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Deciphering the roles of acyl-CoA-binding proteins in plant cells

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Abstract

Lipid trafficking is vital for metabolite exchange and signal communications between organelles and endomembranes. Acyl-CoA-binding proteins (ACBPs) are involved in the intracellular transport, protection, and pool formation of acyl-CoA esters, which are important intermediates and regulators in lipid metabolism and cellular signaling. In this review, we highlight recent advances in our understanding of plant ACBP families from a cellular and developmental perspective. Plant ACBPs have been extensively studied in Arabidopsis thaliana (a dicot) and to a lesser extent in Oryza sativa (a monocot). Thus far, they have been detected in the plasma membrane, vesicles, endoplasmic reticulum, Golgi apparatus, apoplast, cytosol, nuclear periphery, and peroxisomes. In combination with biochemical and molecular genetic tools, the widespread subcellular distribution of respective ACBP members has been explicitly linked to their functions in lipid metabolism during development and in response to stresses. At the cellular level, strong expression of specific ACBP homologs in specialized cells, such as embryos, stem epidermis, guard cells, male gametophytes, and phloem sap, is of relevance to their corresponding distinct roles in organ development and stress responses. Other interesting patterns in their subcellular localization and spatial expression that prompt new directions in future investigations are discussed.

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References

  • Adams J, Kelso R, Cooley L (2000) The kelch repeat superfamily of proteins: propellers of cell function. Trends Cell Biol 10:17–24

    Article  CAS  PubMed  Google Scholar 

  • Aharoni A, Dixit S, Jetter R, Thoenes E, van Arkel G, Pereira A (2004) The SHINE Clade of AP2 domain transcription factors activates wax biosynthesis, alters cuticle properties, and confers drought tolerance when overexpressed in Arabidopsis. Plant Cell 16:2463–2480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Andrews J, Keegstra K (1983) Acyl-CoA synthetase is located in the outer membrane and acyl-CoA thioesterase in the inner membrane of pea chloroplast envelopes. Plant Physiol 72:735–740

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baker A, Graham IA, Holdsworth M, Smith SM, Theodoulou FL (2006) Chewing the fat: β-oxidation in signalling and development. Trends Plant Sci 11:124–132

    Article  CAS  PubMed  Google Scholar 

  • Bates PD, Browse J (2012) The significance of different diacylglycerol synthesis pathways on plant oil composition and bioengineering. Front Plant Sci 3:147

    Article  PubMed  PubMed Central  Google Scholar 

  • Bates PD, Ohlrogge JB, Pollard M (2007) Incorporation of newly synthesized fatty acids into cytosolic glycerolipids in pea leaves occurs via acyl editing. J Biol Chem 282:31206–31216

    Article  CAS  PubMed  Google Scholar 

  • Benning C (2009) Mechanisms of lipid transport involved in organelle biogenesis. Annu Rev Cell Dev Biol 25:71–91

    Article  CAS  PubMed  Google Scholar 

  • Benschop JJ, Mohammed S, O’Flaherty M, Heck AJR, Slijper M, Menke FLH (2007) Quantitative phosphoproteomics of early elicitor signaling in Arabidopsis. Mol Cell Proteomics 6:1198–1214

    Article  CAS  PubMed  Google Scholar 

  • Bessoule JJ, Testet E, Cassagne C (1995) Synthesis of phosphatidylcholine in the chloroplast envelope after import of lysophosphatidylcholine from endoplasmic reticulum membranes. Eur J Biochem 228:490–497

    Article  CAS  PubMed  Google Scholar 

  • Block MA, Jouhet J (2015) Lipid trafficking at endoplasmic reticulum-chloroplast membrane contact sites. Curr Opin Cell Biol 35:21–29

    Article  CAS  PubMed  Google Scholar 

  • Brown AP, Johnson P, Rawsthorne S, Hills MJ (1998) Expression and properties of acyl-CoA binding protein from Brassica napus. Plant Physiol Biochem 36:629–635

