雨生红球藻虾青素合成研究进展
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摘要
虾青素是一种重要的次级类胡萝卜素,具有高活性的抗氧化功能,广泛应用于食品保健、医药、水产养殖等领域。雨生红球藻是一种在胁迫条件下能够大量积累虾青素的微藻。文中回顾了雨生红球藻虾青素的生物合成研究的进展,包括虾青素生物合成的诱导与调控、虾青素合成与光合作用及脂类代谢的关系等研究现状。
Astaxanthin is widely applied as a nutraceutical, pharmaceutical, and aquaculture feed additive because of its high antioxidant activity. Haematococcus pluvialis is a microalgal species that can largely accumulate astaxanthin under adverse environmental conditions. Here we review the research progress of astaxanthin biosynthesis in H. pluvialis, including the induction and regulation of massive astaxanthin, the relationship between astaxanthin synthesis, photosynthesis and lipid metabolism.
Astaxanthin is widely applied as a nutraceutical, pharmaceutical, and aquaculture feed additive because of its high antioxidant activity. Haematococcus pluvialis is a microalgal species that can largely accumulate astaxanthin under adverse environmental conditions. Here we review the research progress of astaxanthin biosynthesis in H. pluvialis, including the induction and regulation of massive astaxanthin, the relationship between astaxanthin synthesis, photosynthesis and lipid metabolism.
引文
[1]Ambati RR,Phang SM,Ravi S,et al.Astaxanthin:sources,extraction,stability,biological activities and its commercial applications-a review.Mar Drugs,2014,12(1):128-152.
[2]Higuera-Ciapara I,Felix-Valenzuela L,Goycoolea FM.Astaxanthin:a review of its chemistry and applications.Crit Rev Food Sci Nutr,2006,46(2):185-196.
[3]Otani H.Site-specific antioxidative therapy for prevention of atherosclerosis and cardiovascular disease.Oxid Med Cell Longev,2013,2013:796891.
[4]Solovchenko AE.Recent breakthroughs in the biology of astaxanthin accumulation by microalgal cell.Photosynth Res,2015,125(3):437-449.
[5]Yuan JP,Peng J,Yin K,et al.Potential health-promoting effects of astaxanthin:a high-value carotenoid mostly from microalgae.Mol Nutr Food Res,2011,55(1):150-165.
[6]Davinelli S,Nielsen ME,Scapagnini G.Astaxanthin in skin health,repair,and disease:a comprehensive review.Nutrients,2018,10(4):522.
[7]Shah MM,Liang YM,Cheng JJ,et al.Astaxanthin-producing green microalga Haematococcus pluvialis:from single cell to high value commercial products.Front Plant Sci,2016,7:531.
[8]Harker M,Tsavalos AJ,Young AJ.Factors responsible for astaxanthin formation in the Chlorophyte Haematococcus pluvialis.Bioresour Technol,1996,55(3):207-214.
[9]Orosa M,Valero JF,Herrero C,et al.Comparison of the accumulation of astaxanthin in Haematococcus pluvialis and other green microalgae under N-starvation and high light conditions.Biotechnol Lett,2001,23(13):1079-1085.
[10]Domínguez-Bocanegra AR,Legarreta IG,Jeronimo FM,et al.Influence of environmental and nutritional factors in the production of astaxanthin from Haematococcus pluvialis.Bioresour Technol,2004,92(2):209-214.
[11]Grünewald K,Hagen C.β-carotene is the intermediate exported from the chloroplast during accumulation of secondary carotenoids in Haematococcus pluvialis.J Appl Phycol,2001,13(1):89-93.
[12]Sun ZR,Cunningham FX Jr,Gantt E.Differential expression of two isopentenyl pyrophosphate isomerases and enhanced carotenoid accumulation in a unicellular chlorophyte.Proc Natl Acad Sci USA,1998,95(19):11482-11488.
