Skip to main content
SpringerLink
Log in

A hypothesis about the origin of carotenoid lipid droplets in the green algae Dunaliella and Haematococcus

  • Review
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

Hypercarotenogenesis in green algae evolved by mutation of PSY that increased its transcription at high light, disintegration of the eyespot in Dunaliella and acquisition of the capacity to export carotenoids from chloroplasts in Haematococcus.

Carotenoids (Car) are lipid-soluble pigments synthesized in plants, algae, bacteria and fungi. Car have strong antioxidative properties and as such are utilized to reduce the danger of different diseases in humans. Two green microalgae are utilized as rich natural sources for Car: Dunaliella salina/bardawil accumulates 10% (w/w) β-carotene (βC), which is also pro-vitamin A, and Haematococcus pluvialis accumulates 4% (w/w) astaxanthin (Ast), the strongest antioxidant among Car. D. bardawil accumulates βC in plastoglobules within the chloroplast, whereas H. pluvialis deposits Ast in cytoplasmic lipid droplets (CLD). In this review we compare the hypercarotenogenic responses (HCR) in Dunaliella and in Haematococcus and try to outline hypothetical evolutionary pathways for its origin. We propose that a mutation in phytoene synthetase that increased its transcription level in response to high light stress had a pivotal role in the evolution of the HCR. Proteomic analyses indicated that in D. bardawil/salina the HCR evolved from dissociation and amplification of eyespot lipid globules. The more robust HCR in algae that accumulate carotenoids in CLD, such as H. pluvialis, required also acquisition of the capacity to export βC out of the chloroplast and its enzymatic conversion into Ast.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

Ast:

Astaxanthin

Ast-TA:

Ast transacylase

βC:

β-carotene

βC-PG:

βC plastoglobules

BKT:

βC ketolase

Car:

Carotenoid/s

Chl:

Chlorophyll

CLD:

Cytoplasmic lipid droplets

CRTR-B:

ΒC hydroxylase

FA:

Fatty acids

HCR:

Hypercarotenogenic response

HL:

High light

ND:

Nutrient deprivation

PS-II:

Photosystem II

PSY:

Phytoene synthase

ROS:

Reactive oxygen species

TAG:

Triacylglycerol

References

  • Aflalo C, Meshulam Y, Zarka A, Boussiba S (2007) On the relative efficiency of two- vs. one-stage production of astaxanthin by the green alga Haematococcus pluvialis. Biotechnol Bioeng 98:300–3005

    Article  CAS  PubMed  Google Scholar 

  • Ambati RR, Gogisetty D, Gokare RA, Ravi S, Bikkina PN, Su Y, Lei B (2018) Botryococcus as an alternative source of carotenoids and its possible applications—an overview. Crit Rev Biotechnol 38:541–558

    Article  CAS  PubMed  Google Scholar 

  • Arad S, Cohen E, Ben-Amotz A (1993) Accumulation of canthaxanthin in Chlorella emersonii. Physiol Plant 87:232–236

    Article  CAS  Google Scholar 

  • Avidan O, Brandis A, Rogachev I, Pick U (2015) Enhanced acetyl-CoA production is associated with increased triglyceride accumulation in the green alga Chlorella desiccata. J Exp Bot 66:3725–3735

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ben Amotz A, Avron M (1983) On the factors which determine massive β-carotene accumulation in the halotolerant alga Dunaliella bardawil. Plant Physiol 72:593–597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ben Amotz A, Avron M (1989) The wavelength dependence of massive carotene synthesis in Dunaliella bardawil (Chlorophyceae). J Phycol 25:175–178

    Article  CAS  Google Scholar 

  • Ben Amotz A, Katz A, Avron M (1982) Accumulation of β-carotene in halotolerant algae: purification and characterization of β-carotene-rich globules from Dunaliella bardawil (Chloropyceae). J Phycol 18:529–537

    Article  CAS  Google Scholar 

  • Ben-Amotz Lers A, Avron M (1988) Stereoisomers of β-carotene in the alga Dunaliella bardawil. Plant Physiol 86:1286–1291

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ben-Amotz A, Shaish A, Avron M (1989) Mode of action of massively accumulated beta-carotene in Dunaliella bardawil in protecting the alga against damage by excess irradiation. Plant Physiol 91:1040–1043