    Article  CAS  Google Scholar 

  • Burton M, Rose TM, Faergeman NJ, Knudsen J (2005) Evolution of the acyl-CoA binding protein (ACBP). Biochem J 392:299–307

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chao H, Zhou M, McIntosh A, Schroeder F, Kier AB (2003) ACBP and cholesterol differentially alter fatty acyl CoA utilization by microsomal ACAT. J Lipid Res 44:72–83

    Article  CAS  PubMed  Google Scholar 

  • Chen QF, Xiao S, Chye ML (2008) Overexpression of the Arabidopsis 10-kilodalton acyl-coenzyme A-binding protein ACBP6 enhances freezing tolerance. Plant Physiol 148:304–315

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen QF, Xiao S, Qi W, Mishra G, Ma J, Wang M, Chye ML (2010) The Arabidopsis acbp1acbp2 double mutant lacking acyl-CoA-binding proteins ACBP1 and ACBP2 is embryo lethal. New Phytol 186:843–855

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choi D, Bostock RM, Avdiushko S, Hildebrand DF (1994) Lipid-derived signals that discriminate wound- and pathogen-responsive isoprenoid pathways in plants: methyl jasmonate and the fungal elicitor arachidonic acid induce different 3-hydroxy-3-methylglutaryl-coenzyme A reductase genes and antimicrobial isoprenoids in Solanum tuberosum L. Proc Natl Acad Sci U S A 91:2329–2333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choi H, Jin JY, Choi S, Hwang JU, Kim YY, Suh MC, Lee Y (2011) An ABCG/WBC-type ABC transporter is essential for transport of sporopollenin precursors for exine formation in developing pollen. Plant J 65:181–193

    Article  CAS  PubMed  Google Scholar 

  • Chung T, Suttangkakul A, Vierstra RD (2009) The ATG autophagic conjugation system in maize: ATG transcripts and abundance of the ATG8-lipid adduct are regulated by development and nutrient availability. Plant Physiol 149:220–234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chung T, Phillips AR, Vierstra RD (2010) ATG8 lipidation and ATG8-mediated autophagy in Arabidopsis require ATG12 expressed from the differentially controlled ATG12A and ATG12B loci. Plant J 62:483–493

    Article  CAS  PubMed  Google Scholar 

  • Chye ML (1998) Arabidopsis cDNA encoding a membrane-associated protein with an acyl-CoA binding domain. Plant Mol Biol 38:827–838

    Article  CAS  PubMed  Google Scholar 

  • Chye ML, Huang BQ, Zee SY (1999) Isolation of a gene encoding Arabidopsis membrane associated acyl-CoA binding protein and immunolocalization of its gene product. Plant J 18:205–214

    Article  CAS  PubMed  Google Scholar 

  • Chye ML, Li HY, Yung MH (2000) Single amino acid substitutions at the acyl-CoA-binding domain interrupt 14[C]palmitoyl-CoA binding of ACBP2, an Arabidopsis acyl-CoA-binding protein with ankyrin repeats. Plant Mol Biol 44:711–721

    Article  CAS  PubMed  Google Scholar 

  • Citharel B, Oursel A, Mazliak P (1983) Desaturation of oleoyl and linoleoyl residues linked to phospholipids in growing roots of yellow lupin. FEBS Lett 161:251–256

    Article  CAS  Google Scholar 

  • Cominelli E, Sala T, Calvi D, Gusmaroli G, Tonelli C (2008) Over-expression of the Arabidopsis AtMYB41 gene alters cell expansion and leaf surface permeability. Plant J 53:53–64

    Article  CAS  PubMed  Google Scholar 

  • Constantinides PP, Steim JM (1985) Physical properties of fatty acyl-CoA. J Biol Chem 260:7573–7580

    CAS  PubMed  Google Scholar 

  • Constantinides PP, Steim JM (1988) Micellization of fatty acyl-CoA mixtures and its relevance to the fatty acyl selectivity of acyltransferases. Arch Biochem Biophys 261:430–436