[13]Gwak Y,Hwang YS,Wang BB,et al.Comparative analyses of lipidomes and transcriptomes reveal a concerted action of multiple defensive systems against photooxidative stress in Haematococcus pluvialis.J Exp Bot,2014,65(15):4317-4334.
[14]Britton G.Biosynthesis of carotenoids//Young AJ,Britton G,Eds.Dordrecht:Springer,1993:133-182.
[15]Cunningham FX,Gantt E.Genes and enzymes of carotenoid biosynthesis in plants.Annu Rev Plant Physiol Plant Mol Biol,1998,49(1):557-583.
[16]Steinbrenner J,Linden H.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,2001,125(2):810-817.
[17]Vidhyavathi R,Venkatachalam L,Sarada R,et al.Regulation of carotenoid biosynthetic genes expression and carotenoid accumulation in the green alga Haematococcus pluvialis under nutrient stress conditions.J Exp Bot,2008,59(6):1409-1418.
[18]Li YT,Sommerfeld M,Chen F,et al.Effect of photon flux densities on regulation of carotenogenesis and cell viability of Haematococcus pluvialis(Chlorophyceae).J Appl Phycol,2010,22(3):253-263.
[19]Chamovitz D,Sandmann G,Hirschberg J.Molecular and biochemical characterization of herbicide-resistant mutants of cyanobacteria reveals that phytoene desaturation is a rate-limiting step in carotenoid biosynthesis.J Biol Chem,1993,268(23):17348-17353.
[20]Collins AM,Jones HD,Han DX,et al.Carotenoid distribution in living cells of Haematococcus pluvialis(Chlorophyceae).PLoS ONE,2011,6(9):e24302.
[21]Kajiwara S,Kakizono T,Saito T,et al.Isolation and functional identification of a novel cDNA for astaxanthin biosynthesis from Haematococcus pluvialis,and astaxanthin synthesis in Escherichia coli.Plant Mol Biol,1995,29(2):343-352.
[22]Lotan T,Hirschberg J.Cloning and expression in Escherichia coli of the gene encodingβ-C-4-oxygenase,that convertsβ-carotene to the ketocarotenoid canthaxanthin in Haematococcus pluvialis.FEBS Lett,1995,364(2):125-128.
[23]Misawa N,Satomi Y,Kondo K,et al.Structure and functional analysis of a marine bacterial carotenoid biosynthesis gene cluster and astaxanthin biosynthetic pathway proposed at the gene level.JBacteriol,1995,177(22):6575-6584.
[24]Lemoine Y,Schoefs B.Secondary ketocarotenoid astaxanthin biosynthesis in algae:a multifunctional response to stress.Photosynth Res,2010,106(1/2):155-177.
[25]Grünewald K,Hirschberg J,Hagen C.Ketocarotenoid biosynthesis outside of plastids in the unicellular green alga Haematococcus pluvialis.JBiol Chem,2001,276(8):6023-6029.
[26]Chen GQ,Wang BB,Han DX,et al.Molecular mechanisms of the coordination between astaxanthin and fatty acid biosynthesis in Haematococcus pluvialis(Chlorophyceae).Plant J,2015,81(1):95-107.
[27]Leu S,Boussiba S.Advances in the production of high-value products by microalgae.Ind Biotechnol,2014,10(3):169-183.
[28]Sarada R,Tripathi U,Ravishankar GA.Influence of stress on astaxanthin production in Haematococcus pluvialis grown under different culture conditions.Proc Biochem,2002,37(6):623-627.
[29]Pelah D,Marton I,Wang W,et al.Accumulation and protection activity of protease-resistant heat-stable proteins in Haematococcus pluvialis during high light and nitrogen starvation.J Appl Phycol,2004,16(2):153-156.
[30]Giannelli L,Yamada H,Katsuda T,et al.Effects of temperature on the astaxanthin productivity and light harvesting characteristics of the green alga Haematococcus pluvialis.J Biosci Bioeng,2015,119(3):345-350.
