Sucrose production mediated by lipid metabolism suppresses the physical interaction of peroxisomes and oil bodies during germination of arabidopsis thaliana

Journal of Biological Chemistry

Volumn 291, Issue 38, 2016, Pages 19734-19745

  Cui, Songkui ^a,b,c,f   Hayashi, Yasuko ^d   Otomo, Masayoshi ^d   Mano, Shoji ^a,b   Oikawa, Kazusato ^d   Hayashi, Makoto ^e   Nishimura, Mikio ^a  

^a NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

^b GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^c Elements Chemistry Laboratory   (Japan)

^d NIIGATA UNIVERSITY   (Japan)

^e NAGAHAMA INSTITUTE OF BIO SCIENCE AND TECHNOLOGY   (Japan)

^f NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CULTIVATION; DISSOCIATION; METABOLISM; PHYSIOLOGY; PROTEINS; SUGAR (SUCROSE);

ARABIDOPSIS THALIANA; ATP BINDING CASSETTE TRANSPORTERS; ENVIRONMENTAL STIMULI; LIPID METABOLISMS; MEMBRANE INTERACTIONS; MOLECULAR MECHANISM; PHYSICAL INTERACTIONS; TRIACYLGLYCEROL LIPASE;

CYTOLOGY;

ABC TRANSPORTER; SUCROSE; TRIACYLGLYCEROL LIPASE; ARABIDOPSIS PROTEIN; CARBOXYLESTERASE; FAT DROPLET; PED3 PROTEIN, ARABIDOPSIS; SDP1 PROTEIN, ARABIDOPSIS;

ACTIN FILAMENT; ALLELE; ARABIDOPSIS THALIANA; ARTICLE; CARBOHYDRATE SYNTHESIS; CELL INTERACTION; CONTROLLED STUDY; FATTY ACID OXIDATION; GENE IDENTIFICATION; GENE LOCATION; GENE MUTATION; GERMINATION; LIPID METABOLISM; LIPID STORAGE; LIPOLYSIS; NONHUMAN; PED1 GENE; PEROXISOME; PLANT GENE; PLANT STRUCTURES; PRIORITY JOURNAL; SDP1 GENE; SEEDLING; WILD TYPE; ARABIDOPSIS; GENETICS; METABOLISM; PHYSIOLOGY;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; ATP-BINDING CASSETTE TRANSPORTERS; CARBOXYLIC ESTER HYDROLASES; GERMINATION; LIPID DROPLETS; LIPID METABOLISM; PEROXISOMES; SUCROSE;

EID: 84987784907     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.748814     Document Type: Article

References (59)