    Article  CAS  PubMed  Google Scholar 

  • Coppé JP, Patil CK, Rodier F, Sun Y, Munoz DP, Goldstein J, Nelson PS, Desprez PY, Campisi J (2008) Senescence-associated secretory phenotypes reveal cell-nonautonomous functions of oncogenic RAS and the p53 tumor suppressor. PLoS Biol 6:e301

    Article  PubMed Central  CAS  Google Scholar 

  • Coppé JP, Desprez PY, Krtolica A, Campisi J (2010) The senescence-associated secretory phenotype: the dark side of tumor suppression. Annu Rev Pathol 5:99–118

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • D’Angelo MA, Raices M, Panowski SH, Hetzer MW (2009) Age-dependent deterioration of nuclear pore complexes causes a loss of nuclear integrity in postmitotic cells. 136:284–295

  • Du ZY, Xiao S, Chen QF, Chye ML (2010) Depletion of the membrane-associated acyl-coenzyme A-binding protein ACBP1 enhances the ability of cold acclimation in Arabidopsis. Plant Physiol 152:1585–1597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Du ZY, Chen MX, Chen QF, Xiao S, Chye ML (2013a) Overexpression of Arabidopsis acyl-CoA-binding protein ACBP2 enhances drought tolerance. Plant Cell Environ 36:300–314

    Article  CAS  PubMed  Google Scholar 

  • Du ZY, Chen MX, Chen QF, Xiao S, Chye ML (2013b) Arabidopsis acyl-CoA-binding protein ACBP1 participates in the regulation of seed germination and seedling development. Plant J 74:294–309

    Article  CAS  PubMed  Google Scholar 

  • Dubacq JP, Drapier D, Trémoliéres A (1983) Polyunsaturated fatty acid synthesis by a mixture of chloroplasts and microsomes from spinach leaves: evidence for two distinct pathways of the biosynthesis of trienoic acids. Plant Cell Physiol 24:1–9

    CAS  Google Scholar 

  • Elle IC, Simonsen KT, Olsen LCB, Birck PK, Ehmsen S, Tuck S, Le TT, Faergeman NJ (2011) Tissue- and paralogue-specific functions of acyl-CoA-binding proteins in lipid metabolism in Caenorhabditis elegans. Biochem J 437:231–241

    Article  CAS  PubMed  Google Scholar 

  • Engeseth NJ, Pacovsky RS, Newman T, Ohlrogge JB (1996) Characterization of an acyl-CoA-binding protein from Arabidopsis thaliana. Arch Biochem Biophys 331:55–62

    Article  CAS  PubMed  Google Scholar 

  • Evans DE, Taylor PE, Singh MB, Knox RB (1991) Quantitative analysis of lipids and protein from the pollen of Brassica napus L. Plant Sci 73:117–126

    Article  CAS  Google Scholar 

  • Evans DE, Taylor PE, Singh MB, Knox RB (1992) The interrelationship between the accumulation of lipids, protein and the level of acyl carrier protein during the development of Brassica napus L. pollen. Planta 186:343–354

    Article  CAS  PubMed  Google Scholar 

  • Faergeman NJ, Knudsen J (1997) Role of long-chain fatty acyl-CoA esters in the regulation of metabolism and in cell signalling. Biochem J 323:1–12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Faergeman NJ, Wadum M, Feddersen S, Burton M, Kragelund BB, Knudsen J (2007) Acyl-CoA binding proteins; structural and functional conservation over 2000 MYA. Mol Cell Biochem 299:55–65

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujioka Y, Noda NN, Fujii K, Yoshimoto K, Ohsumi Y, Inagaki F (2008) In vitro reconstitution of plant Atg8 and Atg12 conjugation systems essential for autophagy. J Biol Chem 283:1921–1928