[31]Li YT,Sommerfeld M,Chen F,et al.Consumption of oxygen by astaxanthin biosynthesis:a protective mechanism against oxidative stress in Haematococcus pluvialis(Chlorophyceae).J Plant Physiol,2008,165(17):1783-1797.
[32]Lin YJ,Chang JJ,Lin HY,et al.Metabolic engineering a yeast to produce astaxanthin.Bioresour Technol,2017,245:899-905.
[33]Hu ZY,Li YT,Sommerfeld M,et al.Enhanced protection against oxidative stress in an astaxanthin-overproduction Haematococcus mutant(Chlorophyceae).Eur J Phycol,2008,43(4):365-376.
[34]Meng CX,Teng CY,Jiang P,et al.Cloning and characterization of beta-carotene ketolase gene promoter in Haematococcus pluvialis.Acta Biochim Biophys Sin,2005,37(4):270-275.
[35]Kobayashi M,Kakizono T,Nagai S.Enhanced carotenoid biosynthesis by oxidative stress in acetate-induced cyst cells of a green unicellular alga,Haematococcus pluvialis.Appl Environ Microbiol,1993,59(3):867-873.
[36]Jeon YC,Cho CW,Yun YS.Combined effects of light intensity and acetate concentration on the growth of unicellular microalga Haematococcus pluvialis.Enzyme Microb Technol,2006,39(3):490-495.
[37]Hong ME,Choi YY,Sim SJ.Effect of red cyst cell inoculation and iron(II)supplementation on autotrophic astaxanthin production by Haematococcus pluvialis under outdoor summer conditions.J Biotechnol,2016,218:25-33.
[38]He BX,Hou LL,Dong MM,et al.Transcriptome analysis in Haematococcus pluvialis:astaxanthin induction by high light with acetate and Fe2+.Int JMol Sci,2018,19(1):E175.
[39]Yong YYR,Lee YK.Do carotenoids play a photoprotective role in the cytoplasm of Haematococcus lacustris(Chlorophyta)?Phycologia,1991,30(3):257-261.
[40]Kobayashi M,Kakizono T,Nishio N,et al.Antioxidant role of astaxanthin in the green alga Haematococcus pluvialis.Appl Microbiol Biotechnol,1997,48(3):351-356.
[41]Steinbrenner J,Linden H.Light induction of carotenoid biosynthesis genes in the green alga Haematococcus pluvialis:regulation by photosynthetic redox control.Plant Mol Biol,2003,52(2):343-356.
[42]Wang BB,Zhang Z,Hu Q,et al.Cellular capacities for high-light acclimation and changing lipid profiles across life cycle stages of the green alga Haematococcus pluvialis.PLoS ONE,2014,9(9):e106679.
[43]Mascia F,Girolomoni L,Alcocer MJP,et al.Functional analysis of photosynthetic pigment binding complexes in the green alga Haematococcus pluvialis reveals distribution of astaxanthin in photosystems.Sci Rep,2017,7:16319.
[44]Scibilia L,Girolomoni L,Berteotti S,et al.Photosynthetic response to nitrogen starvation and high light in Haematococcus pluvialis.Algal Res,2015,12:170-181.
[45]Hagen C,Braune W,Birckner E,et al.Functional aspects of secondary carotenoids in Haematococcus lacustris(Girod)Rostafinski(Volvocales).I.The accumulation period as an active metabolic process.The New Phytol,1993,125(3):625-633.
[46]Kobayashi M,Kurimura Y,Kakizono T,et al.Morphological changes in the life cycle of the green alga Haematococcus pluvialis.J Fermentat Bioeng,1997,84(1):94-97.
[47]Kobayashi M,Sakamoto Y.Singlet oxygen quenching ability of astaxanthin esters from the green alga Haematococcus pluvialis.Biotechnol Lett,1999,21(4):265-269.
[48]Murphy DJ.The biogenesis and functions of lipid bodies in animals,plants and microorganisms.Prog Lipid Res,2001,40(5):325-438.