1. Toulmay, A., and Prinz, W. A. (2011) Lipid transfer and signaling at organelle contact sites: the tip of the iceberg. Curr. Opin. Cell Biol. 23, 458-463
2. Hayashi, T., Rizzuto, R., Hajnoczky, G., and Su, T. P. (2009) MAM: more than just a housekeeper. Trends Cell Biol. 19, 81-88
3. Csordás, G., Renken, C., Várnai, P., Walter, L., Weaver, D., Buttle, K. F., Balla, T., Mannella, C. A., and Hajnóczky, G. (2006) Structural and functional features and significance of the physical linkage between ER and mitochondria. J. Cell Biol. 174, 915-921
4. Simmen, T., Aslan, J. E., Blagoveshchenskaya, A. D., Thomas, L., Wan, L., Xiang, Y., Feliciangeli, S. F., Hung, C. H., Crump, C. M., and Thomas, G. (2005) PACS-2 controls endoplasmic reticulum-mitochondria communication and Bid-mediated apoptosis. EMBO J. 24, 717-729
5. Czabany, T., Wagner, A., Zweytick, D., Lohner, K., Leitner, E., Ingolic, E., and Daum, G. (2008) Structural and biochemical properties of lipid particles from the yeast Saccharomyces cerevisiae. J. Biol. Chem. 283, 17065-17074
6. Tzen, J., Cao, Y., Laurent, P., Ratnayake, C., and Huang, A. (1993) Lipids, proteins, and structure of seed oil bodies from diverse species. Plant Physiol. 101, 267-276
7. Mansfield, S. G., and Briarty, L. G. (1992) Cotyledon cell development in Arabidopsis thaliana during reserve deposition. Can. J. Bot. 70, 151-164
8. Brown, L. A., Larson, T. R., Graham, I. A., Hawes, C., Paudyal, R., Warriner, S. L., and Baker, A. (2013) An inhibitor of oil body mobilization in Arabidopsis. New Phytol. 200, 641-649
9. Eastmond, P. J. (2007) MONODEHYROASCORBATE REDUCTASE4 is required for seed storage oil hydrolysis and postgerminative growth in Arabidopsis. Plant Cell 19, 1376-1387
10. Lehner, A., Corbineau, F., and Bailly, C. (2006) Changes in lipid status and glass properties in cotyledons of developing sunflower seeds. Plant Cell Physiol. 47, 818-828
11. 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
12. Krahmer, N., Hilger, M., Kory, N., Wilfling, F., Stoehr, G., Mann, M., Farese, R. V., Jr, and Walther, T. C. (2013) Protein correlation profiles identify lipid droplet proteins with high confidence. Mol. Cell Proteomics 12, 1115-1126
13. Gidda, S. K., Watt, S., Collins-Silva, J., Kilaru, A., Arondel, V., Yurchenko, O., Horn, P. J., James, C. N., Shintani, D., Ohlrogge, J. B., Chapman, K. D., Mullen, R. T., and Dyer, J. M. (2013) Lipid droplet-associated proteins (LDAPs) are involved in the compartmentalization of lipophilic compounds in plant cells. Plant Signal Behav. 8, e27141
14. Tzen, J. T. C. (2012) Integral proteins in plant oil bodies. ISRN Botany 2012, 1-16
15. 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
16. 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 oil bodies in Arabidopsis. Plant Cell 18, 1961-1974
17. Ayre, B. G., Keller, F., and Turgeon, R. (2003) Symplastic continuity between companion cells and the translocation stream: long-distance transport is controlled by retention and retrieval mechanisms in the phloem. Plant Physiol. 131, 1518-1528
18. 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
19. Hayashi, M., Nito, K., Takei-Hoshi, R., Yagi, M., Kondo, M., Suenaga, A., Yamaya, T., and Nishimura, M. (2002) Ped3p is a peroxisomal ATP-binding cassette transporter that might supply substrates for fatty acid α-oxidation. Plant Cell Physiol. 43, 1-11
20. Zolman, B. K., Silva, I. D., and Bartel, B. (2001) The Arabidopsis pxa1 mutant is defective in an ATP-Binding cassette transporter-like protein required for peroxisomal fatty acid α-oxidation. Plant Physiol. 127, 1266-1278
21. Footitt, S., Slocombe, S. P., Larner, V., Kurup, S., Wu, Y., Larson, T., Graham, I., Baker, A., and Holdsworth, M. (2002) Control of germination and lipid mobilization by COMATOSE, the Arabidopsis homologue of human ALDP. EMBO J. 21, 2912-2922
