Arabidopsis AtGPAT1, a member of the membrane-bound glycerol-3-phosphate acyltransferase gene family, is essential for tapetum differentiation and male fertility

Plant Cell

Volumn 15, Issue 8, 2003, Pages 1872-1887

  Zheng, Zhifu ^a   Xia, Qun ^a   Dauk, Melanie ^a   Shen, Wenyun ^a   Selvaraj, Gopalan ^a   Zou, Jitao ^a  

^a NATIONAL RESEARCH COUNCIL CANADA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BIOSYNTHESIS; GLYCEROL; MICROSCOPIC EXAMINATION; TISSUE;

SPOROPHYTIC EFFECTS;

GENES;

ARABIDOPSIS; BACTERIA (MICROORGANISMS); EMBRYOPHYTA; EUKARYOTA;

EID: 0042922465     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.012427     Document Type: Article

References (66)

1. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. (1990). Basic local alignment search tool. J. Mol. Biol. 215, 403-410.
2. Athenstaedt, K., and Daum, G. (1999). Phosphatidic acid, a key intermediate in lipid metabolism. Eur. J. Biochem. 266, 1-16.
3. Bafor, M., Stobart, A.K., and Stymne, S. (1990). Properties of the glycerol acylating enzyme in microsomal preparations from the developing seeds of safflower (Carthamus tinctorius) and turnip rape (Brassica campestris) and their ability to assemble cocoa-butter type fats. J. Am. Oil Chem. Soc. 67, 217-225.
4. Balk, J., and Leaver, C.J. (2001). The PET1-CMS mitochondrial mutation in sunflower is associated with premature programmed cell death and cytochrome c release. Plant Cell 13, 1803-1818.
5. Bligh, E.G., and Dyer, W.J. (1959). A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911-917.
6. Browse, J., Warwick, N., Somerville, C.R., and Slack, C.R. (1986). Fluxes through the prokaryotic and eukaryotic pathways of lipid synthesis in the 16:3 plant Arabidopsis thaliana. Biochem. J. 235, 25-31.
7. Chourey, P.S., and Taliercio, E.W. (1994). Epistatic interaction and functional compensation between the two tissue- and cell-specific sucrose synthase genes in maize. Proc. Natl. Acad. Sci. USA 91, 7917-7921.
8. Christensen, C.A., Gorsich, S.W., Brown, R.H., Jones, L.G., Brown, J., Shaw, J.M., and Drews, G.N. (2002). Mitochondrial GFA2 is required for synergid cell death in Arabidopsis. Plant Cell 14, 2215-2232.
9. Cleary, S.P., Tan, F-C., Nakrieko, K-A., Thompson, S.J., Mullineaux, P.M., Creissen, G.P., von Stedingk, E., Glaser, E., Smith, A.G., and Robinson, C. (2002). Isolated plant mitochondria import chloroplast precursor proteins in vitro with the same efficiency as chloroplasts. J. Biol. Chem. 277, 5562-5569.
10. Datla, R.S., Hammerlindl, J.K., Panchuk, B., Pelcher, L.E., and Keller, W. (1992). Modified binary plant transformation vectors with the wild-type gene encoding NPTII. Gene 122, 383-384.
11. Dircks, L., and Sul, H.S. (1999). Acyltransferases of de novo glycero-phospholipid biosynthesis. Prog. Lipid Res. 38, 461-479.
12. Dörmann, P., Voelker, T.A., and Ohlrogge, J.B. (2000). Accumulation of palmitate in Arabidopsis mediated by the acyl-acyl carrier protein thioesterase FATB1. Plant Physiol. 123, 637-643.
13. Eccleston, V., and Harwood, J.L. (1992). Glycerol 3-phosphate acylation by microsomal fractions from avocado mesocarp. Biochem. Soc. Trans. 20, 169S.
14. Eccleston, V., and Harwood, J.L. (1995). Solubilization, partial purification and properties of acyl-CoA:glycerol-3-phosphate acyltransferase from avocado (Persea americana) fruit mesocarp. Biochim. Biophys. Acta 1257, 1-10.
