., Plant Physiol. 156(2), 2011
PMID: 21515696

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