    Article  CAS  PubMed  Google Scholar 

  • Fukao Y, Hayashi M, Hara-Nishimura I, Nishimura M (2003) Novel glyoxysomal protein kinase, GPK1, identified by proteomic analysis of glyoxysomes in etiolated cotyledons of Arabidopsis thaliana. Plant Cell Physiol 44:1002–1012

    Article  CAS  PubMed  Google Scholar 

  • Fyrst H, Knudsen J, Schott MA, Lubin BH, Kuypers FA (1995) Detection of acyl-CoA-binding protein in human red blood cells and investigation of its role in membrane phospholipid renewal. Biochem J 306:793–799

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gaigg B, Neergaard TBF, Schneiter R, Hansen JK, Faergeman NJ, Jensen NA, Andersen JR, Friis J, Sandhoff R, Schrøder HD, Knudsen J (2001) Depletion of acyl-coenzyme A-binding protein affects sphingolipid synthesis and causes vesicle accumulation and membrane defects in Saccharomyces cerevisiae. Mol Biol Cell 12:1147–1160

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao W, Xiao S, Li HY, Tsao SW, Chye ML (2009) Arabidopsis thaliana acyl-CoA-binding protein ACBP2 interacts with heavy-metal-binding farnesylated protein AtFP6. New Phytol 181:89–102

    Article  CAS  PubMed  Google Scholar 

  • Gao W, Li HY, Chye ML (2010a) Acyl-CoA-binding protein 2 binds lysophospholipase 2 and lysoPC to promote tolerance to cadmium-induced oxidative stress in transgenic Arabidopsis. Plant J 62:989–1003

    CAS  PubMed  Google Scholar 

  • Gao W, Li HY, Xiao S, Chye ML (2010b) Protein interactors of acyl-CoA-binding protein ACBP2 mediate cadmium tolerance in Arabidopsis. Plant Signal Behav 5:1025–1027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Geng J, Klionsky DJ (2008) The Atg8 and Atg12 ubiquitin-like conjugation systems in macroautophagy. EMBO Rep 9:859–864

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goepfert S, Poirier Y (2007) β-oxidation in fatty acid degradation and beyond. Curr Opin Plant Biol 10:245–251

    Article  CAS  PubMed  Google Scholar 

  • Gosti F, Beaudoin N, Serizet C, Webb AAR, Vartanian N, Giraudat J (1999) ABI1 protein phosphatase 2C is a negative regulator of abscisic acid signaling. Plant Cell 11:1897–1909

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Graham IA (2008) Seed storage oil mobilization. Annu Rev Plant Biol 59:115–142

    Article  CAS  PubMed  Google Scholar 

  • Graham IA, Eastmond PJ (2002) Pathways of straight and branched chain fatty acid catabolism in higher plants. Prog Lipid Res 41:156–181

    Article  CAS  PubMed  Google Scholar 

  • Graham IA, Li Y, Larson TR (2002) Acyl-CoA measurements in plants suggest a role in regulating various cellular processes. Biochem Soc Trans 30:1095–1099

    Article  CAS  PubMed  Google Scholar 

  • Grebenok RJ, Pierson E, Lambert GM, Gong FC, Afonso CL, Haldeman-Cahill R, Carrington JC, Galbraith DW (1997) Green-fluorescent protein fusions for efficient characterization of nuclear targeting. Plant J 11:573–586

    Article  CAS  PubMed  Google Scholar 

  • Greer S, Wen M, Bird D, Wu X, Samuels L, Kunst L, Jetter R (2007) The cytochrome P450 enzyme CYP96A15 is the midchain alkane hydroxylase responsible for formation of secondary alcohols and ketones in stem cuticular wax of Arabidopsis. Plant Physiol 145:63–667

    Article  CAS  Google Scholar 

  • Guelette BS, Benning UF, Hoffmann-Benning S (2012) Identification of lipids and lipid-binding proteins in phloem exudates from Arabidopsis thaliana. J Exp Bot 63:3603–3616

