Ubiquitin-mediated proteasomal degradation of oleosins is involved in oil body mobilization during post-germinative seedling growth in Arabidopsis

Plant and Cell Physiology

Volumn 56, Issue 7, 2015, Pages 1374-1387

  Deruyffelaere, Carine ^a,b   Bouchez, Isabelle ^a,b   Morin, Halima ^a,b   Guillot, Alain ^c   Miquel, Martine ^a,b   Froissard, Marine ^a,b   Chardot, Thierry ^a,b   D'Andrea, Sabine ^a,b  

^a INSTITUT JEAN PIERRE BOURGIN   (France)

^b AGROPARISTECH   (France)

^c UMR1319 MICALIS   (France)

Author keywords

Arabidopsis; Oil body; Oleosin; Proteasome; Seed; Ubiquitin mediated degradation

Indexed keywords

ARABIDOPSIS PROTEIN; BENZYLOXYCARBONYLLEUCYL-LEUCYL-LEUCINE ALDEHYDE; CYSTEINE PROTEINASE INHIBITOR; FAT DROPLET; GREEN FLUORESCENT PROTEIN; ISOPROTEIN; LEUPEPTIN; OLEOSIN PROTEIN, ARABIDOPSIS; PROTEASOME; UBIQUITIN;

ARABIDOPSIS; CONFOCAL MICROSCOPY; DRUG EFFECTS; GENETICS; GERMINATION; GROWTH, DEVELOPMENT AND AGING; IMMUNOBLOTTING; METABOLISM; PHOSPHORYLATION; PLANT SEED; PROCEDURES; PROTEIN DEGRADATION; PROTEOMICS; SEEDLING; TIME FACTOR; TRANSGENIC PLANT; UBIQUITINATION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CYSTEINE PROTEINASE INHIBITORS; GERMINATION; GREEN FLUORESCENT PROTEINS; IMMUNOBLOTTING; LEUPEPTINS; LIPID DROPLETS; MICROSCOPY, CONFOCAL; PHOSPHORYLATION; PLANTS, GENETICALLY MODIFIED; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN ISOFORMS; PROTEOLYSIS; PROTEOMICS; SEEDLINGS; SEEDS; TIME FACTORS; UBIQUITIN; UBIQUITINATION;

EID: 84940932767     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcv056     Document Type: Article

References (69)