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bohne F, Linden H (2002) Regulation of carotenoid biosynthesis in response to light in Chlamydomonas reinhardtii. Biochim Biophys Acta 1579:26–34

    Article  CAS  PubMed  Google Scholar 

  • Bone RA, Landrum JT (2003) Lutein and zeaxanthin dietary supplements raise macular pigment density and serum concentration of these carotenoids in humans. J Nutr 133:992–998

    Article  CAS  PubMed  Google Scholar 

  • Borowitzka MA (2013) High-value products from microalgae—their development and commercialization. J Appl Phycol 25(3):743–756

    Article  CAS  Google Scholar 

  • Borowitzka MA, Huisman JM (1993) The ecology of Dunaliella salina (Chlorophyceae, Volvocales): effect of environmental conditions on aplanospore formation. Bot Marina 36:233–244

    Article  Google Scholar 

  • Botella JA, Murillo FJ, Ruiz-Vázquez R (1995) A cluster of structural and regulatory genes for light-induced carotenogenesis in Mixococcus xanthus. Eur J Biochem 233:238–248

    Article  CAS  PubMed  Google Scholar 

  • Boussiba S (2000) Carotenogenesis in the green alga Haematococcus pluvialis: cellular physiology and stress response. Physiol Plant 108:111–117

    Article  CAS  Google Scholar 

  • Boyd JS, Mittelmeier TM, Dieckmaa CL (2011) New insights into eyespot placement and assembly in Chlamydomonas. Bio Archit 1:196–199

    Google Scholar 

  • Bréhélin C, Kessler F, van Wijk KJ (2007) Plastoglobules: versatile lipoprotein particles in plastids. Trends Plant Sci 12:1360–1385

    Article  CAS  Google Scholar 

  • Caffarri S, Tibiletti T, Jennings RC, Santabarbara S (2014) A comparison between photosystem I and photosystem II architecture and functioning. Curr Prot Peptide Sci 15:296331

    Article  CAS  Google Scholar 

  • Capelli B, Bagchi D, Cysewski GR (2013) Synthetic astaxanthin is significantly inferior to algal-based astaxanthin as an antioxidant and may not be suitable as a human nutraceutical supplement. Nutrafoods 12:145–152

    Article  CAS  Google Scholar 

  • Cazzonelli CI, Pogson BJ (2010) Source to sink: regulation of carotenoid biosynthesis in plants. Trends Plant Sci 15:266–274

    Article  CAS  PubMed  Google Scholar 

  • Chekanov K, Lukyanov A, Boussiba S, Aflalo C, Solovchenko A (2016) Modulation of photosynthetic activity and photoprotection in Haematococcus pluvialis cells during their conversion into haematocysts and back. Photosynth Res 128:313–323

    Article  CAS  PubMed  Google Scholar 

  • Chen CY, Kao AL, Tsai ZC, Shen YM, Kao PH, Nge IS, Chang JS (2017) Expression of synthetic phytoene synthase gene to enhance β-carotene production in Scenedesmus sp. CPC2. Biotechnol J. https://doi.org/10.1002/biot.201700204

    Article  PubMed  Google Scholar 

  • Couso I, Vila M, Rodriguez H, Vargas MA, León R (2011) Overexpression of an exogenous phytoene synthase gene in the unicellular alga Chlamydomonas reinhardtii leads to an increase in the content of carotenoids. Biotechnol Prog 27:54–60

    Article  CAS  PubMed  Google Scholar 

  • Craft NE, Soares JH Jr (1992) Relative solubility, stability, and absorptivity of lutein and β-carotene in organic solvents. J Agric Food Chem 40:431–434

    Article  CAS  Google Scholar 

  • Davidi L, Pick U (2012) Characterization of major lipid droplet proteins from Dunaliella. Planta 236:19–33

    Article  CAS  PubMed  Google Scholar 

  • Davidi L, Pick U (2017) Novel 9-cis/all-trans β-carotene isomerase from plastidic lipid droplets in Dunaliella bardawil catalyze the conversion of all-trans to 9-cis β-carotene. Plant Cell Rep 36:807–814

