Kelly, Amélie A., Quettier, Anne-Laure, Shaw, Eve and Eastmond, Peter J.. (2011) Seed storage oil mobilization is important but not essential for germination or seedling establishment in Arabidopsis. Plant Physiology, Vol.157 (No.2). pp. 866-875. ISSN 0032-0889

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Abstract

Triacylglycerol (TAG) is a major storage reserve in many plant seeds. We previously identified a TAG lipase mutant called sugar-dependent1 (sdp1) that is impaired in TAG hydrolysis following Arabidopsis (Arabidopsis thaliana) seed germination (Eastmond, 2006). The aim of this study was to identify additional lipases that account for the residual TAG hydrolysis observed in sdp1. Mutants were isolated in three candidate genes (SDP1-LIKE [SDP1L], ADIPOSE TRIGLYCERIDE LIPASELIKE, and COMPARATIVE GENE IDENTIFIER-58-LIKE). Analysis of double, triple, and quadruple mutants showed that SDP1L is responsible for virtually all of the residual TAG hydrolysis present in sdp1 seedlings. Oil body membranes purified from sdp1 sdp1L seedlings were deficient in TAG lipase activity but could still hydrolyze di- and monoacylglycerol. SDP1L is expressed less strongly than SDP1 in seedlings. However, SDP1L could partially rescue TAG breakdown in sdp1 seedlings when expressed under the control of the SDP1 or 35S promoters and in vitro assays showed that both SDP1 and SDP1L can hydrolyze TAG, in preference to diacylglycerol or monoacylglycerol. Seed germination was slowed in sdp1 sdp1L and postgerminative seedling growth was severely retarded. The frequency of seedling establishment was also reduced, but sdp1 sdp1L was not seedling lethal under normal laboratory growth conditions. Our data show that together SDP1 and SDP1L account for at least 95% of the rate of TAG hydrolysis in Arabidopsis seeds, and that this hydrolysis is important but not essential for seed germination or seedling establishment.

Item Type:	Journal Article
Subjects:	Q Science > QK Botany
Divisions:	Faculty of Science > Life Sciences (2010- )
Library of Congress Subject Headings (LCSH):	Arabidopsis -- Genetics, Arabidopsis -- Seeds, Germination -- Physiological aspects
Journal or Publication Title:	Plant Physiology
Publisher:	American Society of Plant Biologists
ISSN:	0032-0889
Date:	August 2011
Volume:	Vol.157
Number:	No.2
Page Range:	pp. 866-875
Identification Number:	10.1104/pp.111.181784
Status:	Peer Reviewed
Publication Status:	Published
Access rights to Published version:	Open Access
Funder:	Biotechnology and Biological Sciences Research Council (Great Britain) (BBSRC)
Grant number:	BB/E022197/1 (BBSRC)
References:	Adham AR, Zolman BK, Millius A, Bartel B (2005) Mutations in Arabidopsis acyl-CoA oxidase genes reveal distinct and overlapping roles in beta-oxidation. Plant J 41: 859–874 Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, et al (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653–657 Athenstaedt K, Daum G (2003) YMR313c/TGL3 encodes a novel triacylglycerol lipase located in lipid particles of Saccharomyces cerevisiae. J Biol Chem 278: 23317–23323 Athenstaedt K, Daum G (2005) Tgl4p and Tgl5p, two triacylglycerol lipases of the yeast Saccharomyces cerevisiae are localized to lipid particles. J Biol Chem 280: 37301–37309 Baker A, Graham IA, Holdsworth M, Smith SM, Theodoulou FL (2006) Chewing the fat: b-oxidation in signalling and development. Trends Plant Sci 11: 124–132 Baud S, Boutin J-P, Miquel M, Lepiniec L, Rochat C (2002) An integrated overview of seed development in Arabidopsis thaliana ecotype Ws. Plant Physiol Biochem 40: 151–160 Bewley JD, Black M (1994) Seeds. Physiology of Development and Germination, Ed 2. Plenum Press, New York Browse J, McCourt PJ, Somerville CR (1986) Fatty acid composition of leaf lipids determined after combined digestion and fatty acid methyl ester formation from fresh