Marine Biotechnology

, 10:602 | Cite as

Nutrient Limitation is the Main Regulatory Factor for Carotenoid Accumulation and for Psy and Pds Steady State Transcript Levels in Dunaliella salina (Chlorophyta) Exposed to High Light and Salt Stress

  • Sacha Nicole Coesel
  • Alexandra Cordeiro Baumgartner
  • Licia Marlene Teles
  • Ana Alexandra Ramos
  • Nuno Miguel Henriques
  • Leonor Cancela
  • João Carlos Serafim Varela
Original Article

Abstract

Dunaliella salina (Dunal) Teodoresco (1905) is a green unicellular alga able to withstand severe salt, light, and nutrient stress, adaptations necessary to grow in harsh environments such as salt ponds. In response to such growth conditions, this microalga accumulates high amounts of β-carotene in its single chloroplast. In this study, we show that carotenoid accumulation is consistently inhibited in cells grown in nutrient-supplemented media and exposed either to high-light or medium-low-light conditions. Likewise, carotenogenesis in cells shifted to higher salinity (up to 27% NaCl) under medium-low-light conditions is inhibited by the presence of nutrients. The steady-state levels of transcripts encoding phytoene synthase and phytoene desaturase increased substantially in D. salina cells shifted to high light or high salt under nutrient-limiting conditions, whereas the presence of nutrients inhibited this response. The regulatory effect of nutrient availability on the accumulation of carotenoids and messenger RNA levels of the first two enzymes committed to carotenoid biosynthesis is discussed.

