Advertisement

Regulatory Roles in Photosynthesis of Unsaturated Fatty Acids in Membrane Lipids

  • Suleyman I. Allakhverdiev
  • Dmitry A. Los
  • Norio Murata
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 30)

Summary

The diversity of lipids in thylakoid membranes and their unique characteristics, in addition to their specific orientation in these membranes, strongly suggest that they play specific and important roles in the thylakoid membrane. In the chloroplasts of plants and algae, as well as in cyanobacterial cells, most of the photosyn-thetic machinery is embedded in thylakoid membranes, which are composed of proteins, lipids and pigments. Alterations in the extent of unsaturation of fatty acids in membrane lipids are expected to affect the physical characteristics of the membranes and, consequently, the activities of the photosynthetic machinery. The availability of entire genome sequences and an understanding of the functions of the individual genes for fatty acid desaturases in cyanobacteria led to the successful site-directed mutagenesis of such genes that reduced the extent of unsaturation of fatty acids in membrane lipids in a step-wise manner and, also, to the genetic transformation of cyanobacterial cells and whole plants that increased the extent of unsaturation of fatty acids in lipids of thylakoid membranes. Characterization of the photosynthetic properties of the transformed cyanobacteria and higher plants revealed that polyunsaturated fatty acids are essential for protection of the photosynthetic machinery against environmental stresses, such as strong light, salt stress, and high and low temperatures. Moreover, the available evidence suggests that the unsaturation of fatty acids enhances the repair of the photosystem II complex that has been damaged by strong light under stress conditions.

Keywords

Salt Stress Thylakoid Membrane Monounsaturated Fatty Acid Fatty Acid Desaturases Photosynthetic Machinery 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

ACP

Acyl-carrier protein

DGDG

Diga-lactosyldiacylglycerol

FTIR

Fourier transform infrared

GPAT

Glycerol-3-phosphate acyltransferase

MGDG

Monogalactosyldiacyglycerol

PG

Phosphatidylglycerol

PS I

Photosystem I

PS II

Photosystem II

SODG

Sulfoquinovosyldiacylglycerol

X:Y(Z)

Fatty acid in which X and Y indicate numbers of carbon atoms and double bonds, respectively, and Z in parenthesis indicates the position of double bond as counted from the carboxyl terminus of the fatty-acyl chain.

Notes

Acknowledgments

This work was supported, in part, by the Cooperative Research Program on the Stress Tolerance of Plants of the National Institute for Basic Biology to Norio Murata, and by grants from the Russian Foundation for Basic Research and the Molecular and Cell Biology Program of the Russian Academy of Sciences (to Suleyman I. Allakhverdiev and Dmitry A. Los).