    Article  CAS  PubMed  Google Scholar 

  • Davidi L, Shimoni E, Khozin-Goldberg I, Zamir A, Pick U (2014) Origin of β-carotene-rich plastoglobuli in Dunaliella bardawil. J Physiol 164:2139–2156

    CAS  Google Scholar 

  • Davidi L, Levin Y, Ben-Dor S, Pick U (2015) Proteome analysis of cytoplasmatic and plastidic ß-carotene lipid droplets in Dunaliella bardawil. Plant Physiol 167:60–79

    Article  CAS  PubMed  Google Scholar 

  • Del Campo JA, Rodrìguez H, Moreno J, Vargas MA, Rivas J, Guerrero MG (2004) Accumulation of astaxanthin and lutein in Chlorella zogfingiensis (Chlorophyta). Appl Microbiol Biotechnol 64:848–854

    Article  CAS  PubMed  Google Scholar 

  • Demming-Adams B, Adams WA III (1996) The role of xanthophyll-cycle carotenoids in the protection of photosynthesis. Trends Plant Sci 1:21–26

    Article  Google Scholar 

  • Duanmu D, Bachy C, Sudek S, Wong CH, Jimènez V, Rockwell NC, Martin SS, Ngan CY, Reistetter EN, van Baren MJ, Price DC, Wei CL, Reyes-Prieto A, Lagarias JC, Worden AZ (2014) Marine algae and land plants share conserved phytochrome signaling systems. Proc Natl Acad Sci USA 44:15827–15832

    Article  CAS  Google Scholar 

  • Duffy CDP, Ruban AV (2015) Dissipative pathways in the photosystem-II antenna in plants. J Photochem Photobiol 152:215–226

    Article  CAS  Google Scholar 

  • Dufosse L, Galaup P, Yaron A, Arad SM, Blanc P, Murthy KNC, Ravishankar GA (2005) Microorganisms and microalgae as sources of pigments for food use: a scientific oddity or an industrial reality? Trends Food Sci Technol 16:389–406

    Article  CAS  Google Scholar 

  • During A, Harrison E (2007) Mechanism of provitamin A (carotenoid) and vitamin A (retinol) transport into and out of intestinal Caco-2 cells. J Lipid Res 48:2283–2294

    Article  CAS  PubMed  Google Scholar 

  • El-Sayed AB (2010) Carotenoids accumulation in the green alga Scenedesmus sp. incubated with industrial citrate waste and different incubation stresses. Nat Sci 8:34–40

    Google Scholar 

  • Fan L, Vonshak A, Gabbay R, Hirshberg J, Cohen Z, Boussiba S (1995) The biosynthesis pathway of astaxanthin in a green algae Haematococcus pluvialis as indicated by inhibition with diphenylamine. Plant Cell Physiol 36:1519–1524

    CAS  Google Scholar 

  • Fu X, Feng C, Wang C, Yin X, Lu P, Grierson D, Cu C, Chen K (2014) Involvement of multiple phytoene synthase genes in tissue- and cultivar-specific accumulation of carotenoids. J Exp Bot 65:4679–4689

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galasso C, Corinaldesi C, Sansone C (2017) Carotenoids from marine organisms: biological functions and industrial applications. Antioxidants 6:96. https://doi.org/10.3390/antiox6040096

    Article  CAS  PubMed Central  Google Scholar 

  • García-González M, Moreno J, Manzano JC, Florencio FJ, Guerrero MG (2005) Production of Dunaliella salina biomass rich in 9-cis -carotene and lutein in a closed tubular photobioreactor. J Biotechnol 115:81–90

    Article  CAS  PubMed  Google Scholar 

  • Garone M, Howard J, Fabricant J (2015) A review of common tanning methods. J Clin Aesthet Dermatol 8:43–47

    PubMed  PubMed Central  Google Scholar 

  • Georgianna DR, Hannon MJ, Marchuschi M, Wu S, Botsch K, Lewis AJ, Hyun J, Ghetti F, Herrmann H, Häder D, Seidlitz H (1999) Spectral dependence of the inhibition of photosynthesis under stimulated global radiation in the unicellular green alga Dunaliella salina. J Photochem Photobiol B 48:166–173