1. Barberon, M., Zelazny, E., Robert, S., Conejero, G., Curie, C., Friml, J. et al. (2011) Monoubiquitin-dependent endocytosis of the iron-regulated transporter 1 (IRT1) transporter controls iron uptake in plants. Proc. Natl Acad. Sci USA 108:E450-E458.
2. Bechtold, N. and Pelletier, G. (1998) In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. Methods Mol. Biol. 82:259-266.
3. Beisson, F., Ferte, N., Bruley, S., Voultoury, R., Verger, R. and Arondel, V. (2001) Oil-bodies as substrates for lipolytic enzymes. Biochim. Biophys. Acta 1531:47-58.
4. Bewley, J. D. (1997) Seed germination and dormancy. Plant Cell 9:1055-1066.
5. Bolte, S., Lanquar, V., Soler, M. N., Beebo, A., Satiat-Jeunemaitre, B., Bouhidel, K. et al. (2011) Distinct lytic vacuolar compartments are embedded inside the protein storage vacuole of dry and germinating Arabidopsis thaliana seeds. Plant Cell Physiol. 52:1142-1152.
6. Browse, J., McCourt, P. J. and Somerville, C. R. (1986) Fatty acid composition of leaf lipids determined after combined digestion and fatty acid methyl ester formation from fresh tissue. Anal. Biochem. 152:141-145.
7. Chapman, K. D. and Trelease, R. N. (1991) Acquisition of membrane lipids by differentiating glyoxysomes: role of lipid bodies. J. Cell Biol. 115:995-1007.
8. Chen, Y., Zhao, L., Cao, Y., Kong, X. and Hua, Y. (2014) Oleosins (24 and 18 kDa) are hydrolyzed not only in extracted soybean oil bodies but also in soybean germination. J. Agric. Food Chem. 62:956-965.
9. Chew, K. C., Matsuda, N., Saisho, K., Lim, G. G., Chai, C., Tan, H. M. et al. (2011) Parkin mediates apparent E2-independent monoubiquitination in vitro and contains an intrinsic activity that catalyzes polyubiquitina-tion. PLoS One 6:e19720.
10. Ciechanover, A. and Stanhill, A. (2014) The complexity of recognition of ubiquitinated substrates by the 26S proteasome. Biochim. Biophys. Acta 1843:86-96.
11. Curtis, M. D. and Grossniklaus, U. (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 133:462-469.
12. D'Andrea, S., Jolivet, P., Boulard, C., Larre, C., Froissard, M. and Chardot, T. (2007) Selective one-step extraction of Arabidopsis thaliana seed oleo-sins using organic solvents. J. Agric. Food Chem. 55:10008-10015.
13. Eastmond, P. J. (2006) SUGAR-DEPENDENT1 encodes a patatin domain triacylglycerol lipase that initiates storage oil breakdown in germinating Arabidopsis seeds. Plant Cell 18:665-675.
14. Fernandez, D. E., Qu, R., Huang, A. H. and Staehelin, L. A. (1988) Immunogold localization of the L3 protein of maize lipid bodies during germination and seedling growth. Plant Physiol. 86:270-274.
15. Fernandez, D. E. and Staehelin, L. A. (1987) Does gibberellic acid induce the transfer of lipase from protein bodies to lipid bodies in barley aleurone cells? Plant Physiol. 85:487-496.
16. Froissard, M., D'Andrea, S., Boulard, C. and Chardot, T. (2009) Heterologous expression of AtClo1, a plant oil body protein, induces lipid accumulation in yeast. FEMS Yeast Res. 9:428-438.
17. Fujimuro, M., Sawada, H. and Yokosawa, H. (1994) Production and characterization of monoclonal antibodies specific to multi-ubiquitin chains of polyubiquitinated proteins. FEBS Lett. 349:173-180.
18. Graham, I. A. (2008) Seed storage oil mobilization. Annu. Rev. Plant Biol. 59:115-142.
19. Guerra, D. D. and Callis, J. (2012) Ubiquitin on the move: the ubiquitin modification system plays diverse roles in the regulation of endoplas-mic reticulum- and plasma membrane-localized proteins. Plant Physiol 160:56-64.
20. Guo, Y., Walther, T. C., Rao, M., Stuurman, N., Goshima, G., Terayama, K. et al. (2008) Functional genomic screen reveals genes involved in lipid-droplet formation and utilization. Nature 453:657-661.
21. Haglund, K., Sigismund, S., Polo, S., Szymkiewicz, I., Di Fiore, P. P. and Dikic, I. (2003) Multiple monoubiquitination of RTKs is sufficient for their endocytosis and degradation. Nat. Cell Biol. 5:461-466.
22. Hayashi, Y., Hayashi, M., Hayashi, H., Hara-Nishimura, I. and Nishimura, M. (2001) Direct interaction between glyoxysomes and lipid bodies in cotyledons of the Arabidopsis thaliana ped1 mutant. Protoplasma 218:83-94.
23. Horn, P. J., James, C. N., Gidda, S. K., Kilaru, A., Dyer, J. M., Mullen, R. T. et al. (2013) Identification of a new class of lipid droplet-associated proteins in plants. Plant Physiol. 162:1926-1936.