References

  1. Adir N, Zer H, Shochat S and Ohad I (2003) Photoinhibition — a historical perspective. Photosynth Res 76: 343–370PubMedCrossRefGoogle Scholar
  2. Allakhverdiev SI and Murata N (2004) Environmental stress inhibits the synthesis de novo of proteins involved in the photodamage-repair cycle of photosystem II in Syn-echocystis sp. PCC 6803. Biochim Biophys Acta 1657: 23–32PubMedCrossRefGoogle Scholar
  3. Allakhverdiev SI and Murata N (2008) Salt stress inhibits photosystems II and I in cyanobacteria. Photosynth Res 98: 529–539PubMedCrossRefGoogle Scholar
  4. Allakhverdiev SI, Nishiyama Y, Suzuki I, Tasaka Y and Murata N (1999) Genetic engineering of the unsaturation of fatty acids in membrane lipids alters the tolerance of Synechocystis to salt stress. Proc Natl Acad Sci USA 96: 5862–5867PubMedCrossRefGoogle Scholar
  5. Allakhverdiev SI, Sakamoto A, Nishiyama Y, Inaba M and Murata N (2000) Ionic and osmotic effects of NaCl-induced inactivation of photosystems I and II in Syn-echococcus sp. Plant Physiol 123: 1047–1056PubMedCrossRefGoogle Scholar
  6. Allakhverdiev SI, Kinoshita M, Inaba M, Suzuki I and Murata N (2001) Unsaturated fatty acids in membrane lipids protect the photosynthetic machinery against salt-induced damage in Synechococcus. Plant Physiol 125: 1842–1853PubMedCrossRefGoogle Scholar
  7. Allakhverdiev SI, Tsvetkova N, Mohanty P, Szalontai B, Moon BY, Debreczeny M and Murata N (2005) Irreversible photoinhibition of photosystem II is caused by exposure of Synechocystis cells to strong light for a prolonged period. Biochim Biophys Acta 1708: 342–351PubMedCrossRefGoogle Scholar
  8. Ariizumi T, Kishitani S, Inatsugi R, Nishida I, Murata N and Toriyama K (2002) An increase in unsaturation of fatty acids in phosphatidylglycerol from leaves improves the rates of photosynthesis and growth at low temperatures in transgenic rice seedlings. Plant Cell Physiol 43: 751–758PubMedCrossRefGoogle Scholar
  9. Aro EM, Suorsa M, Rokka A, Allakhverdiyeva Y, Paakka-rinen V, Saleem A, Battchikova N and Rintamäki E (2005) Dynamics of photosystem II: a proteomic approach to thylakoid protein complexes. J Exp Bot 56: 347–356PubMedCrossRefGoogle Scholar
  10. Barkan L, Vijayan P, Carlsson AS, Mekhedov S and Browse J (2006) A suppressor of fab1 challenges hypotheses on the role of thylakoid unsaturation in photosynthetic function. Plant Physiol 141: 1012–1020PubMedCrossRefGoogle Scholar
  11. Chapman DJ, De-Felice J and Barber J (1983) Growth temperature effects on thylakoid membrane lipid and protein content of pea chloroplasts. Plant Physiol 72: 225–228PubMedCrossRefGoogle Scholar
  12. Dilley RA, Nishiyama Y, Gombos Z and Murata N (2001) Bioenergetic responses of Synechocystis 6803 fatty acid desaturase mutants at low temperatures. J Bioenerg Biomembr 33: 135–141PubMedCrossRefGoogle Scholar
  13. Dunn TM, Lynch DV, Michaelson LV and Napier JA (2004) A post-genomic approach to understanding sphingolipid metabolism in Arabidopsis thaliana. Ann Bot (Lond) 93: 483–497CrossRefGoogle Scholar
  14. Frentzen M, Heinz E, McKeon T and Stumpf PK (1983) Specificities and selectivities of glycerol-3-phosphate acyltransferase and monoacylglycerol-3-phosphate acyl-transferase from pea and spinach chloroplasts. Eur J Bio-chem 129: 629–636CrossRefGoogle Scholar
  15. Frentzen M, Nishida I and Murata N (1987) Properties of the plastidial acyl-(acyl-carrier protein): glycerol-3-phosphate acyltransferase from the chilling-sensitive plant squash (Cucurbita moschata). Plant Cell Physiol 28: 1195–1201Google Scholar