tissue. Anal Biochem 152: 141–145 Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium- mediated transformation of Arabidopsis thaliana. Plant J 16: 735–743 Cornah JE, Germain V, Ward JL, Beale MH, Smith SM (2004) Lipid utilization, gluconeogenesis, and seedling growth in Arabidopsis mutants lacking the glyoxylate cycle enzyme malate synthase. J Biol Chem 279: 42916–42923 Dave AM, Herna´ndezML, He Z, Andriotis VME, Vaistij FE, Larson TR, Graham IA (2011) 12-Oxo-phytodienoic acid accumulation during seed development represses seed germination in Arabidopsis. Plant Cell 23: 583–599 Eastmond PJ (2004) Glycerol-insensitive Arabidopsis mutants: gli1 seedlings lack glycerol kinase, accumulate glycerol and are more resistant to abiotic stress. Plant J 37: 617–625 Eastmond PJ (2006) SUGAR-DEPENDENT1 encodes a patatin domain triacylglycerol lipase that initiates storage oil breakdown in germinating Arabidopsis seeds. Plant Cell 18: 665–675 Eastmond PJ, Germain V, Lange PR, Bryce JH, Smith SM, Graham IA (2000) Postgerminative growth and lipid catabolism in oilseeds lacking the glyoxylate cycle. Proc Natl Acad Sci USA 97: 5669–5674 El-Kouhen K, Blangy S, Ortiz E, Gardies AM, Ferte´ N, Arondel V (2005) Identification and characterization of a triacylglycerol lipase in Arabidopsis homologous to mammalian acid lipases. FEBS Lett 579: 6067–6073 Feussner I, Ku¨hn H, Wasternack C (2001) Lipoxygenase-dependent degradation of storage lipids. Trends Plant Sci 6: 268–273 Footitt S, Dietrich D, Fait A, Fernie AR, Holdsworth MJ, Baker A, Theodoulou FL (2007) The COMATOSE ATP-binding cassette transporter is required for full fertility in Arabidopsis. Plant Physiol 144: 1467–1480 Footitt S, Slocombe SP, Larner V, Kurup S, Wu Y, Larson T, Graham I, Baker A, Holdsworth M (2002) Control of germination and lipid mobilization by COMATOSE, the Arabidopsis homologue of human ALDP. EMBO J 21: 2912–2922 Gallardo K, Le Signor C, Vandekerckhove J, Thompson RD, Burstin J (2003) Proteomics of Medicago truncatula seed development establishes the time frame of diverse metabolic processes related to reserve accumulation. Plant Physiol 133: 664–682 Ghosh AK, Chauhan N, Rajakumari S, Daum G, Rajasekharan R (2009) At4g24160, a soluble acyl-coenzyme A-dependent lysophosphatidic acid acyltransferase. Plant Physiol 151: 869–881 Ghosh AK, Ramakrishnan G, Chandramohan C, Rajasekharan R (2008a) CGI-58, the causative gene for Chanarin-Dorfman syndrome, mediates acylation of lysophosphatidic acid. J Biol Chem 283: 24525–24533 Ghosh AK, Ramakrishnan G, Rajasekharan R (2008b) YLR099C (ICT1) encodes a soluble Acyl-CoA-dependent lysophosphatidic acid acyltransferase responsible for enhanced phospholipid synthesis on organic solvent stress in Saccharomyces cerevisiae. J Biol Chem 283: 9768–9775 Graham IA (2008) Seed storage oil mobilization. Annu Rev Plant Biol 59: 115–142 Gro¨nke S, Mildner A, Fellert S, Tennagels N, Petry S,Mu¨ ller G, Ja¨ckle H, Ku¨ hnlein RP (2005) Brummer lipase is an evolutionary conserved fat storage regulator in Drosophila. Cell Metab 1: 323–330 James CN, Horn PJ, Case CR, Gidda SK, Zhang D, Mullen RT, Dyer JM, Anderson RG, Chapman KD (2010) Disruption of the Arabidopsis CGI- 58 homologue produces Chanarin-Dorfman-like lipid droplet accumulation in plants. Proc Natl Acad Sci USA 107: 17833–17838 Kim HU, Hsieh K, Ratnayake C, Huang AH (2002) A novel group of oleosins is present inside the pollen of Arabidopsis. J Biol Chem 277: 22677–22684 Kurat CF, Natter K, Petschnigg J, Wolinski H, Scheuringer K, Scholz H, Zimmermann R, Leber R, Zechner R, Kohlwein SD (2006) Obese yeast: triglyceride lipolysis is functionally conserved from mammals to yeast. J Biol Chem 281: 491–500 Lass A, Zimmermann R, Haemmerle G, Riederer M, Schoiswohl G, Schweiger M, Kienesberger P, Strauss JG, Gorkiewicz G, Zechner R (2006) Adipose triglyceride