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guerrero C, Martín-Rufián M, Reina JJ, Heredia A (2006) Isolation and characterization of a cDNA encoding a membrane bound acyl-CoA binding protein from Agave americana L. epidermis. Plant Physiol Biochem 44:85–90

    Article  CAS  PubMed  Google Scholar 

  • Guidotti A, Forchetti CM, Corda MG, Konkel D, Bennett CD, Costa E (1983) Isolation, characterization, and purification to homogeneity of an endogenous polypeptide with agonistic action on benzodiazepine receptors. Proc Natl Acad Sci U S A 80:3531–3535

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hayashi M, Nito K, Takei-Hoshi R, Yagi M, Kondo M, Suenaga A, Yamaya T, Nishimura M (2002) Ped3p is a peroxisomal ATP-binding cassette transporter that might supply substrates for fatty acid β-oxidation. Plant Cell Physiol 43:1–11

    Article  CAS  PubMed  Google Scholar 

  • Hills MJ, Dann R, Lydiate D, Sharpe A (1994) Molecular cloning of a cDNA from Brassica napus L. for a homologue of acyl-CoA-binding protein. Plant Mol Biol 25:917–920

    Article  CAS  PubMed  Google Scholar 

  • Hobbs DH, Hills MJ (2000) Expression and characterization of diacylglycerol acyltransferase from Arabidopsis thaliana in insect cell cultures. Biochem Soc Trans 28:687–689

    Article  CAS  PubMed  Google Scholar 

  • Hooper CM, Tanz SK, Castleden IR, Vacher MA, Small ID, Millar AH (2014) SUBAcon: a consensus algorithm for unifying the subcellular localization data of the Arabidopsis proteome. Bioinformatics 30:3356–3364

    Article  CAS  PubMed  Google Scholar 

  • Hsiao AS, Haslam RP, Michaelson LV, Liao P, Chen QF, Sooriyaarachchi S, Mowbray SL, Napier JA, Tanner JA, Chye ML (2014a) Arabidopsis cytosolic acyl-CoA-binding proteins ACBP4, ACBP5 and ACBP6 have overlapping but distinct roles in seed development. Biosci Rep 34:e00165

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hsiao AS, Haslam RP, Michaelson LV, Liao P, Napier JA, Chye ML (2014b) Gene expression in plant lipid metabolism in Arabidopsis seedlings. PLoS ONE 9:e107372

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hsiao AS, Yeung EC, Ye ZW, Chye ML (2015) The Arabidopsis cytosolic acyl-CoA-binding proteins play combinatory roles in pollen development. Plant Cell Physiol 56:322–333

    Article  PubMed  Google Scholar 

  • Hsu KHL, Powell GL (1975) Inhibition of citrate synthase by oleoyl-CoA: a regulatory phenomenon. Proc Natl Acad Sci U S A 72:4729–4733

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang H, Atshaves BP, Frolov A, Kier AB, Schroeder F (2005) Acyl-coenzyme A binding protein expression alters liver fatty acyl-coenzyme A metabolism. Biochemistry 44:10282–10297

    Article  CAS  PubMed  Google Scholar 

  • Ito J, Batth TS, Petzold CJ, Redding-Johanson AM, Mukhopadhyay A, Verboom R, Meyer EH, Millar AH, Heazlewood JL (2011) Analysis of the Arabidopsis cytosolic proteome highlights subcellular partitioning of central plant metabolism. J Proteome Res 10:1571–1582

    Article  CAS  PubMed  Google Scholar 

  • Jenks MA, Eigenbrode SD, Lemieux B (2002) Cuticular waxes of Arabidopsis. The Arabidopsis book 1:e0016

  • Jessen D, Roth C, Wiermer M, Fulda M (2015) Two activities of long-chain acyl-coenzyme A synthetase are involved in lipid trafficking between endoplasmic reticulum and the plastid in Arabidopsis. Plant Physiol 167:351–366