  16. Gombos Z and Murata N (1998) Genetic engineering of the unsaturation of membrane glycerolipid: effects on the ability of the photosynthetic machinery to tolerate temperature stress. In: Siegenthaler P-A and Murata N (eds) Lipids in Photosynthesis: Structure, Function and Genetics. Kluwer, Dordrecht, pp. 249–262Google Scholar
  17. Gombos Z, Wada H and Murata N (1992) Unsaturation of fatty acids in membrane lipids enhances tolerance of the cyanobacterium Synechocystis PCC6803 to low-temperature photoinhibition. Proc Natl Acad Sci USA 89: 9959–9963PubMedCrossRefGoogle Scholar
  18. Gombos Z, Wada H and Murata N (1994) The recovery of photosynthesis from low-temperature photoinhibition is accelerated by the unsaturation of membrane lipids: a mechanism of chilling tolerance. Proc Natl Acad Sci USA 91: 8787–8791PubMedCrossRefGoogle Scholar
  19. Gombos Z, Kanervo E, Tsvetkova N, Sakamoto T, Aro EM and Murata N (1997) Genetic enhancement of the ability to tolerate photoinhibition by introduction of unsaturated bonds into membrane glycerolipids. Plant Physiol 115: 551–559PubMedGoogle Scholar
  20. Gutensohn M, Fan E, Frielingsdorf S, Hanner P, Hou B, Hust B and Klösgen RB (2006) Toc, Tic, Tat et al.: structure and function of protein transport machineries in chlo-roplasts. J Plant Physiol 163: 333–347PubMedCrossRefGoogle Scholar
  21. Hakala M, Tuominen I, Keränen M, Tyystjärvi T and Tyys-tjärvi E (2005) Evidence for the role of the oxygen-evolving manganese complex in photoinhibition of photosystem II. Biochim Biophys Acta 1706: 68–80PubMedCrossRefGoogle Scholar
  22. Harwood JL (2007) Temperature stress: reacting and adapting: lessons from poikilotherms. Ann N Y Acad Sci 1113: 52–57PubMedCrossRefGoogle Scholar
  23. Hugly S, Kunst L, Browse J and Somerville C (1989) Enhanced thermal tolerance of photosynthesis and altered chloroplast ultrastructure in a mutant of Arabidopsis deficient in lipid desaturation. Plant Physiol 90: 1134–1142PubMedCrossRefGoogle Scholar
  24. Imai H, Ohnishi M, Hotsubo K, Kojima M and Ito S (1997) Sphingoid base composition of cerebrosides from plant leaves. Biosci Biotechol Biochem 61: 351–353CrossRefGoogle Scholar
  25. Inaba M, Suzuki I, Szalontai B, Kanesaki Y, Los DA, Hayashi H and Murata N (2003) Gene-engineered rigidification of membrane lipids enhances the cold inducibility of gene expression in Synechocystis. J Biol Chem 278: 12191–12198PubMedCrossRefGoogle Scholar
  26. Ishizaki-Nishizawa O, Fujii T, Azuma M, Sekiguchi K, Murata N, Ohtani T and Toguri T (1996) Low-temperature resistance of higher plants is significantly enhanced by a nonspecific cyanobacterial desaturase. Nature Bio-technol 14: 1003–1006CrossRefGoogle Scholar
  27. Kachroo A, Shanklin J, Whittle E, Lapchyk L, Hildebrand D and Kachroo P (2007) The Arabidopsis stearoyl-acyl carrier protein-desaturase family and the contribution of leaf isoforms to oleic acid synthesis. Plant Mol Biol 63: 257–271PubMedCrossRefGoogle Scholar
  28. Kamada Y, Jung US, Piotrowski J and Levin DE (1995) The protein kinase C-activated MAP kinase pathway of Sac-charomyces cerevisiae mediates a novel aspect of the heat shock response. Genes Dev 9: 1559–1571PubMedCrossRefGoogle Scholar
  29. Kanervo E, Aro EM and Murata N (1995) Low unsatura-tion level of thylakoid membrane lipids limits turnover of the D1 protein of photosystem II at high irradiance. FEBS Lett 364: 239–242PubMedCrossRefGoogle Scholar
  30. Kanervo E, Tasaka Y, Murata N and Aro EM (1997) Membrane lipid unsaturation modulates processing of the photosystem II reaction-center protein D1 at low temperatures. Plant Physiol 114: 841–849PubMedCrossRefGoogle Scholar
  31. Liu X-Y, Li B, Yang J-H, Sui N, Yang X-M and Meng Q-W (2008) Overexpression of tomato chloroplast omega-3 fatty acid desaturase gene alleviates the photoinhibition of photosystems 2 and 1 under chilling stress. Photosyn-thetica 46: 185–192CrossRefGoogle Scholar
