Abstract
In higher plants, glycolipids such as monogalactosyldiacylglycerol (MGDG) and digalactosyldiacylglycerol (DGDG) are major components of chloroplast membranes in leaves. A recent study identified an isoform of MGDG synthase that is expressed specifically in floral organs, suggesting a novel function for glycolipids in flowers. To elucidate the localization and developmental changes of glycolipids and their biosynthetic activities in flowers; we carried out a series of analytical studies with Petunia hybrida. The results showed that the biosynthetic activities of galactolipid synthesis, particularly for DGDG, increased during flower development. Among the floral organs, the pistil had the highest galactolipid synthetic activity. Its specific activity for incorporation of UDP-galactose to yield galactolipids was estimated to be more than twice that of leaves, which are the major site of galactolipid synthesis in plant tissues. Analysis of lipid contents of pistils revealed that they contained higher amounts of galactolipids than other floral organs. Moreover, DGDG was more abundant than MGDG in both pistils and petals. These results show that DGDG is a major glycolipid in floral organs and that DGDG biosynthetic activity is highly upregulated in the pistils and petals of Petunia flowers.
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Abbreviations
- 16∶0:
-
palmitic acid
- 16∶1:
-
palmitoleic acid
- 18∶0:
-
stearic acid
- 18∶1:
-
oleic acid
- 18∶2:
-
litholeic acid
- 18∶3:
-
linolenic acid
- atMGD :
-
Arabidopsis thaliana MGDG synthase
- DGDG:
-
digalactosyldiacylglycerol
- MGDG:
-
monogalactosyldiacylglycerol
- PG:
-
phosphatidylglycerol
- SG:
-
sterylglycoside
- SQDG:
-
sulfoquinovosyldiacylglycerol
- TGDG:
-
trigalactosyldiacylglycerol
References
Block, M.A., Dorne, A.J., Joyard, J., and Douce R. (1983) Preparation and Characterization of Membrane Fractions Enriched in Outer and Inner Envelope Membranes from Spinach Chloroplasts. II—Biochemical Characterization, J. Biol. Chem. 258, 13281–13286.
Shimojima, M., Ohta, H., Iwamatsu, A., Masuda, T., Shioi, Y. and Takamiya, K. (1997) Cloning of the Gene for Monogalactosyldiacylglycerol Synthase and Its Evolutionary Origin, Proc. Natl. Acad. Sci. USA 94, 333–337.
Miège, C., Maréchal, E., Shimojima, M., Awai, K., Block, M.A., Ohta, H., Takamiya, K., Douce, R., and Joyard, J. (1999) Biochemical and Topological Properties of Type A MGD, a Spinach Chloroplast Envelope Enzyme Catalyzing the Synthesis of Both Prokaryotic and Eukaryotic MGDG, Eur. J. Biochem. 265, 1–13.
Dorne, A.J., Block, M.A., Joyard, J., and Douce, R. (1982) The Galactolipid:Galactolipid Galactosyltransferase Is Located on the Outer Surface of the Outer Membrane of the Chloroplast Envelope, FEBS Lett. 145, 30–34.
Heemskerk, J.W.M., Storz, T., Schmidt, R.R., and Heinz, E. (1990) Biosynthesis of Digalactosyldiacylglycerol in Plastids from 16∶3 and 18∶3 Plants, Plant Physiol. 93, 1286–1294.
Dörmann, P., Balbo, I., and Benning, C. (1999) Arabidopsis Galactolipid Biosynthesis and Lipid Trafficking Mediated by DGD1, Science 284, 2181–2184.
Kelly, A.A., and Dörmann, P. (2001) DGD2, an Arabidopsis Gene Encoding a UDP-Galactose Dependent Digalactosyldiacylglycerol Synthase Is Expressed During Growth Under Phosphate Limiting Conditions, J. Biol. Chem. 277, 1166–1173.
Awai, K., Maréchal, E., Block, M.A., Brun, D., Masuda, T., Shimada, H., Takamiya, K., Ohta, H., and Joyard, J. (2001) Two Types of MGDG Synthase Genes, Found Widely in Both 16∶3 and 18∶3 Plants, Differentially Mediate Galactolipid Syntheses in Photosynthetic and Nonphotosynthetic Tissues in Arabidopsis thaliana, Proc. Natl. Acad. Sci. USA 98, 10960–10965.
Camara, B., Bardat, F., Dogbo, O., Brangeon, J., and Monéger, R. (1983) Terpenoid Metabolism in Plastids. Isolation and Biochemical Characteristics of Capsicum annuum Chromoplasts, Plant Physiol. 3, 94–99.
