Responsibility of regulatory gene expression and repressed protein synthesis for triacylglycerol accumulation on sulfur-starvation in Chlamydomonas reinhardtii

Frontiers in Plant Science

Volumn 5, Issue SEP, 2014, Pages

  Sato, Atsushi ^a,b   Matsumura, Rie ^a   Hoshino, Naomi ^a   Tsuzuki, Mikio ^a,b   Sato, Norihiro ^a,b  

^a TOKYO UNIVERSITY OF PHARMACY AND LIFE SCIENCES   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Acyltransferases; Chlamydomonas reinhardtii; Lipid droplets; Protein synthesis; SAC1; SNRK2.2; Sulfur starvation; Triacylglycerol

Indexed keywords

EID: 84908191789     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00444     Document Type: Article

References (58)

1. Athenstaedt, K., and Daum, G. (2006). The life cycle of neutral lipids: synthesis, storage and degradation. Cell. Mol. Life Sci. 63, 1355-1369. doi: 10.1007/s00018-006-6016-8
2. Becker, E. W. (2007). Micro-algae as a source of protein. Biotechnol. Adv. 25, 207-210. doi: 10.1016/j.biotechadv.2006.11.002
3. Blaby, I. K., Glaesener, A. G., Mettler, T., Fitz-Gibbon, S. T., Gallaher, S. D., Liu, B., et al. (2013). Systems-level analysis of nitrogen starvation-induced modifications of carbon metabolism in a Chlamydomonas reinhardtiistarchless mutant. Plant Cell 25, 4305-4323. doi: 10.1105/tpc.113.117580
4. Bligh, E. G., and Dyer, W. J. (1959). A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911-917. doi: 10.1139/o59-099
5. Bölling, C., and Fiehn, O. (2005). Metabolite profiling of Chlamydomonas reinhardtii under nutrient deprivation. Plant Physiol. 139, 1995-2005. doi: 10.1104/pp.105.071589
6. Boyle, N. R., Page, M. D., Liu, B., Blaby, I. K., Casero, D., Kropat, J., et al. (2012). Three acyltransferases and nitrogen-responsive regulator are implicated in nitrogen starvation-induced triacylglycerol accumulation inChlamydomonas. J. Biol. Chem. 287, 15811-15825. doi: 10.1074/jbc.M111.334052
7. Cakmak, T., Angun, P., Demiray, Y. E., Ozkan, A. D., Elibol, Z., and Tekinay, T. (2012). Differential effects of nitrogen and sulfur deprivation on growth and biodiesel feedstock production of Chlamydomonas reinhardtii. Biotechnol. Bioeng. 109, 1947-1957. doi: 10.1002/bit.24474
8. Davies, J. P., Yildiz, F. H., and Grossman, A. (1996). Sacl, a putative regulator that is critical for survival ofChlamydomonas reinhardtii during sulfur deprivation. EMBO J. 15, 2150-2159.
9. Davies, J. P., Yildiz, F. H., and Grossman, A. R. (1999). Sac3, an Snf1-like serine/threonine kinase that positively and negatively regulates the responses of Chlamydomonas to sulfur limitation. Plant Cell 11, 1179-1190.
10. Deng, X.-D., Gu, B., Li, Y.-J., Hu, X.-W., Guo, J.-C., and Fei, X.-W. (2012). The roles of acyl-CoA: diacylglycerol acyltransferase 2 genes in the biosynthesis of triacylglycerols by the green algae Chlamydomonas reinhardtii. Mol. Plant 5, 945-947. doi: 10.1093/mp/sss040
11. Dunstan, G. A., Volkman, J. K., Barrett, S. M., and Garland, C. D. (1993). Changes in the lipid composition and maximisation of the polyunsaturated fatty acid content of three microalgae grown in mass culture. J. Appl. Phycol. 5, 71-83.
12. Durrett, T. P., Benning, C., and Ohlrogge, J. (2008). Plant triacylglycerols as feedstocks for the production of biofuels. Plant J. 54, 593-607. doi: 10.1111/j.1365-313X.2008.03492.x
13. Fan, J., Andre, C., and Xu, C. (2011). A chloroplast pathway for the de novo biosynthesis of triacylglycerol inChlamydomonas reinhardtii. FEBS Lett. 585, 1985-1991. doi: 10.1016/j.febslet.2011.05.018