    Article  Google Scholar 

  • Gong M, Bassi A (2016) Carotenoids from microalgae: a review of recent developments. Biotechnol Adv 34:1396–1412

    Article  CAS  PubMed  Google Scholar 

  • Grünewald K, 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

    Article  Google Scholar 

  • Grünewald K, Hirschberg J, Hagen C (2001) Ketocarotenoid biosynthesis outside of plastids in the unicellular green alga Haematococcus pluvialis. J Biol Chem 276:6023–6029

    Article  PubMed  Google Scholar 

  • Grung M, Metzers P, Liaaen-Jensen II (1994) Algal carotenoid 53, secondary carotenoids of alga 4, secondary carotenoids in the green alga Botryococcus braunii, race L, new strain. Biochem Syst Ecol 22:25–29

    Article  CAS  Google Scholar 

  • Gruszecki WI, Strzalka K (2005) Carotenoids as modulators of lipid membrane physical properties. Biochim Biophys Acta 1740:108–115

    Article  CAS  PubMed  Google Scholar 

  • Hagen C, Braune W, Greulich F (1993) Functional aspects of secondary carotenoids in Haematococcus lacustris [Girod] Rostafinski (Volvocales). IV. Protection from photodynamic damage. J Photochem Photobiol 20:153–160

    Article  CAS  Google Scholar 

  • Han D, Wang J, Sommerfeld M, Hu Q (2012) Susceptibility and protective mechanisms of motile and non-motile cells of Haematococcus pluvialis (Chloropyceae) to photooxidative stress. J Phycol 48:693–705

    Article  CAS  PubMed  Google Scholar 

  • Han Y, Zheng QS, Wei YP, Chen J, Liu R, Wan HJ (2015) In silico identification and analysis of phytoene synthase genes in plants. Gen Mol Res 14:9412–9422

    Article  CAS  Google Scholar 

  • Hanagata N, Dubinsky Z (1999) Secondary carotenoid accumulation in Scenedesmus komarekii (Chlorophyceae, Chlorophyta). J Phycol 35:960–966

    Article  CAS  Google Scholar 

  • Hashimoto H, Uragami C, Cogdell RC (2016) Carotenoids and photosynthesis. In: Carotenoids in nature. Subcellular Biochem, vol 74. Springer, Berlin, pp 111–139

  • Henríquez V, Escobar C, Galarza J, Gimpel J (2016) Carotenoids in microalgae. In: Carotenoids in nature. Springer, Cham, pp 219–237

  • Huang J, Zhong Y, Sandmann G, Liu J, Chen F (2012) Cloning and selection of carotenoid ketolase genes for the engineering of high-yield astaxanthin in plants. Planta 236:691–699

    Article  CAS  PubMed  Google Scholar 

  • Husssain G, Sankawa U, Goto H, Matsumoto K, Watanabe H (2006) Astaxanthin, a carotenoid with potential in human health nutrition. J Nat Prod 69:443–449

    Article  CAS  Google Scholar 

  • Jahnke LS (1999) Massive carotenoid accumulation in Dunaliella bardawil induced by ultraviolet-A irradiation. J Photochem Photobiol 48:68–74

    Article  CAS  Google Scholar 

  • Jahns P, Holzwarth AR (2012) The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochim Biophys Acta 1817:182–193

    Article  CAS  PubMed  Google Scholar 

  • Jin E, Polle JEW (2009) Carotenoid biosynthesis in Dunaliella (Chlorophyta). In: Ben-Amotz A, Polle JEW, Rao DVS (eds) The alga Dunaliella: biodiversity, physiology, genomics and biotechnology. Science Publishers, New Hampshire, pp 147–172

    Chapter  Google Scholar 

  • Katz A, Jimenez C, Pick U (1995) Isolation and characterization of a protein associated with carotene globules in the alga Dunaliella bardawil. Plant Physiol 108:1657–1664

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kobayashi M, Okada T (2000) Protective role of astaxanthin against u.v.-B irradiation in the green alga Haematococcus pluvialis. Biotechnol Lett 22:177–181

    Article  CAS  Google Scholar 

  • Kreimer G (2009) The green alga eyespot apparatus: a primordial visual system and more? Curr Genet 55:19–43

