Molecular mechanisms of the coordination between astaxanthin and fatty acid biosynthesis in Haematococcus pluvialis (Chlorophyceae)

Plant Journal

Volumn 81, Issue 1, 2015, Pages 95-107

  Chen, Guanqun ^a,d   Wang, Baobei ^a,b   Han, Danxiang ^a   Sommerfeld, Milton ^a   Lu, Yinghua ^b   Chen, Feng ^c   Hu, Qiang ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

^b XIAMEN UNIVERSITY   (China)

^c PEKING UNIVERSITY   (China)

^d UNIVERSITY OF ALBERTA   (Canada)

Author keywords

acyl CoA diacylglycerol acyltransferase; carotenoid; fatty acid biosynthesis; gene transcription; Haematococcus pluvialis; metabolic coordination; microalgae

Indexed keywords

ALGAE; BIOCHEMISTRY; BIOSYNTHESIS; CELL MEMBRANES; DISSECTION; ESTERIFICATION; ESTERS; GLYCEROL; LIPIDS; MICROORGANISMS; PLANTS (BOTANY); TRANSCRIPTION;

CAROTENOID; DIACYLGLYCEROL ACYLTRANSFERASES; FATTY ACID BIOSYNTHESIS; GENE TRANSCRIPTIONS; HAEMATOCOCCUS PLUVIALIS; METABOLIC COORDINATION; MICRO-ALGAE;

FATTY ACIDS;

CHLOROPHYCEAE; HAEMATOCOCCUS PLUVIALIS;

ALGAL PROTEIN; ASTAXANTHIN; DIACYLGLYCEROL ACYLTRANSFERASE; FATTY ACID; XANTHOPHYLL;

BIOSYNTHESIS; ENDOPLASMIC RETICULUM; ESTERIFICATION; GENETIC TRANSCRIPTION; GENETICS; GREEN ALGA; METABOLISM; MICROALGA; PHYSIOLOGY;

ALGAL PROTEINS; CHLOROPHYTA; DIACYLGLYCEROL O-ACYLTRANSFERASE; ENDOPLASMIC RETICULUM; ESTERIFICATION; FATTY ACIDS; METABOLIC NETWORKS AND PATHWAYS; MICROALGAE; TRANSCRIPTION, GENETIC; XANTHOPHYLLS;

EID: 84920149652     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12713     Document Type: Article

References (56)

