A Role for Diacylglycerol Acyltransferase during Leaf Senescence

Oxford University Press (OUP) - Tập 129 Số 4 - Trang 1616-1626 - 2002
Marianne T. Kaup1, Carol D. Froese1, John E. Thompson1
1Department of Biology, University of Waterloo, Waterloo, Ontario, Canada, N2L 3G1

Tóm tắt

Abstract Lipid analysis of rosette leaves from Arabidopsis has revealed an accumulation of triacylglycerol (TAG) with advancing leaf senescence coincident with an increase in the abundance and size of plastoglobuli. The terminal step in the biosynthesis of TAG in Arabidopsis is catalyzed by diacylglycerol acyltransferase 1 (DGAT1; EC 2.3.1.20). When gel blots of RNA isolated from rosette leaves at various stages of development were probed with the Arabidopsis expressed sequence tag clone, E6B2T7, which has been annotated as DGAT1, a steep increase in DGAT1 transcript levels was evident in the senescing leaves coincident with the accumulation of TAG. The increase in DGAT1 transcript correlated temporally with enhanced levels of DGAT1 protein detected immunologically. Two lines of evidence indicated that the TAG of senescing leaves is synthesized in chloroplasts and sequesters fatty acids released from the catabolism of thylakoid galactolipids. First, TAG isolated from senescing leaves proved to be enriched in hexadecatrienoic acid (16:3) and linolenic acid (18:3), which are normally present in thylakoid galactolipids. Second, DGAT1 protein in senescing leaves was found to be associated with chloroplast membranes. These findings collectively indicate that diacylglycerol acyltransferase plays a role in senescence by sequestering fatty acids de-esterified from galactolipids into TAG. This would appear to be an intermediate step in the conversion of thylakoid fatty acids to phloem-mobile sucrose during leaf senescence.

Từ khóa


Tài liệu tham khảo

Andersson, 2001, Chloroplast biogenesis: regulation of lipid transport to the thylakoid in chloroplasts isolated from expanding and fully expanded leaves of pea., Plant Physiol, 127, 184, 10.1104/pp.127.1.184

Awai, 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, 98, 10960, 10.1073/pnas.181331498

Bailey, 1963, The osmiophilic globules of chloroplasts: II. Globules of the spinach-beet chloroplast., Biochim Biophys Acta, 78, 163, 10.1016/0006-3002(63)91621-4

Bao, 1999, Supply of fatty acid is one limiting factor in the accumulation of triacylglycerol in developing embryos., Plant Physiol, 120, 1057, 10.1104/pp.120.4.1057

Bertrams, 1976, Experiments on enzymatic acylation of sn-glycerol 3-phosphate with enzyme preparations from pea and spinach leaves., Planta, 132, 161, 10.1007/BF00388898

Bligh, 1959, A rapid method of total lipid extraction and purification., Can J Biochem Physiol, 37, 911, 10.1139/o59-099

Browse, 1986, Fluxes through the prokaryotic and eukaryotic pathways of lipid synthesis in the ‘16:3′ plant Arabidopsis thaliana., Biochem J, 235, 25, 10.1042/bj2350025

Colas des Frans-Small, 1993, Identification of a major soluble protein in mitochondria from nonphotosynthetic tissues as NAD-dependent formate dehydrogenase., Plant Physiol, 102, 1171, 10.1104/pp.102.4.1171

Collawn, 1989, Production of antipeptide antibodies., Current Protocols in Molecular Biology on CD., 11.15.1

Davis, 1986, Basic Methods in Molecular Biology., 130, 10.1016/B978-0-444-01082-7.50040-0

De Bellis, 1990, Localization of glyoxylate-cycle marker enzymes in peroxisomes of senescent leaves and green cotyledons., Planta, 180, 435, 10.1007/BF01160401

Drenckhahn, 1993, Production of polyclonal antibodies against proteins and peptides., Methods in Cell Biology, 37, 7, 10.1016/S0091-679X(08)60242-3

El-Hafid, 1989, Enzymatic breakdown of polar lipids in cotton leaves under water stress: I. Degradation of monogalactosyl-diacylglycerol., Plant Physiol Biochem, 27, 495

Engelman-Silvestre, 1989, Changes in membrane phospholipids and galactolipids during the senescence of cut carnations: connection with ethylenic rise., Plant Physiol Biochem, 27, 931

Fairbanks, 1971, Coomassie blue R250 used in isopropanol-acetic acid., Biochemistry, 10, 2606, 10.1021/bi00789a030