24. Hsiao, E. S. and Tzen, J. T. (2011) Ubiquitination of oleosin-H and caleosin in sesame oil bodies after seed germination. Plant Physiol. Biochem. 49:77-81.
25. Huang, A. H. C. (1992) Oil bodies and oleosins in seeds. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43:177-200.
26. Jacquier, N., Mishra, S., Choudhary, V. and Schneiter, R. (2013) Expression of oleosin and perilipins in yeast promotes formation of lipid droplets from the endoplasmic reticulum. J. Cell Sci. 126:5198-5209.
27. Jolivet, P., Acevedo, F., Boulard, C., D'Andrea, S., Faure, J. D., Kohli, A. et al. (2013) Crop seed oil bodies: from challenges in protein identification to an emerging picture of the oil body proteome. Proteomics 13:1836-1849.
28. Jolivet, P., Boulard, C., Bellamy, A., Larre, C., Barre, M., Rogniaux, H. et al. (2009) Protein composition of oil bodies from mature Brassica napus seeds. Proteomics 9:3268-3284.
29. Jolivet, P., Boulard, C., Bellamy, A., Valot, B., D'Andrea, S., Zivy, M. et al. (2011) Oil body proteins sequentially accumulate throughout seed development in Brassica napus. J. Plant Physiol. 168:2015-2020.
30. Jolivet, P., Roux, E., D'Andrea, S., Davanture, M., Negroni, L., Zivy, M. et al. (2004) Protein composition of oil bodies in Arabidopsis thaliana eco-type WS. Plant Physiol. Biochem. 42:501-509.
31. Kelly, A. A., Quettier, A. L., Shaw, E. and Eastmond, P. J. (2011) Seed storage oil mobilization is important but not essential for germination or seedling establishment in Arabidopsis. Plant Physiol. 157:866-875.
32. Khor, V. K., Shen, W.-J. and Kraemer, F. B. (2013) Lipid droplet metabolism. Curr. Opin. Clin. Nutr. Metab. Care 16:632-637.
33. Kim, H. U., Hsieh, K., Ratnayake, C. and Huang, A. H. C. (2002) A novel group of oleosins is present inside the pollen of Arabidopsis. J. Biol. Chem. 277:22677-22684.
34. Kinoshita, E. and Kinoshita-Kikuta, E. (2011) Improved Phos-tag SDS-PAGE under neutral pH conditions for advanced protein phosphoryl-ation profiling. Proteomics 11:319-323.
35. Krahmer, N., Farese, R. V. Jr and Walther, T. C. (2013) Balancing the fat: lipid droplets and human disease. EMBO Mol. Med. 5:905-915.
36. Lacey, D. J., Wellner, N., Beaudoin, F., Napier, J. A. and Shewry, P. R. (1998) Secondary structure of oleosins in oil bodies isolated from seeds of safflower (Carthamus tinctorius L.) and sunflower (Helianthus annuus L.). Biochem. J. 334:469-477.
37. Lee, D. H. and Goldberg, A. L. (1998) Proteasome inhibitors: valuable new tools for cell biologists. Trends Cell Biol. 8:397-403.
38. Leitner, J., Petrasek, J., Tomanov, K., Retzer, K., Parezova, M., Korbei, B. et al. (2012) Lysine63-linked ubiquitylation of PIN2 auxin carrier protein governs hormonally controlled adaptation of Arabidopsis root growth. Proc. Natl Acad. Sci. USA 109:8322-8327.
39. Leprince, O., Van Aelst, A. C., Pritchard, H. W. and Murphy, D. J. (1997) Oleosins prevent oil-body coalescence during seed imbibition as suggested by a low-temperature scanning electron microscope study of desiccation-tolerant and -sensitive oilseeds. Planta 204:109-119.
40. Liavonchanka, A. and Feussner, I. (2006) Lipoxygenases: occurrence, functions and catalysis. J. Plant Physiol. 163:348-357.
41. Matsui, K., Hijiya, K., Tabuchi, Y. and Kajiwara, T. (1999) Cucumber cotyledon lipoxygenase during postgerminative growth.its expression and action on lipid bodies. Plant Physiol. 119:1279-1288.
42. Miquel, M., Trigui, G., D'Andréa, S., Kelemen, Z., Baud, S. B., Berger, A. et al. (2014) Specialization of oleosins in oil body dynamics during seed development in arabidopsis seeds. Plant Physiol. 164:1866-1878.
43. Murphy, D. J. (2012) The dynamic roles of intracellular lipid droplets: from archaea to mammals. Protoplasma 249:541-585.
44. Murphy, D. J., Cummins, I. and Kang, A. S. (1989) Immunocytochemical and biochemical studies of the mobilisation of storage oil-bodies and proteins in germinating cotyledons of oilseed rape, Brassica napus. J. Sci. Food Agric. 48:209-223.
45. Murphy, D. J. and Vance, J. (1999) Mechanisms of lipid-body formation. Trends Biochem. Sci. 24:109-115.
46. Noll, F., May, C. and Kindl, H. (2000) Phospholipid monolayer of plant lipid bodies attacked by phospholipase A2 shows 80 nm holes analyzed by atomic force microscopy. Biophys. Chem. 86:29-35.