1. Ariizumi, T., Kishimoto, S., Kakami, R., et al,. (2014) Identification of the carotenoid modifying gene PALE YELLOW PETAL 1 as an essential factor in xanthophyll esterification and yellow flower pigmentation in tomato (Solanum lycopersicum). Plant J. 79, 453-465.
2. Bao, X.M., Shorrosh, B.S., and, Ohlrogge, J.B., (1997) Isolation and characterization of an Arabidopsis biotin carboxylase gene and its promoter. Plant Mol. Biol. 35, 539-550.
3. Bates, P.D., Johnson, S.R., Cao, X., Li, J., Nam, J.W., Jaworski, J.G., Ohlrogge, J.B., and, Browse, J., (2014) Fatty acid synthesis is inhibited by inefficient utilization of unusual fatty acids for glycerolipid assembly. Proc. Natl Acad. Sci. USA, 111, 1204-1209.
4. Bejarano, E.R., Parra, F., Murillo, F.J., and, Cerdaolmedo, E., (1988) End-product regulation of carotenogenesis in Phycomyces. Arch. Microbiol. 150, 209-214.
5. Biester, E.M., Hellenbrand, J., and, Frentzen, M., (2012) Multifunctional acyltransferases from Tetrahymena thermophila. Lipids, 47, 371-381.
6. Boussiba, S., (2000) Carotenogenesis in the green alga Haematococcus pluvialis: cellular physiology and stress response. Physiol. Plant. 108, 111-117.
7. Burri, B.J., and, Neidlinger, T.R., (2007) DGAT1 (acyl CoA:diacylglycerol acyltransferase 1) catalyzes the formation of many types of retinyl ester in mice. FASEB J. 21, A59-A60.
8. Chapman, K.D., and, Ohlrogge, J.B., (2012) Compartmentation of triacylglycerol accumulation in plants. J. Biol. Chem. 287, 2288-2294.
9. Chen, J.E., and, Smith, A.G., (2012) A look at diacylglycerol acyltransferases (DGATs) in algae. J. Biotechnol. 162, 28-39.
10. Chen, G.Q., Jiang, Y., and, Chen, F., (2007) Fatty acid and lipid class composition of the eicosapentaenoic acid-producing microalga, Nitzschia laevis. Food Chem. 104, 1580-1585.
11. Collins, A.M., Jones, H.D.T., Han, D.X., Hu, Q., Beechem, T.E., and, Timlin, J.A., (2011) Carotenoid distribution in living cells of Haematococcus pluvialis (Chlorophyceae). PLoS ONE, 6, e24302.
12. Cunningham, F.X., and, Gantt, E., (1998) Genes and enzymes of carotenoid biosynthesis in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 557-583.
13. Fassett, R.G., and, Coombes, J.S., (2012) Astaxanthin in cardiovascular health and disease. Molecules, 17, 2030-2048.
14. Fraser, P.D., Miura, Y., and, Misawa, N., (1997) In vitro characterization of astaxanthin biosynthetic enzymes. J. Biol. Chem. 272, 6128-6135.
15. Fraser, P.D., Shimada, H., and, Misawa, N., (1998) Enzymic confirmation of reactions involved in routes to astaxanthin formation, elucidated using a direct substrate in vitro assay. Eur. J. Biochem. 252, 229-236.
16. Grunewald, K., and, Hagen, C., (2001) β-carotene is the intermediate exported from the chloroplast during accumulation of secondary carotenoids in Haematococcus pluvialis. J. Appl. Phycol. 13, 89-93.
17. Grunewald, K., Hirschberg, J., and, Hagen, C., (2001) Ketocarotenoid biosynthesis outside of plastids in the unicellular green alga Haematococcus pluvialis. J. Biol. Chem. 276, 6023-6029.
18. Guerin, M., Huntley, M.E., and, Olaizola, M., (2003) Haematococcus astaxanthin: applications for human health and nutrition. Trends Biotechnol. 21, 210-216.
19. Han, D.X., Li, Y.T., and, Hu, Q., (2013) Astaxanthin in microalgae: pathways, functions and biotechnological implications. Algae, 28, 131-147.
20. Holtin, K., Kuehnle, M., Rehbein, J., Schuler, P., Nicholson, G., and, Albert, K., (2009) Determination of astaxanthin and astaxanthin esters in the microalgae Haematococcus pluvialis by LC-(APCI)MS and characterization of predominant carotenoid isomers by NMR spectroscopy. Anal. Bioanal. Chem. 395, 1613-1622.