14. Fan, J., Yan, C., Andre, C., Shanklin, J., Schwender, J., and Xu, C. (2012). Oil accumulation is controlled by carbon precursor supply for fatty acid synthesis in Chlamydomonas reinhardtii. Plant Cell Physiol. 53, 1380-1390. doi: 10.1093/pcp/pcs082
15. González-Ballester, D., Casero, D., Cokus, S., Pellegrini, M., Merchant, S. S., and Grossman, A. R. (2010). RNA-Seq analysis of sulfur-deprived Chlamydomonas cells reveals aspects of acclimation critical for cell survival. Plant Cell22, 2058-2084. doi: 10.1105/tpc.109.071167
16. Gorman, D. S., and Levine, R. P. (1965). Cytochrome f and plastocyanin: their sequence in the photosynthetic electron transport chain of Chlamydomonas reinhardi. Proc. Natl. Acad. Sci. U.S.A. 54, 1665-1669.
17. Grimme, L. H., and Boardman, N. K. (1972). Photochemical activities of a particle fraction P1 obtained from the green alga Chlorella fusca. Biochem. Biophys. Res. Commun. 49, 1617-1623.
18. Herrera-Valencia, V. A., Macario-González, L. A., Casais-Molina, M. L., Beltran-Aguilar, A. G., and Peraza-Echeverría, S. (2012). In silico cloning and characterization of the glycerol-3-phosphate dehydrogenase (GPDH) gene family in the green microalga Chlamydomonas reinhardtii. Curr. Microbiol. 64, 477-485. doi: 10.1007/s00284-012-0095-6
19. Hu, Q., Sommerfeld, M., Jarvis, E., Ghirardi, M., Posewitz, M., Seibert, M., et al. (2008). Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances. Plant J. 54, 621-639. doi: 10.1111/j.1365-313X.2008.03492.x
20. Hubberten, H. M., Drozd, A., Tran, B. V., Hesse, H., and Hoefgen, R. (2012). Local and systemic regulation of sulfur homeostasis in roots of Arabidopsis thaliana. Plant J. 72, 625-635. doi: 10.1111/j.1365-313X.2012.05105.x
21. Izumo, A., Fujiwara, S., Sakurai, T., Ball, S. G., Ishii, Y., Ono, H., et al. (2011). Effects of granule-bound starch synthase 1-defective mutant on the morphology and structure of pyrenoidal starch in Chlamydomonas. Plant Sci. 180, 238-245. doi: 10.1016/j.plantsci.2010.08.014
22. Khotimchenko, S. V., and Yakovleva, I. M. (2004). Effect of solar irradiance on lipids of the green alga Ulva fenestrata Postels et Ruprecht. Bot. Mar. 47, 395-401. doi: 10.1515/BOT.2004.050
23. Kohlwein, S. D., and Henry, S. A. (2011). Coordination of storage lipid synthesis and membrane biogenesis: evidence for cross-talk between triacylglycerol metabolism and phosphatidylinositol synthesis. J. Biol. Chem. 286, 1696-1708. doi: 10.1074/jbc.M110.172296
24. Li, X., Moellering, E. R., Liu, B., Johnny, C., Fedewa, M., Sears, B. B., et al. (2012). A galactoglycerolipid lipase is required for triacylglycerol accumulation and survival following nitrogen deprivation in Chlamydomonas reinhardtii. Plant Cell 24, 4670-4686. doi: 10.1105/tpc.112.105106
25. Los, D. A., Ray, M. K., and Murata, N. (1997). Differences in the control of the temperature-dependent expression of four genes for desaturases in Synechocystis sp. PCC 6803. Mol. Microbiol. 25, 1167-1175. doi: 10.1046/j.1365-2958.1997.5641912.x
26. Matthew, T., Zhou, W., Rupprecht, J., Lim, L., Thomas-Hall, S. R., Doebbe, A., et al. (2009). The metabolome ofChlamydomonas reinhardtii following induction of anaerobic H2 production by sulfur depletion. J. Biol. Chem. 284, 23415-23425. doi: 10.1074/jbc.M109.003541
27. Merchant, S. S., Kropat, J., Liu, B., Shaw, J., and Warakanont, J. (2012). TAG, You're it! Chlamydomonas as a reference organism for understanding algal triacylglycerol accumulation. Curr. Opin. Biotechnol. 23, 352-363. doi: 10.1016/j.copbio.2011.12.001
28. Merchant, S. S., Prochnik, S. E., Vallon, O., Harris, E. H., Karpowicz, S. J., Witman, G. B., et al. (2007). TheChlamydomonas genome reveals the evolution of key animal and plant functions. Science 318, 245-250. doi: 10.1126/science.1143609