    Article  CAS  PubMed  Google Scholar 

  • Lamb MR, Dutcher SK, Worley CK, Dieckmann CL (1999) Eyespot-assembly mutants in Chlamydomonas reinhardtii. Genetics 153:721–729

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lao YM, Xiao L, Ye ZW, Jiang JG, Zhou SS (2011) In silico analysis of phytoene synthase and its promoter reveals hints for regulation mechanisms of carotenogenesis in Dunaliella bardawil. Bioinformatics 27:2201–2208

    Article  CAS  PubMed  Google Scholar 

  • Lemoine B, Schoefs B (2010) Secondary ketocarotenoid astaxanthin biosynthesis in algae: a multifunctional response to stress. Photosynth Res 106:155–177

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Zhang X (2015) Transcriptome analysis in Haematococcus pluvialis: astaxanthin induction by salicylic acid (SA) and jasmonic acid (JA). Plos One. https://doi.org/10.1371/journal.pone.0140609

    Article  PubMed  PubMed Central  Google Scholar 

  • Li F, Vallabhaneni R, Yu J, Rocheford T, Wurtzel ET (2008) The maize phytoene synthase gene family: overlapping roles of carotenogenesis in endosperm, photomorphogenesis, and thermal stress tolerance. Plant Physiol 147:1334–1346

    Article  PubMed  PubMed Central  Google Scholar 

  • Li F, Tsfadia O, Wurtzel ET (2009) The phytoene synthase gene family in grasses. Plant Signal Behav 4:208–211

    Article  PubMed  PubMed Central  Google Scholar 

  • Liang MH, Jiang JG (2017) Analysis of carotenogenic genes promoters and WRKY transcription factors in response to salt stress in Dunaliella bardawil. Sien Rep 7:37025

    CAS  Google Scholar 

  • Liang CW, Zhao FQ, Meng CX, Tan CP, Qin S (2006) Molecular cloning, characterization and evolutionary analysis of phytoene desaturase (PDS) gene from Haematococcus pluvialis. World J Microbiol Biotechnol 22:59–64

    Article  CAS  Google Scholar 

  • Liu J, Sun Z, Gerken J, Liu Z, Jiang Y, Chen F (2014) Chlorella zofingiensis as an alternative microalgae producer of astaxanthin: biology and industrial potential. Mar Drugs 12:3487–3515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • López-Emparán A, Quezada-Martinez D, Zúñiga-Bustos M, Cifuentes V, Iñiguez-Luy F, Federico L (2014) Functional analysis of the Brassica napus L. phytoene synthase (PSY) gene family. PloS One. https://doi.org/10.1371/journal.pone.0114878

    Article  PubMed  PubMed Central  Google Scholar 

  • Lundquist PK, Poliakov A, Bhuiyan NH, Zybailov B, Sun Q, van Wijk KJ (2012) The functional network of the Arabidopsis plastoglobule proteome based on quantitative proteomics and genome-wide coexpression analysis. Plant Physiol 158:1172–1192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maeda H, Hosokawa M, Sashima T, Murakami-Funayama K, Miyashita K (2009) Anti-obesity and anti-diabetic effects of fucoxanthin on diet-induced obesity conditions in a murine model. Mol Med Rep 2:897–902

    Article  CAS  PubMed  Google Scholar 

  • Manayi A, Abdollahi M, Raman T, Nabavi SF, Habtemariam S, Dagia M, Nabavi SM (2016) Lutein and cataract: from bench to bedside. Crit Rev Biotechnol 8551:1–11

    Google Scholar 

  • Mascia F, Girolomoni L, Alcocer MJP, Bargigia I, Perozeni F, Cazzaniga S, Cerullo G, D’Andrea C, Ballottari M (2017) Functional analysis of photosynthetic pigment binding complexes in the green alga Haematococcus pluvialis reveals distribution of astaxanthin in photosystems. Sci Rep 7:16319. https://doi.org/10.1038/s41598-017-16641-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Merzlyak MN, Chivkunova OB, Gorelova OA, Reshetnikova IV, Solovchenko AE, Khozin-Goldberg I, Cohen Z (2007) Effect of nitrogen starvation on optical properties, and arachidonic acid content of the unicellular green alga Parietochloris incisa. J Phycol 43:833–843