22. Fulda, M., Shockey, J., Werber, M., Wolter, F. P., and Heinz, E. (2002) Two long-chain acyl-CoA synthetases from Arabidopsis thaliana involved in peroxisomal fatty acid α-oxidation. Plant J. 32, 93-103
23. Hayashi, H., De Bellis, L., Hayashi, Y., Nito, K., Kato, A., Hayashi, M., Hara-Nishimura, I., and Nishimura, M. (2002) Molecular characterization of an Arabidopsis acyl-coenzyme a synthetase localized on glyoxysomal membranes. Plant Physiol. 130, 2019-2026
24. Hayashi, M., Toriyama, K., Kondo, M., and Nishimura, M. (1998) 2,4-Dichlorophenoxybutyric acid-resistant mutants of Arabidopsis have defects in glyoxysomal fatty acid α-oxidation. Plant Cell 10, 183-195
25. Kato, A., Hayashi, M., Takeuchi, Y., and Nishimura, M. (1996) cDNA cloning and expression of a gene for 3-ketoacyl-CoA thiolase in pumpkin cotyledons. Plant Mol. Biol. 31, 843- 852
26. Germain, V., Rylott, E. L., Larson, T. R., Sherson, S. M., Bechtold, N., Carde, J. P., Bryce, J. H., Graham, I. A., and Smith, S. M. (2001) Requirement for 3-ketoacyl-CoA thiolase-2 in peroxisome development, fatty acid α-oxidation and breakdown of triacylglycerol in lipid bodies of Arabidopsis seedlings. Plant J. 28, 1-12
27. Peng, C. C., Lin, I. P., Lin, C. K., and Tzen, J. T. (2003) Size and stability of reconstituted sesame oil bodies. Biotechnol. Prog. 19, 1623-1626
28. Mano, S., Nakamori, C., Hayashi, M., Kato, A., Kondo, M., and Nishimura, M. (2002) Distribution and characterization of peroxisomes in Arabidopsis by visualization with GFP: dynamic morphology and actin-dependent movement. Plant Cell Physiol. 43, 331-341
29. Jedd, G., and Chua, N. H. (2002) Visualization of peroxisomes in living plant cells reveals acto-myosin-dependent cytoplasmic streaming and peroxisome budding. Plant Cell Physiol. 43, 384-392
30. Rapp, S., Saffrich, R., Anton, M., Jäkle, U., Ansorge, W., Gorgas, K., and Just, W. W. (1996) Microtubule-based peroxisome movement. J. Cell Sci. 109, 837-849
31. Binns, D., Januszewski, T., Chen, Y., Hill, J., Markin, V. S., Zhao, Y., Gilpin, C., Chapman, K. D., Anderson, R. G., and Goodman, J. M. (2006) An intimate collaboration between peroxisomes and lipid bodies. J. Cell Biol. 173, 719-731
32. Schrader, M. (2001) Tubulo-reticular clusters of peroxisomes in living COS-7 cells: dynamic behavior and association with lipid droplets. J. Histochem. Cytochem. 49, 1421-1429
33. 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
34. Shimada, T. L., Takano, Y., Shimada, T., Fujiwara, M., Fukao, Y., Mori, M., Okazaki, Y., Saito, K., Sasaki, R., Aoki, K., and Hara-Nishimura, I. (2014) Leaf oil body functions as a subcellular factory for the production of a phytoalexin in Arabidopsis. Plant Physiol. 164, 105-118
35. 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
36. Hayashi, M., Nanba, C., Saito, M., Kondo, M., Takeda, A., Watanabe, Y., and Nishimura, M. (2012) Loss of XRN4 function can trigger cosuppression in a sequence-dependent manner. Plant Cell Physiol. 53, 1310-1321
37. Athenstaedt, K., and Daum, G. (2003) YMR313c/TGL3 encodes a novel triacylglycerol lipase located in lipid particles of Saccharomyces cerevisiae. J. Biol. Chem. 278, 23317-23323
38. Nuttall, J. M., Motley, A., and Hettema, E. H. (2011) Peroxisome biogenesis: recent advances. Curr. Opin. Cell Biol. 23, 421-426
39. Mosser, J., Douar, A. M., Sarde, C. O., Kioschis, P., Feil, R., Moser, H., Poustka, A. M., Mandel, J. L., and Aubourg, P. (1993) Putative X-linked adrenoleukodystrophy gene shares unexpected homology with ABC transporters. Nature 361, 726-730
40. Hayashi, M., Nito, K., Toriyama-Kato, K., Kondo, M., Yamaya, T., and Nishimura, M. (2000) AtPex14p maintains peroxisomal functions by determining protein targeting to three kinds of plant peroxisomes. EMBO J. 19, 5701-5710
41. Knoblach, B., Sun, X., Coquelle, N., Fagarasanu, A., Poirier, R. L., and Rachubinski, R. A. (2013) An ER-peroxisome tether exerts peroxisome population control in yeast. EMBO J. 32, 2439-2453