  32. Logue JA, de Vries AL, Fodor E and Cossins AR (2000) Lipid compositional correlates of temperature-adaptive interspecific differences in membrane physical structure. J Exp Biol 203: 2105–2114PubMedGoogle Scholar
  33. Los DA and Murata N (1998) Structure and expression of fatty acid desaturases. Biochim Biophys Acta 1394: 3–15PubMedCrossRefGoogle Scholar
  34. Los DA and Murata N (1999) Responses to cold shock in cyanobacteria. J Mol Microbiol Biotechnol 1: 221–230PubMedGoogle Scholar
  35. Los DA and Murata N (2004) Membrane fluidity and its roles in the perception of environmental signals. Biochim Biophys Acta 1666: 142–157PubMedCrossRefGoogle Scholar
  36. Los DA, Ray MK 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: 1167–1175PubMedCrossRefGoogle Scholar
  37. Ma X and Browse J (2006) Altered rates of protein transport in Arabidopsis mutants deficient in chloroplast membrane unsaturation. Phytochemistry 67: 1629–1636PubMedCrossRefGoogle Scholar
  38. Macartney AI, Maresca B and Cossins AR (1994) Acyl-CoA desaturases and the adaptive regulation of membrane lipid composition. In: Cossins AR (ed) Temperature Adaptation of Biological Membranes. Portland Press, London, pp. 129–139Google Scholar
  39. Mamedov MD, Hayashi H and Murata N (1993) Effects of glycinebetaine and unsaturation of membrane lipids on heat stability of photosynthetic electron transport and phosphorylation reactions in Synechocystis PCC 6803. Biochim Biophys Acta 1142: 1–5CrossRefGoogle Scholar
  40. Matsuda O, Sakamoto H, Hashimoto T and Iba K (2005) A temperature-sensitive mechanism that regulates post-translational stability of a plastidial μ-3 fatty acid desatu-rase (FAD8) in Arabidopsis leaf tissues. J Biol Chem 280: 3597–3604PubMedCrossRefGoogle Scholar
  41. McCourt P, Kunst L, Browse J and Somerville CR (1987) The effects of reduced amounts of lipid unsaturation on chloroplast ultrastructure and photosynthesis in a mutant of Arabidopsis. Plant Physiol 84: 353–360PubMedCrossRefGoogle Scholar
  42. Miyao M and Murata N (1983) Partial disintegration and reconstitution of the photosynthetic oxygen-evolution system: binding of 24 kDa and 18 kDa polypeptides. Bio-chim Biophys Acta 725: 87–93CrossRefGoogle Scholar
  43. Mohanty P, Allakhverdiev SI and Murata N (2007) Application of low temperatures during photoinhibition allows characterization of individual steps in photodamage and the repair of photosystem II. Photosynth Res 94: 217– 224PubMedCrossRefGoogle Scholar
  44. Moon BY, Higashi S, Gombos Z and Murata N (1995) Unsaturation of the membrane lipids of chloroplasts stabilizes the photosynthetic machinery against low-temperature photoinhibition in transgenic tobacco plants. Proc Natl Acad Sci USA 92: 6219–6223PubMedCrossRefGoogle Scholar
  45. Murata N (1989) Low-temperature effects on cyanobacterial membranes. J Bioenerg Biomembr 21: 61–75PubMedCrossRefGoogle Scholar
  46. Murata N and Miyao M (1985) Extrinsic membrane proteins in the photosynthetic oxygen-evolving complex. Trends Biochem Sci 10: 122–124CrossRefGoogle Scholar
  47. Murata N and Wada H (1995) Acyl-lipid desaturases and their importance in the tolerance and acclimatization to cold of cyanobacteria. Biochem J 308: 1–8PubMedGoogle Scholar
  48. Murata N, Ishizaki-Nishizawa O, Higashi S, Hayashi H, Tasaka Y and Nishida I (1992) Genetically engineered alteration in the chilling sensitivity of plants. Nature 356: 710–713; (correction) 357: 607CrossRefGoogle Scholar
  49. Murata N, Takahashi S, Nishiyama Y and Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta 1767: 414–421PubMedCrossRefGoogle Scholar