    Article  CAS  Google Scholar 

  • Mulders KJM, Weesepoel Y, Bodenes P, Lamers PP, Vincken JP, Martens DE, Gruppen H, Wijffels RH (2015) Nitrogen-depleted Chlorella zofingiensis produces astaxanthin, ketolutein and their fatty acid esters: a carotenoid metabolism study. J Appl Phycol 27:125–140

    Article  CAS  Google Scholar 

  • Muradian KH, Vaiserman A, Min KJ, Fraifeld VE (2015) Fucoxanthin and lipid metabolism: a minireview. Nut Metab Cardiovasc Dis 25:891–897

    Article  CAS  Google Scholar 

  • Nguyen HM, Baudet M, Cuiné S, Adriano J-M, Barthe D, Billon E, Bruley C, Beisson F, Peltier G, Ferro M, Li-Beisson Y (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

    Article  CAS  PubMed  Google Scholar 

  • Nisar N, Shan LL, Khin NC, Pogson BJ (2015) Carotenoid metabolism in plants. Mol Plant 8:68–82

    Article  CAS  PubMed  Google Scholar 

  • Orosa M, Valero JF, Herrero C, Abalde J (2001) Comparison of the accumulation of astaxanthin in Haematococcus pluvialis and other green microalgae under N-deprivation and high light conditions. Biotechnol Lett 23:1079–1085

    Article  CAS  Google Scholar 

  • Orset SC, Young AJ (2000) Exposure to low irradiances favors the synthesis of 9-cis, -carotene in Dunaliella salina (Teod.). Plant Physiol 122:609–617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paine JA, Shipton CA, Chaggar S et al (2005) Improving the nutritional value of golden rice through increased provitamin A content. Nat Biotechnol 23:482–487

    Article  CAS  Google Scholar 

  • Peled E, Pick U, Zarka A, Shimoni E, Leu S, Boussiba S (2012) Light-induced oil globule migration in Haematococcus pluvialis (Chloropyceae). J Phycol 48:1209–1219

    Article  PubMed  Google Scholar 

  • Pick U, Avidan O (2017) Triacylglycerol is produced from starch and polar lipids in the green alga Dunaliella tertiolecta. J Exp Bot 68:4939–4950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Plutzky L (2011) The PPAR-RXR transcriptional complex in the vasculature. Energy in the balance. Circ Res 108:1002–1016

    Article  CAS  PubMed  Google Scholar 

  • Polle JEW, Tran D, Ben-Amotz A (2009) History, distribution and habitat of algae of the genus Dunaliella Teodoresco (Chlorophyceae). In: Ben-Amotz A, Polle JEW, Rao DVS (eds) The alga Dunaliella: biodiversity, physiology, genomics and biotechnology. Science Publishers, Enfield, pp 1–14

  • Rabbani S, Beyer P, Lintig J, Hugueney P, Kleinig H (1998) Induced beta-carotene synthesis driven by triacylglycerol deposition in the unicellular alga Dunaliella bardawil. Plant Physiol 116:1239–1248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reboul E (2013) Absorption of vitamin A and carotenoids by enterocyte: focus on transport proteins. Nutrients 5:3563–3581

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Recht L, Zarka A, Boussiba S (2012) Patterns of carbohydrate and fatty acid changes under nitrogen starvation in the microalga Haematococcus pluvialis and Nannochloropsis sp. Appl Microbiol Biotechnol 94:1495–1503

    Article  CAS  PubMed  Google Scholar 

  • Recht L, Topfer N, Batushansky A, Sikron N, Zarka A, Gibon I, Nikoloski Z, Fait A, Boussiba S (2014) Metabolite profiling and integrative modeling reveal metabolic constrains for carbon partitioning under nitrogen-starvation in the green alga Haematococcus pluvialis. J Biol Chem 289:30387–30403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reinecke DL, Castillo-Flores A, Boussiba S, Zarka A (2018) Polyploid polynuclear consecutive cell-cycle enables large genome-size in Haematococcus pluvialis. Algal Res 33:456–461