Kleinig, H., and Liedvogel, B. (1978) Fatty Acid Synthesis by Isolated Chromoplasts from the Daffodil, Eur. J. Biochem. 83, 499–505.
Alban, C., Joyard, J., and Douce, R. (1988) Preparation and Characterization of Envelope Membrane from Nongreen Plastids, Plant Physiol. 88, 709–717.
Bligh, E.G., and Dyer, W.J. (1959) A Rapid Method of Total Lipid Extraction and Purification, Can. J. Biochem. Physiol. 37, 911–917.
Dittmer, J.C., and Lester, R.L. (1964) A Simple, Specific Spray for the Detection of Phospholipids on Thin-Layer Chromatograms, J. Lipid Res. 5, 126–127.
Radin, N.S., Lavin, F.B., and Brown, J.R. (1955) Determination of Cerebrosides, J. Biol. Chem. 217, 789–796.
Zlatkis, A., Zak, B., and Boyle, A.J. (1952) A New Method for the Direct Determination of Serum Cholesterol, J. Lab. Clin. Med. 41, 486–492.
Tian, R.H., Ohmura, E., Matsui, M., and Nohara, T. (1997) Abutiloside A, a 26-Acylamino-3β, 16α-dihydroxy-5α-cholesta-22-one Glycoside from Solanum abutiloides, Phytochemistry 44, 723–726.
Bensadoun, A., and Weinstein, D. (1976) Assay of Proteins in the Presence of Interfering Materials, Anal. Biochem. 70, 241–250.
Murphy, D.J. (1982) The Importance of Non-planar Bilayer Regions in Photosynthetic Membranes and Their Stabilisation by Galactolipids, FEBS Lett. 150, 19–26.
Warnecke, D.C., and Heinz, E. (1994) Purification of a Membrane-Bound UDP-Glucose:Sterol β-d-Glucosyltransferase Based on Its Solubility in Diethylether, Plant Physiol. 105, 1067–1073.
Jordan, P., Fromme, P., Witt, H.T., Klukas, O., Saenger, W., and Krau, N. (2001) Three-Dimensional Structure of Cyanobacterial Photosystem I at 2.5 Å Resolution, Nature 411, 909–917.
Jarvis, P., Dörmann, P., Peto, C.A., Lutes, J., Benning, C., and Chory, J. (2000) Galactolipid Deficiency and Abnormal Chloroplast Development in the Arabidopsis MGD synthase 1 Mutant, Proc. Natl. Acad. Sci. USA 97, 8175–8179.
Dörmann, P., Hoffmann-Benning, S., Balbo, I., and Benning C. (1995) Isolation and Characterization of an Arabidopsis Mutant Deficient in the Thylakoid Lipid Digalactosyl Diacylglycerol, Plant Cell 7, 1801–1810.
Dörmann, P., and Benning, C. (2002) Galactolipids Rule in Seed Plants, Trends Plant Sci. 7, 112–118.
Xu, C., Fan, J., Riekhof, W., Froehlich, J.E., and Benning, C. (2003) A Permease-like Protein Involved in ER to Thylakoid Lipid Transfer in Arabidopsis, EMBO J. 22, 2370–2379.
Härtel, H., Dörmann, P., and Benning, C. (2000). DGD1-Independent Biosynthesis of Extraplastidic Galactolipids Following Phosphate Deprivation in Arabidopsis, Proc. Natl. Acad. Sci. USA 97, 10649–10654.
Gad, M., Awai, K., Shimojima, M., Yamaryo, y., Shimada, H., Masuda, T., Takamiya, K., Ikai, A., and Ohta, H. (2001) Accumulation of Plant Galactolipid Affects Cell Morphology of Escherichia coli, Biochem. Biophys. Res. Commun. 286, 114–118.
Andersson, M.X., Stridh, M.H., Larsson, K.E., Liljenberg, C., and Sandelius, A.S. (2003) Phosphate-Deficient Oat Replaces a Major Portion of the Plasma Membrane Phospholipids with the Galactolipid Digalactosyldiacylglycerol, FEBS Lett. 537, 128–132.
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Nakamura, Y., Arimitsu, H., Yamaryo, Y. et al. Digalactosyldiacylglycerol is a major glycolipid in floral organs of Petunia hybrida . Lipids 38, 1107–1112 (2003). https://doi.org/10.1007/s11745-006-1166-x
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DOI: https://doi.org/10.1007/s11745-006-1166-x