    Article  CAS  PubMed  Google Scholar 

  • Jolly CA, Wilton DC, Schroeder F (2000) Microsomal fatty acyl-CoA transacylation and hydrolysis: fatty acyl-CoA species dependent modulation by liver fatty acyl-CoA binding proteins. Biochim Biophys Acta 1483:185–197

    Article  CAS  PubMed  Google Scholar 

  • Jones AME, MacLean D, Studholme DJ, Serna-Sanz A, Andreasson E, Rathjen JP, Peck SC (2009) Phosphoproteomic analysis of nuclei-enriched fractions from Arabidopsis thaliana. J Proteomics 72:439–451

    Article  CAS  PubMed  Google Scholar 

  • Joyard J, Stumpf PK (1981) Synthesis of long-chain acyl-CoA in chloroplast envelope membranes. 67:250–256

  • Kannan L, Knudsen J, Jolly CA (2003) Aging and acyl-CoA binding protein alter mitochondrial glycerol-3-phosphate acyltransferase activity. Biochim Biophys Acta 1631:12–16

    Article  CAS  PubMed  Google Scholar 

  • Katagiri T, Ishiyama K, Kato T, Tabata S, Kobayashi M, Shinozaki K (2005) An important role of phosphatidic acid in ABA signaling during germination of Arabidopsis thaliana. Plant J 43:107–117

    Article  CAS  PubMed  Google Scholar 

  • Kennedy EP (1961) Biosynthesis of complex lipids. Fed Proc Am Soc Exp Biol 20:934–940

    CAS  Google Scholar 

  • Kerkhoff C, Beuck M, Threige-Rasmussen J, Spener F, Knudsen J, Schmitz G (1997) Acyl-CoA binding protein (ACBP) regulates acyl-CoA:cholesterol acyltransferase (ACAT) in human mononuclear phagocytes. Biochim Biophys Acta 1346:163–172

    Article  CAS  PubMed  Google Scholar 

  • Kjellberg JM, Trimborn M, Andersson M, Sandelius AS (2000) Acyl-CoA dependent acylation of phospholipids in the chloroplast envelope. Biochim Biophys Acta 1485:100–110

    Article  CAS  PubMed  Google Scholar 

  • Knudsen J, Højrup P, Hansen HO, Hansen HF, Roepstorff P (1989) Acyl-CoA-binding protein in the rat. Biochem J 262:513–519

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Knudsen J, Jensen MV, Hansen JK, Faergeman NJ, Neergaard TBF, Gaigg B (1999) Role of acylCoA binding protein in acylCoA transport, metabolism and cell signaling. Mol Cell Biochem 192:95–103

    Article  CAS  PubMed  Google Scholar 

  • Knudsen J, Neergaard TBF, Gaigg B, Jensen MV, Hansen JK (2000) Role of acyl-CoA binding protein in acyl-CoA metabolism and acyl-CoA-mediated cell signaling. J Nutr 130:294S–298S

    CAS  PubMed  Google Scholar 

  • Kornberg A, Pricer WE Jr (1953) Enzymatic synthesis of the coenzyme A derivatives of long chain fatty acids. J Biol Chem 204:329–343

    CAS  PubMed  Google Scholar 

  • Kragelund BB, Knudsen J, Poulsen FM (1999) Acyl-coenzyme A binding protein (ACBP). Biochim Biophys Acta 1441:150–161

    Article  CAS  PubMed  Google Scholar 

  • Lager I, Glab B, Eriksson L, Chen G, Banas A, Stymne S (2015) Novel reactions in acyl editing of phosphatidylcholine by lysophosphatidylcholine transacylase (LPCT) and acyl-CoA:glycerophosphocholine acyltransferase (GPCAT) activities in microsomal preparations of plant tissues. Planta 241:347–358