47. Parthibane, V., Iyappan, R., Vijayakumar, A., Venkateshwari, V. and Rajasekharan, R. (2012) Serine/threonine/tyrosine protein kinase phos-phorylates oleosin, a regulator of lipid metabolic functions. Plant Physiol. 159:95-104.
48. Penfield, S., Pinfield-Wells, H. M. and Graham, I. A. (2006) Storage reserve mobilisation and seedling establishment in Arabidopsis. Arabidopsis Book 4:e0100.
49. Poxleitner, M., Rogers, S. W., Lacey Samuels, A., Browse, J. and Rogers, J. C. (2006) A role for caleosin in degradation of oil-body storage lipid during seed germination. Plant J. 47:917-933.
50. Radetzky, R. and Langheinrich, U. (1994) Induction of accumulation and degradation of the 18.4-kDa oleosin in a triacylglycerol-storing cell culture of anise (Pimpinella anisum L.). Planta 194:1-8.
51. Rottet, S., Besagni, C. and Kessler, F. (2015) The role of plastoglobules in thylakoid lipid remodeling during plant development. Biochim. Biophys. Acta, doi: 10.1016/j.bbabio.2015.02.002.
52. Sadeghipour, H. R. and Bhatla, S. C. (2002) Differential sensitivity of oleosins to proteolysis during oil body mobilization in sunflower seedlings. Plant Cell Physiol. 43:1117-1126.
53. Schlereth, A., Standhardt, D., Mock, H.-P. and Müntz, K. (2001) Stored cysteine proteinases start globulin mobilization in protein bodies of embryonic axes and cotyledons during vetch (Vicia sativa L.) seed germination. Planta 212:718-727.
54. Schmidt, M. A. and Herman, E. M. (2008) Suppression of soybean oleosin produces micro-oil bodies that aggregate into oil body/ER complexes. Mol. Plant 1:910-924.
55. Shabek, N., Herman-Bachinsky, Y., Buchsbaum, S., Lewinson, O., Haj-Yahya, M., Hejjaoui, M. et al. (2012) The size of the proteasomal substrate determines whether its degradation will be mediated by mono- or polyubiquitylation. Mol. Cell 48:87-97.
56. Shevchenko, A., Tomas, H., Havlis, J., Olsen, J. V. and Mann, M. (2006) In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat. Protoc. 1:2856-2860.
57. Shimada, T. L., Shimada, T., Takahashi, H., Fukao, Y. and Hara-Nishimura, I. (2008) A novel role for oleosins in freezing tolerance of oilseeds in Arabidopsis thaliana. Plant J. 55:798-809.
58. 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.
59. Sun, Z., Gong, J., Wu, H., Xu, W., Wu, L., Xu, D. et al. (2013) Perilipin1 promotes unilocular lipid droplet formation through the activation of Fsp27 in adipocytes. Nat. Commun. 4:1594.
60. Thiam, A. R., Farese, R. V. Jr and Walther, T. C. (2013) The biophysics and cell biology of lipid droplets. Nat. Rev. Mol. Cell Biol. 14:775-786.
61. Tiedemann, J., Neubohn, B. and Muntz, K. (2000) Different functions of vicilin and legumin are reflected in the histopattern of globulin mobilization during germination of vetch (Vicia sativa L.). Planta 211:1-12.
62. Tzen, J. T. and Huang, A. H. (1992) Surface structure and properties of plant seed oil bodies. J. Cell Biol. 117:327-335.
63. Tzen, J. T., Peng, C. C., Cheng, D. J., Chen, E. C. and Chiu, J. M. (1997) A new method for seed oil body purification and examination of oil body integrity following germination. J. Biochem. 121:762-768.
64. Vandana, S. and Bhatla, S. C. (2006) Evidence for the probable oil body association of a thiol-protease, leading to oleosin degradation in sunflower seedling cotyledons. Plant Physiol. Biochem. 44:714-723.
65. Winichayakul, S., Scott, R. W., Roldan, M., Hatier, J.-H. B., Livingston, S., Cookson, R. et al. (2013) In vivo packaging of triacylglycerols enhances Arabidopsis leaf biomass and energy density. Plant Physiol. 162:626-639.
66. Xu, G., Sztalryd, C. and Londos, C. (2006) Degradation of perilipin is mediated through ubiquitination-proteasome pathway. Biochim. Biophys. Acta 1761:83-90.
67. Xu, G., Sztalryd, C., Lu, X., Tansey, J. T., Gan, J., Dorward, H. et al. (2005) Post-translational regulation of adipose differentiation-related protein by the ubiquitin/proteasome pathway. J. Biol. Chem. 280:42841-42847.
68. Zheng, H. and Staehelin, L. A. (2011) Protein storage vacuoles are transformed into lytic vacuoles in root meristematic cells of germinating seedlings by multiple, cell type-specific mechanisms. Plant Physiol. 155:2023-2035.
69. Zienkiewicz, A., Zienkiewicz, K., Rejón, J. D., De Dios Alché, J., Castro, A. J. and Rodríguez-García, M. I. (2014) Olive seed protein bodies store degrading enzymes involved in mobilization of oil bodies. J. Exp. Bot. 65:103-115.