Ghosh, 1988, Use of a scanning densitometer or an ELISA plate reader for measurement of nanogram amounts of protein in crude extracts from biological tissues., Anal Biochem, 169, 227, 10.1016/0003-2697(88)90278-3

Ghosh, 1994, Release of photosynthetic protein catabolites by blebbing from thylakoids., Plant Physiol, 106, 1547, 10.1104/pp.106.4.1547

Guiamét, 1999, Mass exodus from senescing soybean chloroplasts., Plant Cell Physiol, 40, 986, 10.1093/oxfordjournals.pcp.a029632

Harwood, 1972, Fat metabolism in higher plants: XLIX. Fatty acid biosynthesis by subcellular fractions of higher plants., Lipids, 7, 8, 10.1007/BF02531263

Himelblau, 2001, Nutrients mobilized from leaves of Arabidopsis thaliana during leaf senescence., J Plant Physiol, 158, 1317, 10.1078/0176-1617-00608

Hobbs, 1999, Cloning of a cDNA encoding diacylglycerol acyltransferase from Arabidopsis thaliana and its functional expression., FEBS Lett, 452, 145, 10.1016/S0014-5793(99)00646-8

Hobbs, 2000, Expression and characterization of diacylglycerol acyltransferase from Arabidopsis thaliana in insect cell cultures., Biochem Soc Trans, 28, 687, 10.1042/bst0280687

Hodges, 1974, Purification of a plasma membrane-bound adenosine triphosphatase from plant roots., Methods in Enzymology, 32, 392, 10.1016/0076-6879(74)32039-3

Huang, 1992, Oil bodies and oleosins in seeds., Annu Rev Plant Physiol Plant Mol Biol, 43, 177, 10.1146/annurev.pp.43.060192.001141

Huang, 1996, Oleosin and oil bodies in seeds and other organs., Plant Physiol, 110, 1055, 10.1104/pp.110.4.1055

Jako, 2001, Seed-specific over-expression of an Arabidopsis cDNA encoding a diacylglycerol acyltransferase enhances seed oil content and seed weight., Plant Physiol, 126, 861, 10.1104/pp.126.2.861

Katavic, 1995, Alteration of seed fatty acid composition by an ethyl methanesulfonate-induced mutation in Arabidopsis thaliana affecting diacylglycerol acyltransferase activity., Plant Physiol, 108, 399, 10.1104/pp.108.1.399

Kessler, 1999, Identification of proteins associated with plastoglobules isolated from pea (Pisum sativum L.) chloroplasts., Planta, 208, 107, 10.1007/s004250050540

Kim, 2001, Thermal inactivation kinetics and application of phospho-and galactolipid-degrading enzyme for evaluation of quality changes in frozen vegetables., J Agric Food Chem, 49, 2241, 10.1021/jf001379b

Kunst, 1998, Preparation of physiologically active chloroplasts from Arabidopsis., Methods in Molecular Biology: Arabidopsis Protocols., 43, 10.1385/0-89603-391-0:43

Kwanyuen, 1986, Isolation and purification of diacylglycerol acyltransferase from germinating soybean cotyledons., Biochim Biophys Acta, 877, 238, 10.1016/0005-2760(86)90300-0

Lacey, 1999, The accumulation of TAG within the endoplasmic reticulum of developing seeds of Helianthus annus., Plant J, 17, 397, 10.1046/j.1365-313X.1999.00387.x

Lardizabal, 2001, DGAT2 is a new diacylglycerol acyltransferase gene family., J Biol Chem, 276, 38862, 10.1074/jbc.M106168200

Lee, 2000, Membrane lipids: it’s only a phase., Curr Biol, 10, R377, 10.1016/S0960-9822(00)00477-2

Lichtenthaler, 1969, The plastoglobuli of spinach: their size, isolation and lipoquinone composition., Protoplasma, 68, 65, 10.1007/BF01247897

Lichtenthaler, 1970, the correlation between lipoquinone accumulation and plastoglobuli formation in the chloroplasts of Ficus elastica Roxb., Z Naturforsch, 25b, 619, 10.1515/znb-1970-0614

Martin, 1983, Properties of diacylglycerol acyltransferase from spinach leaves., Lipids, 18, 1, 10.1007/BF02534682

Martin, 1984, Subcellular localization of TAG synthesis in spinach leaves., Lipids, 19, 117, 10.1007/BF02534501

Matile, 1992, Chloroplast senescence., Crop Photosynthesis: Spatial and Temporal Determinants., 413, 10.1016/B978-0-444-89608-7.50025-3