    Article  CAS  PubMed  Google Scholar 

  • Larsen MK, Tuck S, Faergeman NJ, Knudsen J (2006) MAA-1, a novel acyl-CoA-binding protein involved in endosomal vesicle transport in Caenorhabditis elegans. Mol Biol Cell 17:4318–4329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee SB, Suh MC (2013) Recent advances in cuticular wax biosynthesis and its regulation in Arabidopsis. Mol Plant 6:246–249

    Article  CAS  PubMed  Google Scholar 

  • Lessire R, Bessoule JJ, Cassagne C (1989) Involvement of a β-ketoacyl-CoA intermediate in acyl-CoA elongation by an acyl-CoA elongase purified from leek epidermal cells. Biochim Biophys Acta 1006:35–40

    Article  CAS  Google Scholar 

  • Lessire R, Domergue F, Spinner C, Lucet-Levannier K, Lellouche JP, Mioskowski C, Cassagne C (1998) Dehydration of 3-hydroxy icosanoyl-CoA and reduction of (E) 2,3 icosenoyl-CoA are required for elongation by leek microsomal elongase(s). Plant Physiol Biochem 36:205–211

    Article  CAS  Google Scholar 

  • Leung KC, Li HY, Mishra G, Chye ML (2004) ACBP4 and ACBP5, novel Arabidopsis acyl-CoA-binding proteins with kelch motifs that bind oleoyl-CoA. Plant Mol Biol 55:297–309

    Article  CAS  PubMed  Google Scholar 

  • Leung KC, Li HY, Xiao S, Tse MH, Chye ML (2006) Arabidopsis ACBP3 is an extracellularly targeted acyl-CoA-binding protein. Planta 223:871–881

    Article  CAS  PubMed  Google Scholar 

  • Li HY, Chye ML (2003) Membrane localization of Arabidopsis acyl-CoA binding protein ACBP2. Plant Mol Biol 51:483–492

    Article  CAS  PubMed  Google Scholar 

  • Li HY, Chye ML (2004) Arabidopsis acyl-CoA-binding protein ACBP2 interacts with an ethylene-responsive element-binding protein, AtEBP, via its ankyrin repeats. Plant Mol Biol 54:233–243

    Article  CAS  PubMed  Google Scholar 

  • Li F, Vierstra RD (2012) Autophagy: a multifaceted intracellular system for bulk and selective recycling. Trends Plant Sci 17:526–537

    Article  CAS  PubMed  Google Scholar 

  • Li HY, Xiao S, Chye ML (2008) Ethylene- and pathogen-inducible Arabidopsis acyl-CoA-binding protein 4 interacts with an ethylene-responsive element binding protein. J Exp Bot 59:3997–4006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liao P, Chen QF, Chye ML (2014) Transgenic Arabidopsis flowers overexpressing acyl-CoA-binding protein ACBP6 are freezing tolerant. Plant Cell Physiol 55:1055–1071

    Article  CAS  PubMed  Google Scholar 

  • Licausi F, Kosmacz M, Weits DA, Giuntoli B, Giorgi FM, Voesenek LACJ, Perata P, van Dongen JT (2011) Oxygen sensing in plants is mediated by an N-end rule pathway for protein destabilization. Nature 479:419–422

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Bassham DC (2012) Autophagy: pathways for self-eating in plant cells. Annu Rev Plant Biol 63:215–237

    Article  CAS  PubMed  Google Scholar 

  • Lü S, Song T, Kosma DK, Parsons EP, Rowland O, Jenks MA (2009) Arabidopsis CER8 encodes LONG-CHAIN ACYL-COA SYNTHETASE 1 (LACS1) that has overlapping functions with LACS2 in plant wax and cutin synthesis. Plant J 59:553–564

    Article  PubMed  CAS  Google Scholar 

  • Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324:1064–1068

    CAS  PubMed  Google Scholar 

  • Meng W, Chye ML (2014) Rice acyl-CoA-binding proteins OsACBP4 and OsACBP5 are differentially localized in the endoplasmic reticulum of transgenic Arabidopsis. Plant Signal Behav 9:e29544