lipase-mediated lipolysis of cellular fat stores is activated by CGI-58 and defective in Chanarin-Dorfman syndrome. Cell Metab 3: 309–319 Lemieux B, Miquel M, Somerville C, Browse J (1990) Mutants of Arabidopsis with alterations in seed lipid fatty-acid composition. Theor Appl Genet 80: 234–240 Li-Beisson Y, Shorrosh B, Beisson F, Andersson M, Arondel V, Bates PD, Baud S, Bird D, DeBono A, Durrett TP, et al (2010) Acyl-lipid metabolism. In R Last, ed, The Arabidopsis Book. American Society of Plant Biologists, Rockville, MD, pp 1–65 Lin YH, Huang AHC (1983) Lipase in lipid bodies of cotyledons of rape and mustard seedlings. Arch Biochem Biophys 225: 360–369 Montero-MoranG, Caviglia JM,McMahonD, RothenbergA, Subramanian V, Xu Z, Lara-Gonzalez S, Storch J, Carman GM, Brasaemle DL (2010) CGI- 58/ABHD5 is a coenzyme A-dependent lysophosphatidic acid acyltransferase. J Lipid Res 51: 709–719 Penfield S, Rylott EL, Gilday AD, Graham S, Larson TR, Graham IA (2004) Reserve mobilization in the Arabidopsis endosperm fuels hypocotyl elongation in the dark, is independent of abscisic acid, and requires PHOSPHOENOLPYRUVATE CARBOXYKINASE1. Plant Cell 16: 2705–2718 Quettier AL, Eastmond PJ (2009) Storage oil hydrolysis during early seedling growth. Plant Physiol Biochem 47: 485–490 Rajakumari S, Daum G (2010a) Janus-faced enzymes yeast Tgl3p and Tgl5p catalyze lipase and acyltransferase reactions. Mol Biol Cell 21: 501–510 Rajakumari S, Daum G (2010b) Multiple functions as lipase, steryl ester hydrolase, phospholipase, and acyltransferase of Tgl4p from the yeast Saccharomyces cerevisiae. J Biol Chem 285: 15769–15776 Rodrı´guez-Garcı´a MI, M’rani-Alaoui M, Ferna´ndez MC (2003) Behavior of storage lipids during development and germination of olive (Olea europaea L.) pollen. Protoplasma 221: 237–244 Roudier F, Gissot L, Beaudoin F, Haslam R, Michaelson L, Marion J, Molino D, Lima A, Bach L, Morin H, et al (2010) Very-long-chain fatty acids are involved in polar auxin transport and developmental patterning in Arabidopsis. Plant Cell 22: 364–375 Smirnova E, Goldberg EB, Makarova KS, Lin L, Brown WJ, Jackson CL (2006) ATGL has a key role in lipid droplet/adiposome degradation in mammalian cells. EMBO Rep 7: 106–113 Thimm O, Bla¨sing O, Gibon Y, Nagel A, Meyer S, Kru¨ ger P, Selbig J, Mu¨ ller LA, Rhee SY, Stitt M (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37: 914–939 Winter D, Vinegar B, Hardeep N, Ammar R,Wilson GV, Provart NJ (2007) An “Electronic Fluorescent Pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS ONE 2: e718 Wu Y, Llewellyn DJ, Dennis ES (2002) A quick and easy method for isolating good quality RNA from cotton (Gossypium hirsutum L.) tissues. Plant Mol Biol Rep 20: 213–218 Xu C, Fan J, Froehlich JE, Awai K, Benning C (2005) Mutation of the TGD1 chloroplast envelope protein affects phosphatidate metabolism in Arabidopsis. Plant Cell 17: 3094–3110 Zhang M, Fan J, Taylor DC, Ohlrogge JB (2009) DGAT1 and PDAT1 acyltransferases have overlapping functions in Arabidopsis triacylglycerol biosynthesis and are essential for normal pollen and seed development. Plant Cell 21: 3885–3901 Zechner R, Kienesberger PC, Haemmerle G, Zimmermann R, Lass A (2009) Adipose triglyceride lipase and the lipolytic catabolism of cellular fat stores. J Lipid Res 50: 3–21 Zimmermann R, Strauss JG, Haemmerle G, Schoiswohl G, Birner- Gruenberger R, Riederer M, Lass A, Neuberger G, Eisenhaber F, Hermetter A, et al (2004) Fat mobilization in adipose tissue is promoted by adipose triglyceride lipase. Science 306: 1383–1386 Zolman BK, Silva ID, Bartel B (2001) The Arabidopsis pxa1 mutant is defective in an ATP-binding cassette transporter-like protein required for peroxisomal fatty acid beta-oxidation. Plant Physiol 127: 1266–1278
URI:	http://wrap.warwick.ac.uk/id/eprint/38842

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