15. Enjuto, M., Balcells, L., Campos, N., Caelles, C., Arro, M., and Boronat, A. (1994). Arabidopsis thaliana contains two differentially expressed 3-hydroxy-3-methylglutaryl-CoA reductase genes, which encode microsomal forms of the enzyme. Proc. Natl. Acad. Sci. USA 91, 927-931.
16. Ferreira, M.A., de Almeida Engler, J., Miguens, F.C., van Montagu, M., Engler, G., and de Oliveira, D.E. (1997). Oleosin gene expression in Arabidopsis thaliana tapetum coincides with accumulation of lipids in plastids and cytoplasmic bodies. Plant Physiol. Biochem. 35, 729-739.
17. Focks, N., and Benning, C. (1998). wrinkled1: A novel, low-seed-oil mutant of Arabidopsis with a deficiency in the seed-specific regulation of carbohydrate metabolism. Plant Physiol. 118, 91-101.
18. Frentzen, M. (1990). Comparison of certain properties of membrane bound and solubilized acyltransferase activities of plant microsomes. Plant Sci. 69, 39-48.
19. Frentzen, M. (1993). Acyltransferases and triacylglycerols. In Lipid Metabolism in Plants, T.S. Moore, Jr., ed (Boca Raton, FL: CRC Press), pp. 195-220.
20. Fritz, P.J., Kauffman, J.M., Robertson, C.A., and Wilson, M.R. (1986). Cocoa butter biosynthesis, purification and characterization of a soluble sn-glycerol-3-phosphate acyltransferase from cocoa seeds. J. Biol. Chem. 261, 194-199.
21. Fujiki, Y., Hubbard, A.L., Fowler, S., and Lazarow, P.B. (1982). Isolation of intracellular membranes by means of sodium carbonate treatment: Application to endoplasmic reticulum. J. Cell Biol. 93, 97-102.
22. Grant, I., Beversdorf, W.D., and Peterson, R.L. (1986). A comparative light and electron microscopic study of microspore and tapetal development in male fertile and cytoplasmic sterile oilseed rape (Brassica napus). Can. J. Bot. 64, 1055-1068.
23. Griffiths, G., Stobart, A.K., and Stymne, S. (1985). The acylation of sn-glycerol-3-phosphate and the metabolism of phosphatidate in microsomal preparations from the developing cotyledons of safflower (Carthamus tinctorius L.) seed. Biochem. J. 230, 379-388.
24. Hares, W., and Frentzen, M. (1991). Substrate specificities of the membrane-bound and partially purified microsomal acyl-CoA:1-acylglycerol-3-phosphate acyltransferase from etiolated shoots of Pisum sativum (L.). Planta 185, 124-131.
25. Heinz, E., and Roughan, P.G. (1983). Similarities and differences in lipid metabolism of chloroplasts isolated from 18:3 and 16:3 plants. Plant Physiol. 72, 273-279.
26. Hernandez-Pinzon, I., Ross, J.H.E., Barnes, K.A., Damant, A.P., and Murphy, D.J. (1999). Composition and role of tapetal lipid bodies in the biogenesis of the pollen coat of Brassica napus. Planta 208, 588-598.
27. Hofmann, K., and Stoffel, W. (1993). Tmbase: A database of membrane spanning protein segments. Biol. Chem. Hoppe-Seyler 374,166.
28. Horner, H.T. (1977). A comparative light- and electron-microscopic study of microsporogenesis in male-fertile and cytoplasmic male-sterile sunflower (Helianthus annuus). Am. J. Bot. 64, 745-759.
29. Ichihara, K. (1984). sn-Glycerol-3-phosphate acyltransferase in a particulate fraction from maturing safflower seeds. Arch. Biochem. Biophys. 232, 685-698.
30. Jones, A.M. (2000). Does the plant mitochondrion integrate cellular stress and regulate programmed cell death? Trends Plant Sci. 5, 225-230.
31. Kannan, L., Knudsen, J., and Jolly, C.A. (2003). Aging and acyl-CoA binding protein alter mitochondrial glycerol-3-phosphate acyltransferase activity. Biochim. Biophys. Acta 1631, 12-16.