29. Miller, R., Wu, G., Deshpande, R. R., Vieler, A., Gärtner, K., Li, X., et al. (2010). Changes in transcript abundance inChlamydomonas reinhardtii following nitrogen deprivation predict diversion of metabolism. Plant Physiol. 154, 1737-1752. doi: 10.1104/pp.110.165159
30. Minoda, A., Sonoike, K., Okada, K., Sato, N., and Tsuzuki, M. (2003). Decrease in the efficiency of the electron donation to tyrosine Z of photosystem II in an SQDG-deficient mutant of Chlamydomonas. FEBS Lett. 553, 109-112. doi: 10.1016/S0014-5793(03)00981-5
31. Moseley, J. L., Gonzalez-Ballester, D., Pootakham, W., Bailey, S., and Grossman, A. R. (2009). Genetic interactions between regulators of Chlamydomonas phosphorus and sulfur deprivation responses. Genetics 181, 889-905. doi: 10.1534/genetics.108.099382
32. Msanne, J., Xu, D., Konda, A. R., Casas-Mollano, J. A., Awada, T., Cahoon, E. B., et al. (2012). Metabolic and gene expression changes triggered by nitrogen deprivation in the photoautotrophically grown microalgaeChlamydomonas reinhardtii and Coccomyxa sp. C-169. Phytochemistry 75, 50-59. doi: 10.1016/j.phytochem.2011.12.007
33. Nguyen, H. M., Baudet, M., Cuine, S., Adriano, J.-M., Barthe, D., Billon, E., 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. doi: 10.1002/pmic.201100114
34. Nikiforova, V., Freitag, J., Kempa, S., Adamik, M., Hesse, H., and Hoefgen, R. (2003). Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: interlacing of biosynthetic pathways provides response specificity. Plant J. 33, 633-650. doi: 10.1046/j.1365-313X.2003.01657.x
35. Nishida, I., Tasaka, Y., Shiraishi, H., and Murata, N. (1993). The gene and the RNA for the precursor to the plastid-located glycerol-3-phosphate acyltransferase of Arabidopsis thaliana. Plant Mol. Biol. 21, 267-277. doi: 10.1007/BF00019943
36. Otsuka, H. (1961). Changes of lipid and carbohydrate contents of Chlorella cells during the sulfur starvation, as studied by the technique of synchronous culture. J. Gen. Appl. Microbiol. 7, 72-77. doi: 10.2323/jgam.7.72
37. Pootakham, W., Gonzalez-Ballester, D., and Grossman, A. R. (2010). Identification and regulation of plasma membrane sulfate transporters in Chlamydomonas. Plant Physiol. 153, 1653-1668. doi: 10.1104/pp.110.157875
38. Quettier, A. L., and Eastmond, P. J. (2009). Storage oil hydrolysis during early seedling growth. Plant Physiol. Biochem. 47, 485-490. doi: 10.1016/j.plaphy.2008.12.005
39. Rajakumari, S., Rajasekharan, R., and Daum, G. (2010). Triacylglycerol lipolysis is linked to sphingolipid and phospholipid metabolism of the yeast, Saccharomyces cerevisiae. Biochim. Biophys. Acta 1801, 1314-1322. doi: 10.1016/j.bbalip.2010.08.004
40. Ramanan, R., Kim, B. H., Cho, D. H., Ko, S. R., Oh, H. M., and Kim, H. S. (2013). Lipid droplet synthesis is limited by acetate availability in starchless mutant of Chlamydomonas reinhardtii. FEBS Lett. 587, 370-377. doi: 10.1016/j.febslet.2012.12.020
41. Ravina, C. G., Chang, C.-I., Tsakraklides, G. P., McDermott, J. P., Vega, J. M., Leustek, T., et al. (2002). The sacmutants of Chlamydomonas reinhardtii reveal transcriptional and posttranscriptional control of cysteine biosynthesis. Plant Physiol. 130, 2076-2084. doi: 10.1104/pp.012484
42. Remacle, C., Cline, S., Boutaffala, L., Gabilly, S., Larosa, V., Barbieri, M. R., et al. (2009). The ARG9 gene encodes the plastid-resident N-acetyl ornithine aminotransferase in the green alga Chlamydomonas reinhardtii. Eukaryot. Cell 8, 1460-1463. doi: 10.1128/EC.00108-09
43. Rochaix, J. D. (1995). Chlamydomonas reinhardtii as the photosynthetic yeast. Annu. Rev. Genet. 29, 209-230. doi: 10.1146/annurev.ge.29.120195.001233