[49]Guo Y,Cordes KR,Farese RV Jr,et al.Lipid droplets at a glance.J Cell Sci,2009,122(6):749-752.
[50]Zhekisheva M,Zarka A,Khozin-Goldberg I,et al.Inhibition of astaxanthin synthesis under high irradiance does not abolish triacylglycerol accumulation in the green alga Haematococcus pluvialis(Chlorophyceae).J Phycol,2005,41(4):819-826.
[51]Damiani MC,Popovich CA,Constenla D,et al.Lipid analysis in Haematococcus pluvialis to assess its potential use as a biodiesel feedstock.Bioresour Technol,2010,101(11):3801-3807.
[52]Goncalves EC,Johnson JV,Rathinasabapathi B.Conversion of membrane lipid acyl groups to triacylglycerol and formation of lipid bodies upon nitrogen starvation in biofuel green algae Chlorella UTEX29.Planta,2013,238(5):895-906.
[53]Kim DK,Hong SJ,Bae JH,et al.Transcriptomic analysis of Haematococcus lacustris during astaxanthin accumulation under high irradiance and nutrient starvation.Biotechnol Bioproc Eng,2011,16(4):698-705.
[54]Su YX,Wang JX,Shi ML,et al.Metabolomic and network analysis of astaxanthin-producing Haematococcus pluvialis under various stress conditions.Bioresour Technol,2014,170:522-529.
[55]Lu YD,Jiang P,Liu SF,et al.Methyl jasmonate-or gibberellins A3-induced astaxanthin accumulation is associated with up-regulation of transcription ofβ-carotene ketolase genes(bkts)in microalga Haematococcus pluvialis.Bioresour Technol,2010,101(16):6468-6474.
[56]Ding W,Zhao YT,Xu JW,et al.Melatonin:Amultifunctional molecule that triggers defense responses against high light and nitrogen starvation stress in Haematococcus pluvialis.J Agric Food Chem,2018,66(29):7701-7711.
[57]Zhao YT,Yue CC,Ding W,et al.Butylated hydroxytoluene induces astaxanthin and lipid production in Haematococcus pluvialis under high-light and nitrogen-deficiency conditions.Bioresour Technol,2018,266:315-321.
[58]Li QQ,Zhang LT,Liu JG.Examination of carbohydrate and lipid metabolic changes during Haematococcus pluvialis non-motile cell germination using transcriptome analysis.J Appl Phycol,2018,doi:10.1007/s10811-018-1524-0.
[59]Recht L,T?pfer N,Batushansky A,et al.Metabolite profiling and integrative modeling reveal metabolic constraints for carbon partitioning under nitrogen starvation in the green algae Haematococcus pluvialis.J Biol Chem,2014,289(44):30387-30403.
[2]Higuera-Ciapara I,Felix-Valenzuela L,Goycoolea FM.Astaxanthin:a review of its chemistry and applications.Crit Rev Food Sci Nutr,2006,46(2):185-196.
[3]Otani H.Site-specific antioxidative therapy for prevention of atherosclerosis and cardiovascular disease.Oxid Med Cell Longev,2013,2013:796891.
[4]Solovchenko AE.Recent breakthroughs in the biology of astaxanthin accumulation by microalgal cell.Photosynth Res,2015,125(3):437-449.
[5]Yuan JP,Peng J,Yin K,et al.Potential health-promoting effects of astaxanthin:a high-value carotenoid mostly from microalgae.Mol Nutr Food Res,2011,55(1):150-165.
[6]Davinelli S,Nielsen ME,Scapagnini G.Astaxanthin in skin health,repair,and disease:a comprehensive review.Nutrients,2018,10(4):522.
[7]Shah MM,Liang YM,Cheng JJ,et al.Astaxanthin-producing green microalga Haematococcus pluvialis:from single cell to high value commercial products.Front Plant Sci,2016,7:531.