  50. Nishida I and Murata N (1996) Chilling sensitivity in plants and cyanobacteria: the crucial contribution of membrane lipids. Annu Rev Plant Physiol Plant Mol Biol 47: 541– 568PubMedCrossRefGoogle Scholar
  51. Nishida I, Frentzen M, Ishizaki O and Murata N (1987) Purification of isomeric forms of acyl-[acyl-carrier-protein]:glycerol-3-phosphate acyltransferase from greening squash cotyledons. Plant Cell Physiol 28: 1071–1079Google Scholar
  52. 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 thal-iana. Plant Mol Biol 21: 267–277PubMedCrossRefGoogle Scholar
  53. Nishiyama Y, Allakhverdiev SI and Murata N (2005) Inhibition of the repair of photosystem II by oxidative stress in cyanobacteria. Photosynth Res 84: 1–7PubMedCrossRefGoogle Scholar
  54. Nishiyama Y, Allakhverdiev SI and Murata N (2006) A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochim Biophys Acta 1757: 742–749PubMedCrossRefGoogle Scholar
  55. Ohnishi N, Allakhverdiev SI, Takahashi S, Higashi S, Watanabe M, Nishiyama Y and Murata N (2005) The two-step mechanism of photodamage to photosystem II: step one occurs at the oxygen-evolving complex and step two occurs at the photochemical reaction center. Biochemistry 44: 8494–8499PubMedCrossRefGoogle Scholar
  56. Orlova IV, Serebriiskaya TS, Popov V, Merkulova N, Nosov AM, Trunova TI, Tsydendambaev VD and Los DA (2003) Transformation of tobacco with a gene for the thermophilic acyl-lipid desaturase enhances the chilling tolerance of plants. Plant Cell Physiol 44: 447–450PubMedCrossRefGoogle Scholar
  57. Panpoom S, Los DA and Murata N (1998) Biochemical characterization of a Δ12 acyl-lipid desaturase after over-expression of the enzyme in Escherichia coli. Biochim Biophys Acta 1390: 323–332PubMedCrossRefGoogle Scholar
  58. Popova AV, Velitchkova M and Zanev Y (2007) Effect of membrane fluidity on photosynthetic oxygen production reactions. Z Naturforsch [C] 62: 253–260Google Scholar
  59. Reddy AS, Nuccio ML, Gross LM and Thomas TL (1993) Isolation of a Δ6-desaturase gene from the cyanobacte-rium Synechocystis sp. strain PCC 6803 by gain-of-func-tion expression in Anabaena sp. strain PCC 7120. Plant Mol Biol 22: 293–300PubMedCrossRefGoogle Scholar
  60. Sakamoto A, Sulpice R, Hou C-X, Kinoshita M, Higashi S, Kanaseki T, Nonaka H, Moon BY and Murata N (2003) Genetic modification of fatty acid unsaturation of phos-phatidylglycerol in chloroplasts alters the sensitivity of tobacco plants to cold stress. Plant Cell Environ 27: 99–105CrossRefGoogle Scholar
  61. Sakamoto T, Los DA, Higashi S, Wada H, Nishida I, Ohmori M and Murata N (1994) Cloning of μ3 desaturase from cyanobacteria and its use in altering the degree of mem-brane-lipid unsaturation. Plant Mol Biol 26: 249–263PubMedCrossRefGoogle Scholar
  62. Sayanova O, Haslam R, Guschina I, Lloyd D, Christie WW, Harwood JL and Napier JA (2006) A bifunctional Β12,Β15-desaturase from Acanthamoeba castellanii directs the synthesis of highly unusual n-1 series unsatu-rated fatty acids. J Biol Chem 281: 36533–36541PubMedCrossRefGoogle Scholar
  63. Sippola K, Kanervo E, Murata N and Aro EM (1998) A genetically engineered increase in fatty acid unsaturation in Synechococcus sp. PCC 7942 allows exchange of D1 protein forms and sustenance of photosystem II activity at low temperature. Eur J Biochem 251: 641–648PubMedCrossRefGoogle Scholar
  64. Sui N, Li M, Zhao S-J, Li F, Liang H and Meng Q-W (2007a) Overexpression of glycerol-3-phosphate acyltransferase gene improves chilling tolerance in tomato. Planta 226: 1097–1108CrossRefGoogle Scholar
  65. Sui N, Li M, Shu D-F, Zhao S-J and Meng Q-W (2007b) Antisense-mediated depletion of tomato chloroplast glyc-erol-3-phosphate acyltransferase affects male fertility and increases thermal tolerance. Physiol Plant 130: 301–314CrossRefGoogle Scholar