44. Sato, N. (2004). Roles of the acidic lipids sulfoquinovosyl diacylglycerol and phosphatidylglycerol in photosynthesis: their specificity and evolution. J. Plant Res. 117, 495-505. doi: 10.1007/s10265-004-0183-1
45. Sato, N., Aoki, M., Maru, Y., Sonoike, K., Minoda, A., and Tsuzuki, M. (2003a). Involvement of sulfoquinovosyl diacylglycerol in the structural integrity and heat-tolerance of photosystem II. Planta 217, 245-251. doi: 10.1007/s00425-003-0992-9
46. Sato, N., Tsuzuki, M., and Kawaguchi, A. (2003b). Glycerolipid synthesis in Chlorella kessleri 11h. I. Existence of a eukaryotic pathway. Biochim. Biophys. Acta 1633, 27-34. doi: 10.1016/S1388-1981(03)00069-6
47. Sato, N., Tsuzuki, M., Matsuda, Y., Ehara, T., Osafune, T., and Kawaguchi, A. (1995). Isolation and characterization of mutants affected in lipid metabolism of Chlamydomonas reinhardtii. Eur. J. Biochem. 230, 987-993. doi: 10.1111/j.1432-1033.1995.0987g.x
48. Siaut, M., Cuiné, S., Cagnon, C., Fessler, B., Nguyen, M., Carrier, P., et al. (2011). Oil accumulation in the model green alga Chlamydomonas reinhardtii: characterization, variability between common laboratory strains and relationship with starch reserves. BMC Biotechnol. 11:7. doi: 10.1186/1472-6750-11-7
49. Sueoka, N. (1960). Mitotic replication of deoxyribonucleic acid in Chlamydomonas reinhardti. Proc. Natl. Acad. Sci. U.S.A. 46, 83-89.
50. Sugimoto, K., Midorikawa, T., Tsuzuki, M., and Sato, N. (2008). Upregulation of PG synthesis on sulfur-starvation for PSI in Chlamydomonas. Biochem. Biophys. Res. Commun. 369, 660-665. doi: 10.1016/j.bbrc.2008.02.058
51. Sugimoto, K., Sato, N., and Tsuzuki, M. (2007). Utilization of a chloroplast membrane sulfolipid as a major internal sulfur source for protein synthesis in the early phase of sulfur starvation in Chlamydomonas reinhardtii. FEBS Lett. 581, 4519-4522. doi: 10.1016/j.febslet.2007.08.035
52. Sugimoto, K., Tsuzuki, M., and Sato, N. (2010). Regulation of synthesis and degradation of a sulfolipid under sulfur-starved conditions and its physiological significance in Chlamydomonas reinhardtii. New Phytol. 185, 676-686. doi: 10.1111/j.1469-8137.2009.03115.x
53. Tabei, Y., Okada, K., and Tsuzuki, M. (2007). Sll1330 controls the expression of glycolytic genes in Synechocystissp. PCC 6803. Biochem. Biophys. Res. Commun. 355, 1045-1050. doi: 10.1016/j.bbrc.2007.02.065
54. Teramoto, H., Nakamori, A., Minagawa, J., and Ono, T. (2002). Light-intensity-dependent expression of Lhc gene family encoding light-harvesting chlorophyll-a/b proteins of photosystem II in Chlamydomonas reinhardtii. Plant Physiol. 130, 325-333. doi: 10.1104/pp.004622
55. Toepel, J., Albaum, S. P., Arvidsson, S., Goesmann, A., la Russa, M., Rogge, K., et al. (2011). Construction and evaluation of a whole genome microarray of Chlamydomonas reinhardtii. BMC Genomics 25:579. doi: 10.1186/1471-2164-12-579
56. Wykoff, D. D., Davies, J. P., Melis, A., and Grossman, A. R. (1998). The regulation of photosynthetic electron transport during nutrient deprivation in Chlamydomonas reinhardtii. Plant Physiol. 117, 129-139. doi: 10.1104/pp.117.1.129
57. Yu, B., Wakao, S., Fan, J., and Benning, C. (2004). Loss of plastidic lysophosphatidic acid acyltransferase causes embryo-lethality in Arabidopsis. Plant Cell Physiol. 45, 503-510. doi: 10.1093/pcp/pch064
58. Zhang, Z., Shrager, J., Jain, M., Chang, C.-W., Vallon, O., and Grossman, A. R. (2004). Insights into the survival ofChlamydomonas reinhardtii during sulfur starvation based on microarray analysis of gene expression. Eukaryot. Cell 3, 1331-1348. doi: 10.1128/EC.3.5.1331-1348.2004