[8]Harker M,Tsavalos AJ,Young AJ.Factors responsible for astaxanthin formation in the Chlorophyte Haematococcus pluvialis.Bioresour Technol,1996,55(3):207-214.
[9]Orosa M,Valero JF,Herrero C,et al.Comparison of the accumulation of astaxanthin in Haematococcus pluvialis and other green microalgae under N-starvation and high light conditions.Biotechnol Lett,2001,23(13):1079-1085.
[10]Domínguez-Bocanegra AR,Legarreta IG,Jeronimo FM,et al.Influence of environmental and nutritional factors in the production of astaxanthin from Haematococcus pluvialis.Bioresour Technol,2004,92(2):209-214.
[11]Grünewald K,Hagen C.β-carotene is the intermediate exported from the chloroplast during accumulation of secondary carotenoids in Haematococcus pluvialis.J Appl Phycol,2001,13(1):89-93.
[12]Sun ZR,Cunningham FX Jr,Gantt E.Differential expression of two isopentenyl pyrophosphate isomerases and enhanced carotenoid accumulation in a unicellular chlorophyte.Proc Natl Acad Sci USA,1998,95(19):11482-11488.
[13]Gwak Y,Hwang YS,Wang BB,et al.Comparative analyses of lipidomes and transcriptomes reveal a concerted action of multiple defensive systems against photooxidative stress in Haematococcus pluvialis.J Exp Bot,2014,65(15):4317-4334.
[14]Britton G.Biosynthesis of carotenoids//Young AJ,Britton G,Eds.Dordrecht:Springer,1993:133-182.
[15]Cunningham FX,Gantt E.Genes and enzymes of carotenoid biosynthesis in plants.Annu Rev Plant Physiol Plant Mol Biol,1998,49(1):557-583.
[16]Steinbrenner J,Linden H.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,2001,125(2):810-817.
[17]Vidhyavathi R,Venkatachalam L,Sarada R,et al.Regulation of carotenoid biosynthetic genes expression and carotenoid accumulation in the green alga Haematococcus pluvialis under nutrient stress conditions.J Exp Bot,2008,59(6):1409-1418.
[18]Li YT,Sommerfeld M,Chen F,et al.Effect of photon flux densities on regulation of carotenogenesis and cell viability of Haematococcus pluvialis(Chlorophyceae).J Appl Phycol,2010,22(3):253-263.
[19]Chamovitz D,Sandmann G,Hirschberg J.Molecular and biochemical characterization of herbicide-resistant mutants of cyanobacteria reveals that phytoene desaturation is a rate-limiting step in carotenoid biosynthesis.J Biol Chem,1993,268(23):17348-17353.
[20]Collins AM,Jones HD,Han DX,et al.Carotenoid distribution in living cells of Haematococcus pluvialis(Chlorophyceae).PLoS ONE,2011,6(9):e24302.
[21]Kajiwara S,Kakizono T,Saito T,et al.Isolation and functional identification of a novel cDNA for astaxanthin biosynthesis from Haematococcus pluvialis,and astaxanthin synthesis in Escherichia coli.Plant Mol Biol,1995,29(2):343-352.
[22]Lotan T,Hirschberg J.Cloning and expression in Escherichia coli of the gene encodingβ-C-4-oxygenase,that convertsβ-carotene to the ketocarotenoid canthaxanthin in Haematococcus pluvialis.FEBS Lett,1995,364(2):125-128.
[23]Misawa N,Satomi Y,Kondo K,et al.Structure and functional analysis of a marine bacterial carotenoid biosynthesis gene cluster and astaxanthin biosynthetic pathway proposed at the gene level.JBacteriol,1995,177(22):6575-6584.
[24]Lemoine Y,Schoefs B.Secondary ketocarotenoid astaxanthin biosynthesis in algae:a multifunctional response to stress.Photosynth Res,2010,106(1/2):155-177.
[25]Grünewald K,Hirschberg J,Hagen C.Ketocarotenoid biosynthesis outside of plastids in the unicellular green alga Haematococcus pluvialis.JBiol Chem,2001,276(8):6023-6029.