42. Oikawa, K., Matsunaga, S., Mano, S., Kondo, M., Yamada, K., Hayashi, M., Kagawa, T., Kadota, A., Sakamoto, W., Higashi, S., Watanabe, M., Mitsui, T., Shigemasa, A., Iino, T., Hosokawa, Y., and Nishimura, M. (2015) Physical interaction between peroxisomes and chloroplasts elucidated by in situ laser analysis. Nature Plants 1, 15035
43. Mullen, R. T., Lisenbee, C. S., Flynn, C. R., and Trelease, R. N. (2001) Stable and transient expression of chimeric peroxisomal membrane proteins induces an independent "zippering" of peroxisomes and an endoplasmic reticulum subdomain. Planta 213, 849- 863
44. Lisenbee, C. S., Karnik, S. K., and Trelease, R. N. (2003) Overexpression and mislocalization of a tail-anchored GFP redefines the identity of peroxisomal ER. Traffic 4, 491-501
45. Reumann, S. (2004) Specification of the peroxisome targeting signals type 1 and type 2 of plant peroxisomes by bioinformatics analyses. Plant Physiol. 135, 783-800
46. Mano, S., Nakamori, C., Nito, K., Kondo, M., and Nishimura, M. (2006) The Arabidopsis pex12 and pex13 mutants are defective in both PTS1-and PTS2-dependent protein transport to peroxisomes. Plant J. 47, 604-618
47. Hernández, M. L., Whitehead, L., He, Z., Gazda, V., Gilday, A., Kozhevnikova, E., Vaistij, F. E., Larson, T. R., and Graham, I. A. (2012) A cytosolic acyltransferase contributes to triacylglycerol synthesis in sucrose-rescued Arabidopsis seed oil catabolism mutants. Plant Physiol. 160, 215-225
48. Thomas, B. R., and Rodriguez, R. L. (1994) Metabolite signals regulate gene expression and source/sink relations in cereal seedlings. Plant Physiol. 106, 1235-1239
49. To, J. P., Reiter, W. D., and Gibson, S. I. (2002) Mobilization of seed storage lipid by Arabidopsis seedlings is retarded in the presence of exogenous sugars. BMC Plant Biol. 2, 4
50. Rognoni, S., Teng, S., Arru, L., Smeekens, S. C. M., and Perata, P. (2007) Sugar effects on early seedling development in Arabidopsis. Plant Growth Regul. 52, 217-228
51. Rylott, E. L., Hooks, M. A., and Graham, I. A. (2001) Co-ordinate regulation of genes involved in storage lipid mobilization in Arabidopsis thaliana. Biochem. Soc. Trans. 29, 283-287
52. Zhou, L., Jang, J. C., Jones, T. L., and Sheen, J. (1998) Glucose and ethylene signal transduction crosstalk revealed by an Arabidopsis glucose-insensitive mutant. Proc. Natl. Acad. Sci. U.S.A. 95, 10294-10299
53. Gibson, S. I., Laby, R. J., and Kim, D. (2001) The sugar-insensitive1 (sis1) mutant of Arabidopsis is allelic to ctr1. Biochem. Biophys. Res. Commun. 280, 196-203
54. Nishimura, M., Yamaguchi, J., Mori, H., Akazawa, T., and Yokota, S. (1986) Immunocytochemical analysis shows that glyoxysomes are directly transformed to leaf peroxisomes during greening of pumpkin cotyledons. Plant Physiol. 81, 313-316
55. Fan, J., Yan, C., Roston, R., Shanklin, J., and Xu, C. (2014) Arabidopsis lipins, PDAT1 acyltransferase, and SDP1 triacylglycerol lipase synergistically direct fatty acids toward α-oxidation, thereby maintaining membrane lipid homeostasis. Plant Cell 26, 4119- 4134
56. Bechtold, N., Ellis, J., and Pelletier, G. (1993) In planta Agrobacteriummediated gene transfer by infiltration of adult Arabidopsis thaliana plants. C. R. Acad. Sci. Paris, Life Sciences 316, 1194-1199
57. Cui, S., Fukao, Y., Mano, S., Yamada, K., Hayashi, M., and Nishimura, M. (2013) Proteomic analysis reveals that the Rab GTPase RabE1c is involved in the degradation of the peroxisomal protein receptor PEX7 (peroxin 7). J. Biol. Chem. 288, 6014-6023
58. Mitsuhashi, N., Shimada, T., Mano, S., Nishimura, M., and Hara-Nishimura, I. (2000) Characterization of organelles in the vacuolar-sorting pathway by visualization with GFP in tobacco BY-2 cells. Plant Cell Physiol. 41, 993-1001
59. Yamaguchi, K., Mori, H., and Nishimura, M. (1995) A novel isoenzyme of ascorbate peroxidase localized on glyoxysomal and leaf peroxisomal membranes in pumpkin. Plant Cell Physiol. 36, 1157-1162