21. Hu, Z.Y., Li, Y.T., Sommerfeld, M., Chen, F., and, Hu, Q., (2008) Enhanced protection against oxidative stress in an astaxanthin-overproduction Haematococcus mutant (Chlorophyceae). Eur. J. Phycol. 43, 365-376.
22. Inokoshi, J., Kawamoto, K., Takagi, Y., Matsuhama, M., Omura, S., and, Tomoda, H., (2009) Expression of two human acyl-CoA:diacylglycerol acyltransferase isozymes in yeast and selectivity of microbial inhibitors toward the isozymes. J. Antibiot. (Tokyo) 62, 51-54.
23. James, E.S., and, Cronan, J.E., (2004) Expression of two Escherichia coli acetyl-CoA carboxylase subunits is autoregulated. J. Biol. Chem. 279, 2520-2527.
24. Ke, J., Wen, T.N., Nikolau, B.J., and, Wurtele, E.S., (2000) Coordinate regulation of the nuclear and plastidic genes coding for the subunits of the heteromeric acetyl-coenzyme A carboxylase. Plant Physiol. 122, 1057-1071.
25. King, A.J., Segreti, J.A., Larson, K.J., Souers, A.J., Kym, P.R., Reilly, R.M., Zhao, G., Mittelstadt, S.W., and, Cox, B.F., (2009) Diacylglycerol acyltransferase 1 inhibition lowers serum triglycerides in the Zucker fatty rat and the hyperlipidemic hamster. J. Pharmacol. Exp. Ther. 330, 526-531.
26. Lang, N.J., (1968) Electron microscopic studies of extraplastidic astaxanthin in Haematococcus. J. Phycol. 4, 12-19.
27. Lemoine, Y., and, Schoefs, B., (2010) Secondary ketocarotenoid astaxanthin biosynthesis in algae: a multifunctional response to stress. Photosynth. Res. 106, 155-177.
28. Li, Y., Sommerfeld, M., Chen, F., and, Hu, Q., (2008) Consumption of oxygen by astaxanthin biosynthesis: a protective mechanism against oxidative stress in Haematococcus pluvialis (Chlorophyceae). J. Plant Physiol. 165, 1783-1797.
29. Li, Y.T., Sommerfeld, M., Chen, F., and, Hu, Q., (2010) Effect of photon flux densities on regulation of carotenogenesis and cell viability of Haematococcus pluvialis (Chlorophyceae). J. Appl. Phycol. 22, 253-263.
30. Li, J., Zhu, D.L., Niu, J.F., Shen, S.D., and, Wang, G.C., (2011) An economic assessment of astaxanthin production by large scale cultivation of Haematococcus pluvialis. Biotechnol. Adv. 29, 568-574.
31. Li, Y., Han, D., Yoon, K., Zhu, S., Sommerfeld, M., and, Hu, Q., (2013) Molecular and cellular mechanisms for lipid synthesis and accumulation in microalgae: biotechnological implications. In Handbook of Microalgal Culture (, Richmond, A., and, Hu, Q., eds). West Sussex, UK: John Wiley & Sons, Ltd, pp. 545-565.
32. Li, J., Han, D., Wang, D., et al,. (2014) Choreography of transcriptomes and lipidomes of Nannochloropsis reveals the mechanisms of oil synthesis in microalgae. Plant Cell, 26, 1645-1665.
33. Lippold, F., vom Dorp, K., Abraham, M., et al,. (2012) Fatty acid phytyl ester synthesis in chloroplasts of Arabidopsis. Plant Cell, 24, 2001-2014.
34. Liu, Q., Siloto, R.M.P., Lehner, R., Stone, S.J., and, Weselake, R.J., (2012) Acyl-CoA:diacylglycerol acyltransferase: molecular biology, biochemistry and biotechnology. Prog. Lipid Res. 51, 350-377.
35. Liu, G., Chater, K.F., Chandra, G., Niu, G., and, Tan, H., (2013) Molecular regulation of antibiotic biosynthesis in Streptomyces. Microbiol. Mol. Biol. Rev. 77, 112-143.
36. Lord, J.M., (1987) Isolation of endoplasmic reticulum: general principles, enzymatic markers, and endoplasmic reticulum-bound polysomes. Methods Enzymol. 148, 576-584.
37. Mendoza, H., Martel, A., del Rio, M.J., and, Reina, G.G., (1999) Oleic acid is the main fatty acid related with carotenogenesis in Dunaliella salina. J. Appl. Phycol. 11, 15-19.
38. Murphy, D.J., (2001) The biogenesis and functions of lipid bodies in animals, plants and microorganisms. Prog. Lipid Res. 40, 325-438.
39. Saha, S.K., McHugh, E., Hayes, J., Moane, S., Walsh, D., and, Murray, P., (2013) Effect of various stress-regulatory factors on biomass and lipid production in microalga Haematococcus pluvialis. Bioresour. Technol. 128, 118-124.