32. Katavić, V., Reed, D.W., Taylor, D.C., Giblin, E.M., Barton, D.L., Zou, J., MacKenzie, S.L., Covello, P.S., and Kunst, L. (1995). Alteration of seed fatty acid composition by an ethyl methanesulfonate-induced mutation in Arabidopsis thaliana affecting diacylglycerol acyltransferase activity. Plant Physiol. 108, 399-409.
33. Knutzon, D.S., Hayes, T.R., Wyrick, A., Xiong, H., Davis, H.M., and Voelker, T.A. (1999). Lysophosphatidic acid acyltransferase from coconut endosperm mediates the insertion of laurate at the sn-2 position of triacylglycerols in lauric rapeseed oil and can increase total laurate levels. Plant Physiol. 120, 739-746.
34. Knutzon, D.S., Lardizabal, K.D., Nelsen, J.S., Bleibaum, J.L., Davis, H.M., and Metz, J.G. (1995). Cloning of a coconut endosperm cDNA encoding a 1-acyl-sn-glycerol-3-phosphate acyltransferase that accepts medium-chain-length substrates. Plant Physiol. 109, 999-1006.
35. Kunst, L., Browse, J., and Somerville, C. (1988). Altered regulation of lipid biosynthesis in a mutant Arabidopsis deficient in chloroplast glycerol-3-phosphate acyltransferase activity. Proc. Natl. Acad. Sci. USA 85, 4143-4147.
36. Lessner, M.W., Levering, C.K., Davids, H.M., and Knutzon, D.S. (1995). Lysophosphatidic acid acyltransferase from meadowform mediates insertion of erucic acid at the sn-2 position of triacylglycerol in transgenic rapeseed oil. Plant Physiol. 109, 1389-1394.
37. Lewin, T.M., Wang, P., and Coleman, R.A. (1999). Analysis of amino acid motifs diagnostic for the sn-glycerol-3-phosphate acyltransferase reaction. Biochemistry 38, 5764-5771.
38. Manaf, A.M., and Harwood, J.L. (2000). Purification and characterization of acyl-CoA:glycerol 3-phosphate acyltransferase from oil palm (Elaeis guineensis) tissues. Planta 210, 318-328.
39. Mouline, K., Very, A.A., Gaymard, F., Boucherez, J., Pilot, G., Devic, M., Bouchez, D., Thibaud, J.B., and Sentenac, H. (2002). Pollen tube development and competitive ability are impaired by disruption of a Shaker K(+) channel in Arabidopsis. Genes Dev. 16, 339-350.
40. Murgia, M., Charzynska, M., Rougier, M., and Cresti, M. (1991). Secretory tapetum of Brassica oleracea L.: Polarity and ultrastructural features. Sex. Plant Reprod. 4, 28-35.
41. Murphy, D.J., and Vance, J. (1999). Mechanisms of lipid-body formation. Trends Biochem. Sci. 24, 109-115.
42. Overman, M.A., and Warmke, H.E. (1972). Cytoplasmic male sterility in sorghum. II. Tapetal behaviour in fertile and sterile anthers. J. Hered. 63, 227-234.
43. Owen, H.A., and Makaroff, C.A. (1995). Ultrastructure of microsporogenesis and microgametogenesis in Arabidopsis thaliana (L.) Heynh. ecotype Wassilewskija (Brassicaceae). Protoplasma 185, 7-21.
44. Pacini, E., Franchi, G., and Hesse, M. (1985). The tapetum: Its form, function, and possible phylogeny in Embryophyta. Plant Syst. Evol. 149, 155-185.
45. Papini, A., Mosti, S., and Brighigna, L. (1999). Programmed-cell-death events during tapetum development of angiosperms. Protoplasma 207, 213-221.
46. Piffanelli, P., Ross, J.H.E., and Murphy, D.U. (1997). Intra- and extracellular lipid composition and associated gene expression patterns during pollen development in Brassica napus. Plant J. 11, 549-562.
47. Piffanelli, P., Ross, J.H.E., and Murphy, D.U. (1998). Biogenesis and function of the lipidic structures of pollen grains. Sex. Plant Reprod. 11, 65-80.
48. Platt, K.A., Huang, A.H.C., and Thomson, W.W. (1998). Ultrastructural study of lipid accumulation in tapetal cells of Brassica napus L. cv. Westar during microsporogenesis. Int. J. Plant Sci. 159, 724-737.