Miquel, 1998, A new class of Arabidopsis mutants with reduced hexadecatrienoic acid fatty acid levels., Plant Physiol, 117, 923, 10.1104/pp.117.3.923

Miranda, 1993, Instantaneous blocking for immunoblots., Anal Biochem, 209, 376, 10.1006/abio.1993.1138

Morrison, 1964, Preparation of fatty acid methyl esters and dimethylacetals from lipids with boron fluoride-methanol., J Lipid Res, 5, 600, 10.1016/S0022-2275(20)40190-7

Peoples, 1980, Nitrogen redistribution during grain growth in wheat (Triticum aestivum L.): II. Chloroplast senescence and the degradation of ribulose-1,5-bisphosphate carboxylase., Planta, 149, 241, 10.1007/BF00384560

Post-Beittenmiller, 1996, Biochemistry and molecular biology of wax production in plants., Annu Rev Plant Physiol Plant Mol Biol, 47, 405, 10.1146/annurev.arplant.47.1.405

Pozueta-Romero, 1997, A ubiquitous plant housekeeping gene, PAP, encodes a major protein component of bell pepper chromoplasts., Plant Physiol, 115, 1185, 10.1104/pp.115.3.1185

Rey, 2000, Over-expression of a pepper plastid lipid-associated protein in tobacco leads to changes in plastid ultrastructure and plant development upon stress., Plant J, 21, 483, 10.1046/j.1365-313x.2000.00699.x

Routaboul, 1999, The TAG1 locus of Arabidopsis encodes for a diacylglycerol acyltransferase., Plant Physiol Biochem, 37, 831, 10.1016/S0981-9428(99)00115-1

Sakaki, 1990, Free fatty acids regulate two galactosyltransferases in chloroplast envelope membranes isolated from spinach leaves., Plant Physiol, 94, 781, 10.1104/pp.94.2.781

Sakaki, 1990, Pathway for the synthesis of triacylglycerols from monogalactosyldiacylglycerols in ozone-fumigated spinach leaves., Plant Physiol, 94, 773, 10.1104/pp.94.2.773

Sakaki, 1990, Conversion of monogalactosyldiacylglycerols to triacylglycerols in ozone-fumigated spinach leaves., Plant Physiol, 94, 766, 10.1104/pp.94.2.766

Sanchez, 1981, Synthesis of acyl CoAs by isolated spinach chloroplasts in relation to added CoA and ATP., Planta, 153, 519, 10.1007/BF00385535

Shimakata, 1982, Fatty ace synthetase of Spinacia oleracea leaves., Plant Physiol, 69, 1257, 10.1104/pp.69.6.1257

Siebertz, 1979, Characterization of lipids from chloroplast envelopes., Eur J Biochem, 101, 429, 10.1111/j.1432-1033.1979.tb19736.x

Smart, 1994, Gene expression during leaf senescence., New Phytol, 126, 419, 10.1111/j.1469-8137.1994.tb04243.x

Smith, 2000, Co-association of cytochrome f catabolites and plastid-lipid-associated protein with chloroplast lipid particles., Plant Physiol, 124, 211, 10.1104/pp.124.1.211

Sprey, 1966, Zur frage der beziehungen zwischen plastoglobuli und thylakoidgense in gertenkeimlingen., Z Naturforsch, 21b, 697, 10.1515/znb-1966-0717

Steinmüller, 1985, Composition and function of plastoglobuli: I. Isolation and purification from chloroplasts and chromoplasts., Planta, 163, 201, 10.1007/BF00393507

Steinmüller, 1985, Composition and function of plastoglobuli: II. Lipid composition of leaves and plastoglobuli during beech leaf senescence., Planta, 163, 91, 10.1007/BF00393507

Thompson, 1998, Lipid metabolism during plant senescence., Prog Lipid Res, 37, 119, 10.1016/S0163-7827(98)00006-X

Yao, 1991, Identification and characterization of nonsedementable lipid-protein microvesicles., Proc Natl Acad Sci USA, 88, 2269, 10.1073/pnas.88.6.2269

Young, 1976, Mixed function oxidase from germinating castor bean endosperm., Phytochemistry, 15, 379, 10.1016/S0031-9422(00)86827-2

Zou, 1999, The Arabidopsis thaliana TAG1 mutant has a mutation in a diacylglycerol acyltransferase gene., Plant J, 19, 645, 10.1046/j.1365-313x.1999.00555.x