    Article  Google Scholar 

  • Remias D, Lütz-Meindl U, Lütz C (2005) Photosynthesis, pigments and ultrastructure of the alpine snow alga Chlamydomonas nivalis. Eur J Phycol 40:259–268

    Article  CAS  Google Scholar 

  • Rohmer M (1999) The discovery of a mevalonate-independent pathway for isoprenoid biosynthesis in bacteria, algae and higher plants. Nat Prod Rep 16(5):565–574

    Article  CAS  PubMed  Google Scholar 

  • Roth MS, Cockus SJ, Gallaher SD, Walter A, Lopez D, Erickson E, Emdelman B, Westcott D, Larabell CA, Merchant SS, Pellegrini M, Niyogi KK (2017) Chromosome-level genome assembly and transcriptome of the green alga Chromochloris zofingiensis illuminates astaxanthin production. Proc Natl Acad Sci USA. https://doi.org/10.1073/pnas.1619928114

  • Rottet S, Besagni C, Kessler F (2015) The role of plastoglobules in thylakoid lipid remodeling during plant development. Biochim Biophys Acta 1847:889–899

    Article  CAS  PubMed  Google Scholar 

  • Sanchez-Saavedra MP, Jimenez C, Figueroa FL (1996) Far-red light inhibits growth but promotes carotenoid accumulation in the green microalga Dunaliella bardawil. Physiol Plant 98:419–423

    Article  CAS  Google Scholar 

  • Sandmann G (2002) Molecular evolution of carotenoid biosynthesis: from bacteria to plants. Physiol Plant 116:431–440

    Article  CAS  Google Scholar 

  • Schmidhauser TJ, Lauter FR, Schumacher M, Zhou W, Russo VEA, Yanofsky C (1994) Characterization of al-2, the phytoene synthase gene of Neurospora crassa. J Biol Chem 269:12060–12066

    CAS  PubMed  Google Scholar 

  • Schmidt M, Gessner G, Luff M, Heiland I, Wagner V, Kaminski M, Geimer S, Eitzinger N, Reissenweber T, Voytsekh O et al (2006) Proteomic analysis of the eyespot of Chlamydomonas reinhardtii provides novel insights into the components and tactic movement. Plant Cell 18:1908–1930

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shah MR, Liang Y, Cheng JJ, Daroch M (2016) Astaxanthin-producing green microalga Haematococcus pluvialis: from single cell to high value commercial products. Front Plant Sci. https://doi.org/10.3389/fpls.2016.00531

  • Shaish A, Avron M, Ben-Amotz A (1990) Effect of inhibitors on the formation of stereoisomers in the biosynthesis of β-carotene in Dunaliella bardawil. Plant Cell Physiol 31:689–696

    CAS  Google Scholar 

  • Shaish A, Ben-Amotz A, Avron M (1991) Production and selection of high β-carotene mutants of Dunaliella bardawil (chlorophyta). J Phycol 27:652–656

    Article  CAS  Google Scholar 

  • Solovchenko AE (2015) Recent breakthroughs in the biology of astaxanthin accumulation by microalgal cell. Photosynth Res 125:145–152

    Article  CAS  Google Scholar 

  • Solovchenko A, Neverov K (2017) Carotenogenic response in photosynthetic organisms: a colorful story. Photosynth Res 133:31–47

    Article  CAS  PubMed  Google Scholar 

  • Story EN, Kopec RE, Schwartz SJ, Harris GK (2010) An update of the health effects of tomato lycopene. Ann Rev Food Sci Technol. https://doi.org/10.1146/annurev.food.102308.124120

  • Strzalka K, Gruszecki WI (1994) Effect of beta-carotene on structural and dynamic properties of model phosphatidylcholine membranes. I. An EPR spin-label study. Biochim Biophys Acta 24:138–142

    Article  Google Scholar 

  • Su Y, Wang J, Shi M, Niu X, Yu X, Gao L, Zhang X, Chen L, Zhang W (2014) Metabolic and network analysis of astaxanthin producing Haematococcus pluvialis under various stress conditions. Bioresour Technol 170:522–529

