Biopolym. Cell. 2009; 25(1):3-11.
Reviews
Plant sulfolipid. II. Mutant study and
phosphate deficiency
- Taras Shevchenko National University of Kyiv
64, Volodymyrska Str., Kyiv, Ukraine, 01601
Abstract
Study with SQDG-deficient mutants showed that formation of the sulfonic acid precursor, UDP-sulfoquinovose, in higher plants is considered to be catalyzed by the orthologous plant proteins SQD1. The second required plant enzyme, SQD2, is highly similar to glycosyltransferases and it is proposed that this protein represents sulfolipid synthase. The results of recent works have shown that for the stable activity PS II needs the presence of SQDG and that it participates in PS II recovering through some mechanism dependent on light. Under phosphate-limiting conditions a decrease in the content of one acidic lipid (PG) was accompanied by an increase in the content of the other acidic lipid (SQDG), which resulted in the maintenance of a certain level of total acidic lipids of chloroplast membranes.
Keywords: glycolipid, sulfolipid, sulfoquinovosyldiacylglycerol, SQDG
Full text: (PDF, in English)
References
[1]
Benning C., Somerville C. R. Isolation and genetic complementation of a sulfolipid-deficient mutant of Rhodobacter sphaeroides. J. Bacteriol. 1992; 174(7):2352–2360.
[2]
Benning C., Somerville C. R. Identification of an operon involved in sulfolipid biosynthesis in Rhodobacter sphaeroides. J. Bacteriol. 1992; 174(20):6479–6487.
[3]
Rossak M., Tietje C., Heinz E., Benning C. Accumulation of UDP-sulphoquinovose in a sulfolipid-deficient mutant of Rhodobacter sphaeroides J. Biol. Chem 1995 270, N 43:25792–25797.
[4]
Benning C. Membrane lipids in anoxygenic photosynthetic bacteria Lipids in photosynthesis: structure, function and genetics. Eds P.-A. Siegenthaler, N. Murata Amsterdam: Kluwer Acad. Publ., 1998:83–101.
[5]
Guler S., Essigmann B., Benning C. A cyanobacterial gene, sqdx, required for biosynthesis of the sulfolipid sulfoquinovosyldiacylglycerol J. Bacteriol 2000 182, N 2:543–545.
[6]
Guler S., Seeliger A., Hartel H., Renger G., Benning C. A null mutant of Synechococcus sp. PCC7942 deficient in the sulfolipid sulfoquinovosyl diacylglycerol J. Biol. Chem 1996 271, N 13:7501-7507.
[7]
Essigmann B., Guler S., Narang R. A., Linke D., Benning C. Phosphate availability affects the thylakoid lipid composition and the expression of SQD1, a gene required for sulfolipid biosynthesis in Arabidopsis thaliana Proc. Nat. Acad. Sci. USA 1998 95, N 4:1950–1955.
[8]
Sanda S., Leustek T., Theisen M. J., Garavito R. M., Benning C. Recombinant Arabidopsis SQD1 converts UDP-glucose and sulfite to the sulfolipid head group precursor UDPsulfoquinovose in vitro J. Biol. Chem 2001 276, N 6 P. 3941–3946.
[9]
Berg S., Edman M., Li L., Wikstrom M., Wieslander A. Sequence properties of the 1,2-diacylglycerol 3-glucosyltransferase from Acholeplasma laidlawii membranes J. Biol. Chem 2001 276, N 25:22056–22063.
[10]
Yu B., Xu C., Benning C. Arabidopsis disrupted in SQD2 encoding sulfolipid synthase is impaired in phosphate-limited growth Proc. Nat. Acad. Sci. USA 2002 99, N 8 P. 5732–5737.
[11]
Benning C., Beatty J. T., Prince R. C., Somerville C. R. The sulfolipid sulfoquinovosyldiacylglycerol is not required for photosynthetic electron transport in Rhodobacter sphaeroides but enhances growth under phosphate limitation Proc. Nat. Acad. Sci. USA 1993 90, N 4:1561–1565.