49. Roughan, P.G., and Slack, C.R. (1982). Cellular organization of glycerolipid metabolism. Annu. Rev. Plant Physiol. 33, 97-132.
50. Routaboul, J.M., Benning, C., Bechtold, N., Caboche, M., and Lepiniec, L. (1999). The TAG1 locus of Arabidopsis encodes for a diacylglycerol acyltransferase. Plant Physiol. Biochem. 37, 831-840.
51. Scheideier, M.A., and Bell, R.M. (1989). Phospholipid dependence of homogeneous, reconstituted sn-glycerol-3-phosphate acyltransferase of Escherichia coli. J. Biol. Chem. 264, 12455-12461.
52. Schnable, P.S., and Wise, R.P. (1998). The molecular basis of cytoplasmic male sterility and fertility restoration. Trends Plant Sci. 3, 175-210.
53. Schrauwen, J.A.M., Mettenmeyer, T., Croes, A.F., and Wullems, G.J. (1996). Tapetum-specific genes: What role do they play in male gametophyte development? Acta Bot. Neerl. 45, 1-15.
54. Shen, W., Wei, Y., Dauk, M., Zheng, Z., and Zou, J. (2003). Identification of a mitochondrial glycerol-3-phosphate dehydrogenase from Arabidopsis thaliana: Evidence for a mitochondrial glycerol-3-phosphate shuttle in plants. FEBS Lett. 536, 92-96.
55. Sun, C., Cao, Y.Z., and Huang, A.H.C. (1988). Acyl coenzyme A preference of the glycerol phosphate pathway in the microsomes from the maturing seeds of palm, maize and rapeseed. Plant Physiol. 88, 56-60.
56. Sussman, M.R., Amasino, R.M., Young, U.C., Krysan, P.J., and Austin-Phillips, S. (2000). The Arabidopsis Knockout Facility at the University of Wisconsin-Madison. Plant Physiol. 124, 1465-1467.
57. Uemura, M., Joseph, R.A., and Steponkus, P.L. (1995). Cold acclimation of Arabidopsis thaliana: Effect on plasma membrane lipid composition and freeze-induced lesions. Plant Physiol. 109, 15-30.
58. von Heijne, G. (1992). Membrane protein structure prediction, hydrophobicity analysis and the positive-inside rule. J. Mol. Biol. 225, 487-494.
59. Wilkison, W.O., and Bell, R.M. (1997). sn-Glycerol-3-phosphate acyltransferase from Escherichia coli. Biochim. Biophys. Acta 1348, 3-9.
60. Wu, H.M., and Cheung, A.Y. (2000). Programmed cell death in plant reproduction. Plant Mol. Biol. 44, 267-281.
61. Yet, S.-H., Lee, S., Hahm, Y.T., and Sul, H.S. (1993). Expression and identification of p90 as the murine mitochondrial glycerol-3-phosphate acyltransferase. Biochemistry 32, 9486-9491.
62. Zenkteler, M. (1962). Microsporogenesis and tapetal development in normal and male sterile carrots (Daucus carota). Am. J. Bot. 49, 341-348.
63. Zheng, Z., Uchacz, T.M., and Taylor, J.L. (2001). Isolation and characterization of novel defence-related genes induced by copper, salicylic acid, methyl jasmonate, abscisic acid and pathogen infection in Brassica carinata. Mol. Plant Pathol. 2, 159-169.
64. Zheng, Z., and Zou, J. (2001). The initial step of the glycerolipid pathway: Identification of glycerol 3-phosphate/dihydroxyacetone phosphate dual substrate acyltransferases in Saccharomyces cerevisiae. J. Biol. Chem. 276, 41710-41716.
65. Zou, J., Katavić, V., Giblin, E.M., Barton, D.L., Mackenzie, S.L., Keller, W.A., Hu, X., and Taylor, D.C. (1997). Modification of seed oil content and acyl composition in the Brassicaceae by expression of a yeast sn-2 acyltransferase gene. Plant Cell 9, 909-923.
66. Zou, J., Wei, Y., Jako, C., Kumar, A., Selvaraj, G., and Taylor, D.C. (1999). The Arabidopsis thaliana TAG1 mutant has a mutation in a diacylglycerol acyltransferase gene. Plant J. 19, 645-653.