    Article  CAS  PubMed  Google Scholar 

  • Takichi S (2011) Carotenoids in algae: distributions, biosynthesis and functions. Mar Drugs 9:1101–1118

    Article  CAS  Google Scholar 

  • Telfer A (2002) What is β-carotene doing in the photosystem II reaction center? Phil Trans R Soc Lond B 357:1431–1440

    Article  CAS  Google Scholar 

  • Toledo-Ortiz G, Huq E, Rodríguez-Concepción M (2010) Direct regulation of phytoene synthase gene expression and carotenoid biosynthesis by phytochrome-interacting factors. Proc Natl Acad Sci USA 107:11626–11631

    Article  PubMed  Google Scholar 

  • Tran D, Haven J, Qiu WG, Polle JEW (2009) An update on carotenoid biosynthesis in algae: phylogenetic evidence for the existence of two classes of phytoene synthase. Planta 229:723–729

    Article  CAS  PubMed  Google Scholar 

  • Trebst A (2003) Function of β-carotene and tocopherol in photosystem II. Z Naturforsch 58:609–620

    Article  CAS  Google Scholar 

  • Wang 2003, Zarka A, Trebst A, Boussiba S (2003) Astaxanthin accumulation in Haematococcus pluvialis (Chlorophyceae) as an active photoprotective process under high irradiance. J Phycol. https://doi.org/10.1111/j.0022-3646.2003.03-043.x

  • Wang B, Zhang Z, Hu Q, Sommerfeld M, Lu Y, Han D (2014a) Cellular capacities for high-light acclimation and changing lipid profiles across life cycle stages of the green alga Haematococcus pluvialis. PLoS One 9:e106679

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang H, Ou CG, Zhuang FY, Ma ZG (2014b) The dual role of phytoene synthase genes in carotenogenesis in carrot roots and leaves. Mol Breed 34:2065–2079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wolf AM, Asoh S, Hiranuma H, Ohsawa I, Iio K, Satou A, Ishikura M, Ohta S (2009) Astaxanthin protects mitochondrial redox state and functional integrity against oxidative stress. J Nut Biochem 21:381–389

    Article  CAS  Google Scholar 

  • Yuan J-P, Peng J, Yin K, Wang J-H (2011) Potential health promoting effects of astaxanthin: a high-value carotenoid mostly from microalgae. Mol Nut Food Res 55:437–449

    Google Scholar 

  • Zechmeister L (1962) cis-trans-isomeric carotenoids, vitamin A and Aryl polyenes. Springer, Vienna

    Book  Google Scholar 

  • Zhekisheva YJ, Zarka A, Khozin-Goldberg I, Cohen Z, 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

    Article  CAS  Google Scholar 

  • Zhou X, Welsch R, Yang Y, Álvarez A, Matthias R, Yuan H, Fish T, Liu J, Thannhouser TW, Li L (2015) Arabidopsis OR proteins are the major posttranscriptional regulators of phytoene synthase in controlling carotenoid biosynthesis. Proc Natl Acad Sci USA 112:3558–3563

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We wish to thank Dr. Aviv Shaish, The Bert W. Strassburger Lipid Center, Sheba Medical Center, Tel-Hashomer in Israel for critical comments and helpful discussions.

Author information

Authors and Affiliations

  1. Department of Biomolecular Sciences, The Weizmann Institute of Science, 76100, Rehovot, Israel

    Uri Pick

  2. Microalgal Biotechnology Laboratory, French Associates Institute for Agriculture and Biotechnology of Drylands, The Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede-Boker Campus, Beer-Sheva, 8499000, Israel

    Aliza Zarka & Sammy Boussiba

  3. Department of Chemistry and Biochemistry, University of California, Los Angeles, CA, 90095-1569, USA

    Lital Davidi

Authors
  1. Uri Pick
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Aliza Zarka
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sammy Boussiba
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lital Davidi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Uri Pick.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 17 kb)

Supplementary material 2 (PPTX 115 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pick, U., Zarka, A., Boussiba, S. et al. A hypothesis about the origin of carotenoid lipid droplets in the green algae Dunaliella and Haematococcus. Planta 249, 31–47 (2019). https://doi.org/10.1007/s00425-018-3050-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-018-3050-3

Keywords

Search

Navigation