Keywords

Dunaliella salina Carotenoid biosynthesis Light Nitrate Nutrients Salt Stress 

References

  1. Ben-Amotz A, Avron M (1983) On the factors which determine massive β-carotene accumulation in the halotolerant alga Dunaliella bardawil. Plant Physiol 72:593–597PubMedCrossRefGoogle Scholar
  2. Ben-Amotz A, Katz A, Avron M (1982) Accumulation of β-carotene in halotolerant algae: purification and characterization of beta-carotene-rich globules from Dunaliella bardawil (Chlorophyceae). J Phycol 18:529–537CrossRefGoogle Scholar
  3. Ben-Amotz A, Gressel J, Avron A (1987) Massive accumulation of phytoene induced by norflurazon in Dunaliella bardawil (Chlorophyceae) prevents recovery from photoinhibition. J Phycol 23:176–181Google Scholar
  4. Ben-Amotz A, Shaish A, Avron M (1989) Mode of action of the massively accumulated beta-carotene of Dunaliella bardawil in protecting the alga against damage by excess irradiation. Plant Physiol 91:1040–1043PubMedGoogle Scholar
  5. Bohne F, Linden H (2002) Regulation of carotenoid biosynthesis genes in response to light in Chlamydomonas reinhardtii. Biochim Biophys Acta 1579:26–34PubMedGoogle Scholar
  6. Borowitzka MA, Borowitzka LJ, Kessly D (1990) Effects of salinity increase on carotenoid accumulation in the green alga Dunaliella salina. J Appl Phycol 2:111–119CrossRefGoogle Scholar
  7. Campisi L, Fambrini M, Michelotti V, Salvini M, Giuntini D, Pugliesi C (2006) Phytoene accumulation in sunflower decreases the transcript levels of the phytoene synthase gene. Plant Growth Regul 48:79–87CrossRefGoogle Scholar
  8. Cowan AK, Rose PD, Horne LG (1992) Dunaliella salina: a model system for studying the response of plant cells to stress. J Exp Bot 43:1535–1547CrossRefGoogle Scholar
  9. Cunningham FX, Gantt E (1998) Genes and enzymes of carotenoid biosynthesis in plants. Annu Rev Plant Phys 49:557–583CrossRefGoogle Scholar
  10. Demmig-Adams B, Gilmore AM, Adams WW 3rd (1996) Carotenoids 3: in vivo function of carotenoids in higher plants. FASEB J 10:403–412PubMedGoogle Scholar
  11. Goodwin TW (1980) The biochemistry of the carotenoids. London, Chapham and HallGoogle Scholar
  12. Grossman AR, Lohr M, Im CS (2004) Chlamydomonas reinhardtii in the landscape of pigments. Annu Rev Genet 38:119–173PubMedCrossRefGoogle Scholar
  13. Grunewald K, Eckert M, Hirschberg J, Hagen C (2000) Phytoene desaturase is localized exclusively in the chloroplast and up-regulated at the mRNA level during accumulation of secondary carotenoids in Haematococcus pluvialis (Volvocales, Chlorophyceae). Plant Physiol 122:1261–1268PubMedCrossRefGoogle Scholar
  14. Hagen C, Braune W, Bjorn LO (1994) Functional aspects of secondary carotenoids in Haematococcus lacustris (Volvocales). III. Action as a “sunshade”. J Phycol 30:241–248CrossRefGoogle Scholar
  15. Lers A, Biener Y, Zamir A (1990) Photoinduction of massive beta-carotene accumulation by the alga Dunaliella bardawil: kinetics and dependence on gene activation. Plant Physiol 93:389–395PubMedGoogle Scholar
  16. Lohr M, Im CS, Grossman AR (2005) Genome-based examination of chlorophyll and carotenoid biosynthesis in Chlamydomonas reinhardtii. Plant Physiol 138:490–515PubMedCrossRefGoogle Scholar
  17. Marin N, Morales F, Lodeiros C, Tamigneaux E (1998) Effect of nitrate concentration on growth and pigment synthesis of Dunaliella salina cultivated under low illumination and preadapted to different salinities. J Appl Phycol 10:405–411CrossRefGoogle Scholar
  18. Masuda T, Polle JE, Melis A (2002) Biosynthesis and distribution of chlorophyll among the photosystems during recovery of the green alga Dunaliella salina from irradiance stress. Plant Physiol 128:603–614PubMedCrossRefGoogle Scholar
  19. Navalho J (1997) Biotechnology of Dunaliella salina for beta-carotene production. MSc thesis, University of Algarve, Faro, PortugalGoogle Scholar
  20. Rabbani S, Beyer P, Von Lintig J, Hugueney P, Kleinig H (1998) Induced beta-carotene synthesis driven by triacylglycerol deposition in the unicellular alga Dunaliella bardawil. Plant Physiol 116:1239–1248PubMedCrossRefGoogle Scholar
  21. Salguero A, De La Morena B, Vigara J, Vega JM, Vilchez C, Leon R (2003) Carotenoids as protective response against oxidative damage in Dunaliella bardawil. Biomol Eng 20:249–253PubMedCrossRefGoogle Scholar
  22. Salvini M, Bernini A, Fambrini M, Pugliesi C (2005) cDNA cloning and expression of the phytoene synthase gene in sunflower. J Plant Physiol 162:479–484PubMedCrossRefGoogle Scholar
  23. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NYGoogle Scholar
  24. Sánchez-Estudillo L, Freile-Pelegrin Y, Rivera-Madrid R, Robledo D, Narvaez-Zapata JA (2006) Regulation of two photosynthetic pigment-related genes during stress-induced pigment formation in the green alga, Dunaliella salina. Biotechnol Lett 28:787–791PubMedCrossRefGoogle Scholar
  25. Schaeffer L, Sandmann M, Woitsch S, Sandmann G (2006) Coordinate up-regulation of carotenoid biosynthesis as a response to light stress in Synechococcus PCC7942. Plant Cell Environ 29:1349–1356CrossRefGoogle Scholar
  26. Simkin AJ, Laboure AM, Kuntz M, Sandmann G (2003a) Comparison of carotenoid content, gene expression and enzyme levels in tomato (Lycopersicon esculentum) leaves. Z Naturforsch [C] 58:371–380Google Scholar
  27. Simkin AJ, Zhu C, Kuntz M, Sandmann G (2003b) Light-dark regulation of carotenoid biosynthesis in pepper (Capsicum annuum) leaves. J Plant Physiol 160:439–443PubMedCrossRefGoogle Scholar
  28. Steinbrenner J, 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 125:810–817PubMedCrossRefGoogle Scholar
  29. Steinbrenner J, Linden H (2003) Light induction of carotenoid biosynthesis genes in the green alga Haematococcus pluvialis: regulation by photosynthetic redox control. Plant Mol Biol 52:343–356PubMedCrossRefGoogle Scholar
  30. Von Lintig J, Welsch R, Bonk M, Giuliano G, Batschauer A, Kleinig H (1997) Light-dependent regulation of carotenoid biosynthesis occurs at the level of phytoene synthase expression and is mediated by phytochrome in Sinapis alba and Arabidopsis thaliana seedlings. Plant J 12:625–634CrossRefGoogle Scholar
  31. Wang B, Zarka A, Trebst A, Boussiba S (2003) Astaxanthin accumulation in Haematococcus pluvialis (Chlorophyceae) as an active photoprotective process under high irradiance. J Phycol 39:1116–1124CrossRefGoogle Scholar
  32. White AL, Jahnke LS (2002) Contrasting effects of UV-A and UV-B on photosynthesis and photoprotection of beta-carotene in two Dunaliella spp. Plant Cell Physiol 43:877–884PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • Sacha Nicole Coesel
    • 1
  • Alexandra Cordeiro Baumgartner
    • 2
  • Licia Marlene Teles
    • 1
  • Ana Alexandra Ramos
    • 1
  • Nuno Miguel Henriques
    • 1
  • Leonor Cancela
    • 1
  • João Carlos Serafim Varela
    • 1
  1. 1.Centre of Marine Sciences (CCMar)University of Algarve, Campus de GambelasFaroPortugal
  2. 2.Institute of Veterinary MedicineUniversity of GöttingenGöttingenGermany

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