  66. Szalontai B, Nishiyama Y, Gombos Z and Murata N (2000) Membrane dynamics as seen by Fourier transform infrared spectroscopy in a cyanobacterium, Synechocystis PCC 6803. The effects of lipid unsaturation and the protein-to-lipid ratio. Biochim Biophys Acta 1509: 409–419PubMedCrossRefGoogle Scholar
  67. Szalontai B, Kota Z, Nonaka H and Murata N (2003) Structural consequences of genetically engineered saturation of the fatty acids of phosphatidylglycerol in tobacco thylakoid membranes. An FTIR Study. Biochemistry 42: 4292–4299PubMedCrossRefGoogle Scholar
  68. Takahashi S and Murata N (2008) How do environmental stresses accelerate photoinhibition? Trends Plant Sci 13: 178–182PubMedCrossRefGoogle Scholar
  69. Tang G-Q, Novitzky WP, Griffin HC, Huber SC and Dewey RE (2005) Oleate desaturase enzymes of soybean: evidence of regulation through differential stability and phosphorylation. Plant J 44: 433–446PubMedCrossRefGoogle Scholar
  70. Tasaka Y, Gombos Z, Nishiyama Y, Mohanty P, Ohba T, Ohki K and Murata N (1996) Targeted mutagenesis of acyl-lipid desaturases in Synechocystis: evidence for the important roles of polyunsaturated membrane lipids in growth, respiration and photosynthesis. EMBO J 15: 6416–6425PubMedGoogle Scholar
  71. Tiku PE, Gracey AY, Macartney AI, Beynon RJ and Cossins AR (1996) Cold-induced expression of Β9-desaturase in carp by transcriptional and posttranslational mechanisms. Science 271: 815–818PubMedCrossRefGoogle Scholar
  72. Tyystjärvi E (2008) Photoinhibition of photosystem II and photodamage to the oxygen-evolving manganese cluster. Coord Chem Rev 252: 361–376CrossRefGoogle Scholar
  73. Vijayan P and Browse J (2002) Photoinhibition in mutants of Arabidopsis deficient in thylakoid unsaturation. Plant Physiol 129: 876–885PubMedCrossRefGoogle Scholar
  74. Wada H and Murata N (1990) Temperature-induced changes in the fatty acid composition of the cyanobacterium Syn-echocystis PCC 6803. Plant Physiol 92: 1062–1069PubMedCrossRefGoogle Scholar
  75. Wada H, Gombos Z and Murata N (1990) Enhancement of chilling tolerance of a cyanobacterium by genetic manipulation of fatty acid desaturation. Nature 347: 200–203PubMedCrossRefGoogle Scholar
  76. Wada H, Gombos Z and Murata N (1994) Contribution of membrane lipids to the ability of the photosynthetic machinery to tolerate temperature stress. Proc Natl Acad Sci USA 91: 4273–4277PubMedCrossRefGoogle Scholar
  77. Wallis JG and Browse J (2002) Mutants of Arabidopsis reveal many roles for membrane lipids. Prog Lipid Res 41: 254–278PubMedCrossRefGoogle Scholar
  78. Wu J and Browse J (1995) Elevated levels of high-melting-point phosphatidylglycerols do not induce chilling sensitivity in an Arabidopsis mutant. Plant Cell 1: 17–27Google Scholar
  79. Wu J, Lightner J, Warwick N and Browse J (1997) Low-temperature damage and subsequent recovery of fab1 mutant Arabidopsis exposed to 2°C. Plant Physiol 113: 347–56PubMedCrossRefGoogle Scholar
  80. Yokoi S, Higashi S, Kishitani S, Murata N and Toriyama K (1998) Introduction of the cDNA for Arabidopsis glycerol-3-phosphate acyltransferase (GPAT) confers unsaturation of fatty acids and chilling tolerance of photosynthesis on rice. Mol Breed 4: 269–275CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Suleyman I. Allakhverdiev
    • 1
  • Dmitry A. Los
    • 2
  • Norio Murata
    • 3
  1. 1.Institute of Basic Biological ProblemsRussian Academy of SciencesPushchinoRussia
  2. 2.Institute of Plant PhysiologyRussian Academy of SciencesMoscowRussia
  3. 3.National Institute for Basic BiologyMyodaijiJapan

Personalised recommendations