[12]
Sato N., Somoke K., Tsuzsuki M., Kawaguchi A. Impared PS II in a mutant of Chlamydomonas reinhardtii defective in sulfoquinovosyldiacylglycerol Eur. J. Biol. Chem 1995 234, N 1:16–23.
[13]
Minoda A., Sonoike K., Nozaki H., Okada K., Sato N., Tsuzuki M. Contribution of SQDG in photosystem II of Chlamydomonas reinhardtii. PS2001 Proc. 12th Int. Cong. Photosynthesis Brisbane, 2001; S5–039.
[14]
Minoda A., Sato N., Nozaki H., Okada K., Takahashi H., Sonoike K., Tsuzuki M. Role of sulfoquinovosyl diacylglycerol for the maintenance of photosystem II in Chlamydomonas reinhardtii Eur. J. Biochem 2002 269, N 9:2353– 2358.
[15]
Minoda A., Sonoike K., Okada K., Sato N., Tsuzuki M. Decrease in the efficiency of the electron donation to tyrosine Z of photosystem II in an SQDG-deficient mutant of Chlamydomonas FEBS Lett 2003 553, N 1:109–112.
[16]
Sato N., Aoki M., Maru Y., Sonoike K., Minoda A., Tsuzuki M. Involvement of sulfoquinovosyl diacylglycerol in the structural integrity and heat-tolerance of photosystem II. Planta. 2003; 217(2):245–251.
[17]
Aoki M., Sato N., Meguro A., Tsuzuki M. Differing involvement of sulfoquinovosyl diacylglycerol in photosystem II in two species of unicellular cyanobacteria Eur. J. Biochem 2004 271, N 4:685–693.
[18]
Raghothama K.G. Phosphate acquisition Ann. Rev. Plant Physiol. Plant Mol. Biol 1999 50:665–693.
[19]
Misson J., Raghothama K. G., Jain A., Jouhet J., Block M. A., Bligny R., Ortet Ph., Creff A., Somerville S., Rolland N., Doumas P., Nacry Ph., Herrerra-Estrella L., Nussaume L., Thibaud M.-Chr. A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation Proc. Nat. Acad. Sci. USA 2005 102, N 33 P.11934–11939.
[20]
Benning C., Ohta H. Three enzyme systems for galactoglycerolipid biosynthesis are coordinately regulated in plants J. Biol. Chem 2005 280, N 4:2397–2400.
[21]
Kelly A. A., Froehlich J. E., Dormann P. Disruption of the two digalactosyldiacylglycerolsynthase genes DGD1 and DGD2 in Arabidopsis reveals the existence of an additional enzyme of galactolipid synthesis Plant Cell 2003 15, N 11:2694–2706.
[22]
Hartel H., Dormann P., Benning C. DGD1-independent biosynthesis of extraplastidic galactolipids after phosphate deprivation in Arabidopsis Proc. Natl. Acad. Sci. USA 2000 97, N 19:10649–10654.
[23]
Wasaki J., Yonetani R., Kuroda S., Shinano T., Yazaki J., Fujii F., Shimbo K., Yamamoto K., Sakata K., Sasaki T., Kishimoto N., Kikuchi S., Yamagishi M., Osaki M. Transcriptomic analysis of metabolic changes by phosphorus stress in rice plant roots Plant Cell Environ 2003 26, N 9:1515–1523.
[24]
Yu B., Benning C. Anionic lipids are required for chloroplast structure and function in Arabidopsis Plant J 2003 36, N 6:762–770.
[25]
Hammond J. P., Bennett M. J., Bowen H. C., Broadley M. R., Eastwood D. C., May S. T., Rahn C., Swarup R., Woolaway K. E., White P. J. Changes in gene expression in arabidopsis shoots during phosphate starvation and the potential for developing smart plants Plant Physiol 2003 132, N 2 P. 578–596.