40. Santos, M.F., and, Mesquita, J.F., (1984) Ultrastructural study of Haematococcus lacustris (Girod) Rostafinski (Volvocales). 1. Some aspects of carotenogenesis. Cytologia (Tokyo), 49, 215-228.
41. Schoefs, B., Rmiki, N.E., Rachadi, J., and, Lemoine, Y., (2001) Astaxanthin accumulation in Haematococcus requires a cytochrome P450 hydroxylase and an active synthesis of fatty acids. FEBS Lett. 500, 125-128.
42. Schroeder, W.A., and, Johnson, E.A., (1995) Singlet oxygen and peroxyl radicals regulate carotenoid biosynthesis in Phaffia rhodozyma. J. Biol. Chem. 270, 18374-18379.
43. Shih, M.Y.S., Kane, M.A., Zhou, P., Yen, C.L.E., Streeper, R.S., Napoli, J.L., and, Farese, R.V., (2009) Retinol esterification by DGAT1 is essential for retinoid homeostasis in murine skin. J. Biol. Chem. 284, 4292-4299.
44. Shintani, D.K., and, Ohlrogge, J.B., (1995) Feedback inhibition of fatty acid synthesis in tobacco suspension cells. Plant J. 7, 577-587.
45. Steinbrenner, J., and, Linden, H., (2001) Regulation of two carotenoid biosynthesis genes coding for phytoene synthase and carotenoid hydroxylase during stress-induced astaxanthin formation in the green alga Haematococcus pluvialis. Plant Physiol. 125, 810-817.
46. Steinbrenner, J., and, Linden, H., (2003) Light induction of carotenoid biosynthesis genes in the green alga Haematococcus pluvialis: regulation by photosynthetic redox control. Plant Mol. Biol. 52, 343-356.
47. Vidhyavathi, R., Venkatachalam, L., Sarada, R., and, Ravishankar, G.A., (2008) Regulation of carotenoid biosynthetic genes expression and carotenoid accumulation in the green alga Haematococcus pluvialis under nutrient stress conditions. J. Exp. Bot. 59, 1409-1418.
48. Walther, T.C., and, Farese, R.V., (2009) The life of lipid droplets. Biochim. Biophys. Acta, 1791, 459-466.
49. Wilfling, F., Wang, H.J., Haas, J.T., et al,. (2013) Triacylglycerol synthesis enzymes mediate lipid droplet growth by relocalizing from the ER to lipid droplets. Dev. Cell, 24, 384-399.
50. Yen, C.L.E., Monetti, M., Burri, B.J., and, Farese, R.V., (2005) The triacylglycerol synthesis enzyme DGAT1 also catalyzes the synthesis of diacylglycerols, waxes, and retinyl esters. J. Lipid Res. 46, 1502-1511.
51. Yen, C.L.E., Stone, S.J., Koliwad, S., Harris, C., and, Farese, R.V., (2008) DGAT enzymes and triacylglycerol biosynthesis. J. Lipid Res. 49, 2283-2301.
52. Yuan, J.P., and, Chen, F., (2000) Purification of trans-astaxanthin from a high-yielding astaxanthin ester-producing strain of the microalga Haematococcus pluvialis. Food Chem. 68, 443-448.
53. Zhang, C., Iskandarov, U., Klotz, E.T., Stevens, R.L., Cahoon, R.E., Nazarenus, T.J., Pereira, S.L., and, Cahoon, E.B., (2013) A thraustochytrid diacylglycerol acyltransferase 2 with broad substrate specificity strongly increases oleic acid content in engineered Arabidopsis thaliana seeds. J. Exp. Bot. 64, 3189-3200.
54. Zhao, G., Souers, A.J., Voorbach, M., et al,. (2008) Validation of diacyl glycerolacyltransferase I as a novel target for the treatment of obesity and dyslipidemia using a potent and selective small molecule inhibitor. J. Med. Chem. 51, 380-383.
55. Zhekisheva, M., Boussiba, S., Khozin-Goldberg, I., Zarka, A., and, Cohen, Z., (2002) Accumulation of oleic acid in Haematococcus pluvialis (Chlorophyceae) under nitrogen starvation or high light is correlated with that of astaxanthin esters. J. Phycol. 38, 325-331.
56. Zhekisheva, M., Zarka, A., Khozin-Goldberg, I., Cohen, Z., and, Boussiba, S., (2005) Inhibition of astaxanthin synthesis under high irradiance does not abolish triacylglycerol accumulation in the green alga Haematococcus pluvialis (Chlorophyceae). J. Phycol. 41, 819-826.