[26]Chen GQ,Wang BB,Han DX,et al.Molecular mechanisms of the coordination between astaxanthin and fatty acid biosynthesis in Haematococcus pluvialis(Chlorophyceae).Plant J,2015,81(1):95-107.
[27]Leu S,Boussiba S.Advances in the production of high-value products by microalgae.Ind Biotechnol,2014,10(3):169-183.
[28]Sarada R,Tripathi U,Ravishankar GA.Influence of stress on astaxanthin production in Haematococcus pluvialis grown under different culture conditions.Proc Biochem,2002,37(6):623-627.
[29]Pelah D,Marton I,Wang W,et al.Accumulation and protection activity of protease-resistant heat-stable proteins in Haematococcus pluvialis during high light and nitrogen starvation.J Appl Phycol,2004,16(2):153-156.
[30]Giannelli L,Yamada H,Katsuda T,et al.Effects of temperature on the astaxanthin productivity and light harvesting characteristics of the green alga Haematococcus pluvialis.J Biosci Bioeng,2015,119(3):345-350.
[31]Li YT,Sommerfeld M,Chen F,et al.Consumption of oxygen by astaxanthin biosynthesis:a protective mechanism against oxidative stress in Haematococcus pluvialis(Chlorophyceae).J Plant Physiol,2008,165(17):1783-1797.
[32]Lin YJ,Chang JJ,Lin HY,et al.Metabolic engineering a yeast to produce astaxanthin.Bioresour Technol,2017,245:899-905.
[33]Hu ZY,Li YT,Sommerfeld M,et al.Enhanced protection against oxidative stress in an astaxanthin-overproduction Haematococcus mutant(Chlorophyceae).Eur J Phycol,2008,43(4):365-376.
[34]Meng CX,Teng CY,Jiang P,et al.Cloning and characterization of beta-carotene ketolase gene promoter in Haematococcus pluvialis.Acta Biochim Biophys Sin,2005,37(4):270-275.
[35]Kobayashi M,Kakizono T,Nagai S.Enhanced carotenoid biosynthesis by oxidative stress in acetate-induced cyst cells of a green unicellular alga,Haematococcus pluvialis.Appl Environ Microbiol,1993,59(3):867-873.
[36]Jeon YC,Cho CW,Yun YS.Combined effects of light intensity and acetate concentration on the growth of unicellular microalga Haematococcus pluvialis.Enzyme Microb Technol,2006,39(3):490-495.
[37]Hong ME,Choi YY,Sim SJ.Effect of red cyst cell inoculation and iron(II)supplementation on autotrophic astaxanthin production by Haematococcus pluvialis under outdoor summer conditions.J Biotechnol,2016,218:25-33.
[38]He BX,Hou LL,Dong MM,et al.Transcriptome analysis in Haematococcus pluvialis:astaxanthin induction by high light with acetate and Fe2+.Int JMol Sci,2018,19(1):E175.
[39]Yong YYR,Lee YK.Do carotenoids play a photoprotective role in the cytoplasm of Haematococcus lacustris(Chlorophyta)?Phycologia,1991,30(3):257-261.
[40]Kobayashi M,Kakizono T,Nishio N,et al.Antioxidant role of astaxanthin in the green alga Haematococcus pluvialis.Appl Microbiol Biotechnol,1997,48(3):351-356.
[41]Steinbrenner J,Linden H.Light induction of carotenoid biosynthesis genes in the green alga Haematococcus pluvialis:regulation by photosynthetic redox control.Plant Mol Biol,2003,52(2):343-356.
[42]Wang BB,Zhang Z,Hu Q,et al.Cellular capacities for high-light acclimation and changing lipid profiles across life cycle stages of the green alga Haematococcus pluvialis.PLoS ONE,2014,9(9):e106679.