[26]
Andersson M. X., Stridh M. H., Larsson K. E., Liljenberg C., Sandelius A. E. Phosphate-deficient oat replaces a major portion of the plasma membrane phospholipids with the galactolipid digalactosyldiacylglycerol FEBS Lett 2003 537, N 1:128–132.
[27]
Sato N., Hagio M., Wada H., Tsuzuki M. Environmental effects on acidic lipids of thylakoid membranes Biochem. Soc. Trans 2000 28, N 6:912–914.
[28]
Selstam E. Development of thylakoid membranes with respect to lipids Lipids in photosynthesis: structure, function and genetics. Advances in photosynthesis 6. Eds P.-A. Siegenthaler, N. Murata Amsterdam: Kluwer Acad. Publ., 1998:209–224.
[29]
Sakurai I., Mizusawa N., Ohashi S., Kobayashi M., Wada H. Effects of the lack of phosphatidylglycerol on the donor side of photosystem II Plant Physiol 2007 144, N 3:1336– 1346.
[30]
Hagio M., Gombos Z., Varkonyi Z., Masamoto K., Sato N., Tsuzuki M., Wada H. Direct evidence for requirement of phosphatidylglycerol in photosystem II of photosynthesis Plant Physiol 2000 124, N 2:795–804.
[31]
Weissenmayer B., Geiger O., Benning C. Disruption of a gene essential for sulfoquinovosyldiacylglycerol biosynthesis in Sinorhizobium meliloti has no detectable effect on root nodule symbiosis Mol. Plant-Microbe Interact 2000 13, N 6:666–672.
[32]
Hartel H., Essigmann B., Lokstein H., Hoffmann-Benning S., Peters-Kottig M., Benning C. The phospholipid-deficient pho1 mutant of Arabidopsis thaliana is affected in the organization, but not in the light acclimation, of the thylakoid membrane Biochim. Biophys. Acta 1998 1415, N 1 P. 205–218.
[33]
Kelly A., Dormann P. DGD2, an arabidopsis gene encoding a udp-galactose-dependent digalactosyldiacylglycerol synthase is expressed during growth under phosphate-limiting conditions J. Biol. Chem 2002 277, N 2:1166–1173.
[34]
Cruz-Ramirez A., Oropeza-Aburto A., Razo-Hernandez F., Ramirez-Chavez E., Herrera-Estrella L. Phospholipase DZ2 plays an important role in extraplastidic galactolipid biosynthesis and phosphate recycling in Arabidopsis roots Proc. Nat. Acad. Sci. USA 2006 103, N 17:6765–6770.
[35]
Jouhet J., Marechal E., Baldan B., Bligny R., Joyard J., Block M. A. Phosphate deprivation induces transfer of DGDG galactolipid from chloroplast to mitochondria J. Cell Biol 2004 167, N 5:863–874.
[36]
Yang W., Feng F.-Y., Hou H.-T., Jiang G.-Z., Xu Y.-N., Kuang T.-Y. Alternation in lipid composition of wheat leaves induced by phosphate deficiency is related to both lipid biosynthesis and phosphatidylglycerol degradation. Acta Bot. Sin. 2004; 46(2):211–215.
[37]
Li M., Welti R., Wang X. Quantitative profiling of Arabidopsis polar glycerolipids in response to phosphorus starvation. Roles of phospholipases Dz1 and Dz2 in phosphatidylcholine hydrolysis and digalactosyldiacylglycerol accumulation in phosphorus-starved plants Plant Physiol 2006 142, N 2 P. 750–761.
[38]
Andersson M. X., Larsson K. E., Tjellstrwm H., Liljenberg C., Sandelius A. S. Phosphate-limited oat. The plasma membrane and the tonoplast as major targets for phospholipid-toglycolipid replacement and stimulation of phospholipases in the plasma membrane J. Biol. Chem. 2005 280, N 30 P. 27578–27586.
[39]
Frentzen M. Phosphatidylglycerol and sulfoquinovosyldiacylglycerol: anionic membrane lipids and phosphate regulation Curr. Opin. Plant Biol 2004 7, N 3:270–276.