[43]Mascia F,Girolomoni L,Alcocer MJP,et al.Functional analysis of photosynthetic pigment binding complexes in the green alga Haematococcus pluvialis reveals distribution of astaxanthin in photosystems.Sci Rep,2017,7:16319.
[44]Scibilia L,Girolomoni L,Berteotti S,et al.Photosynthetic response to nitrogen starvation and high light in Haematococcus pluvialis.Algal Res,2015,12:170-181.
[45]Hagen C,Braune W,Birckner E,et al.Functional aspects of secondary carotenoids in Haematococcus lacustris(Girod)Rostafinski(Volvocales).I.The accumulation period as an active metabolic process.The New Phytol,1993,125(3):625-633.
[46]Kobayashi M,Kurimura Y,Kakizono T,et al.Morphological changes in the life cycle of the green alga Haematococcus pluvialis.J Fermentat Bioeng,1997,84(1):94-97.
[47]Kobayashi M,Sakamoto Y.Singlet oxygen quenching ability of astaxanthin esters from the green alga Haematococcus pluvialis.Biotechnol Lett,1999,21(4):265-269.
[48]Murphy DJ.The biogenesis and functions of lipid bodies in animals,plants and microorganisms.Prog Lipid Res,2001,40(5):325-438.
[49]Guo Y,Cordes KR,Farese RV Jr,et al.Lipid droplets at a glance.J Cell Sci,2009,122(6):749-752.
[50]Zhekisheva M,Zarka A,Khozin-Goldberg I,et al.Inhibition of astaxanthin synthesis under high irradiance does not abolish triacylglycerol accumulation in the green alga Haematococcus pluvialis(Chlorophyceae).J Phycol,2005,41(4):819-826.
[51]Damiani MC,Popovich CA,Constenla D,et al.Lipid analysis in Haematococcus pluvialis to assess its potential use as a biodiesel feedstock.Bioresour Technol,2010,101(11):3801-3807.
[52]Goncalves EC,Johnson JV,Rathinasabapathi B.Conversion of membrane lipid acyl groups to triacylglycerol and formation of lipid bodies upon nitrogen starvation in biofuel green algae Chlorella UTEX29.Planta,2013,238(5):895-906.
[53]Kim DK,Hong SJ,Bae JH,et al.Transcriptomic analysis of Haematococcus lacustris during astaxanthin accumulation under high irradiance and nutrient starvation.Biotechnol Bioproc Eng,2011,16(4):698-705.
[54]Su YX,Wang JX,Shi ML,et al.Metabolomic and network analysis of astaxanthin-producing Haematococcus pluvialis under various stress conditions.Bioresour Technol,2014,170:522-529.
[55]Lu YD,Jiang P,Liu SF,et al.Methyl jasmonate-or gibberellins A3-induced astaxanthin accumulation is associated with up-regulation of transcription ofβ-carotene ketolase genes(bkts)in microalga Haematococcus pluvialis.Bioresour Technol,2010,101(16):6468-6474.
[56]Ding W,Zhao YT,Xu JW,et al.Melatonin:Amultifunctional molecule that triggers defense responses against high light and nitrogen starvation stress in Haematococcus pluvialis.J Agric Food Chem,2018,66(29):7701-7711.
[57]Zhao YT,Yue CC,Ding W,et al.Butylated hydroxytoluene induces astaxanthin and lipid production in Haematococcus pluvialis under high-light and nitrogen-deficiency conditions.Bioresour Technol,2018,266:315-321.
[58]Li QQ,Zhang LT,Liu JG.Examination of carbohydrate and lipid metabolic changes during Haematococcus pluvialis non-motile cell germination using transcriptome analysis.J Appl Phycol,2018,doi:10.1007/s10811-018-1524-0.
[59]Recht L,T?pfer N,Batushansky A,et al.Metabolite profiling and integrative modeling reveal metabolic constraints for carbon partitioning under nitrogen starvation in the green algae Haematococcus pluvialis.J Biol Chem,2014,289(44):30387-30403.