    Article  PubMed Central  CAS  Google Scholar 

  • Meng W, Su YCF, Saunders RMK, Chye ML (2011) The rice acyl-CoA-binding protein gene family: phylogeny, expression and functional analysis. New Phytol 189:1170–1184

    Article  CAS  PubMed  Google Scholar 

  • Meng W, Hsiao AS, Gao C, Jiang L, Chye ML (2014) Subcellular localization (ACBPs) indicates that OsACBP6::GFP is targeted to the peroxisomes. New Phytol 203:469–482

    Article  CAS  PubMed  Google Scholar 

  • Metzner M, Ruecknagel KP, Knudsen J, Kuellertz G, Mueller-Uri F, Diettrich B (2000) Isolation and characterization of two acyl-CoA-binding proteins from proembryogenic masses of Digitalis lanata Ehrh. Planta 210:683–685

    Article  CAS  PubMed  Google Scholar 

  • Millar AH, Carrie C, Pogson B, Whelan J (2009) Exploring the function-location nexus: using multiple lines of evidence in defining the subcellular location of plant proteins. Plant Cell 21:1625–1631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mogensen IB, Schulenberg H, Hansen HO, Spener F, Knudsen J (1987) A novel acyl-CoA-binding protein from bovine liver. Effect on fatty acid synthesis. Biochem J 241:189–192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moore I, Murphy A (2009) Validating the location of fluorescent protein fusions in the endomembrane system. Plant Cell 21:1632–1636

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murphy DJ (2006) The extracellular pollen coat in members of the Brassicaceae: composition, biosynthesis, and functions in pollination. Protoplasma 228:31–39

    Article  CAS  PubMed  Google Scholar 

  • Murphy DJ, Woodrow IE, Mukherjee KD (1985) Substrate specificities of the enzymes of the oleate desaturase system from photosynthetic tissue. Biochem J 225:267–270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Napier JA, Haslam RP (2010) As simple as ACB – new insights into the role of acyl-CoA-binding proteins in Arabidopsis. New Phytol 186:783–785

    Article  Google Scholar 

  • Nawrath C (2006) Unraveling the complex network of cuticular structure and function. Curr Opin Plant Biol 9:281–287

    Article  CAS  PubMed  Google Scholar 

  • Neess D, Bek S, Engelsby H, Gallego SF, Færgeman NJ (2015) Long-chain acyl-CoA esters in metabolism and signaling: role of acyl-CoA binding proteins. Prog Lipid Res 59:1–25

    Article  CAS  PubMed  Google Scholar 

  • Ohlrogge J, Browse J (1995) Lipid Biosynthesis. Plant Cell 7:957–970

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olsen LJ (1998) The surprising complexity of peroxisome biogenesis. Plant Mol Biol 38:163–189

    Article  CAS  PubMed  Google Scholar 

  • Park SY, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow TF (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324:1068–1071

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pastor S, Sethumadhavan K, Ullah AHJ, Gidda S, Cao H, Mason C, Chapital D, Scheffler B, Mullen R, Dyer J, Shockey J (2013) Molecular properties of the class III subfamily of acyl-coenzyme A binding proteins from tung tree (Vernicia fordii). Plant Sci 203–204:79–88

    Article  PubMed  CAS  Google Scholar 

  • Piffanelli P, Ross JHE, Murphy DJ (1997) Intra- and extracellular lipid composition and associated gene expression patterns during pollen development in Brassica napus. Plant J 11:549–562

    Article  CAS  PubMed  Google Scholar 

  • Powell GL, Grothusen JR, Zimmerman JK, Evans CA, Fish WW (1981) A re-examination of some properties of fatty acyl-CoA micelles. J Biol Chem 256:12740–12747

    CAS  PubMed  Google Scholar 

  • Quilichini TD, Friedmann MC, Samuels AL, Douglas CJ (2010) ATP-binding cassette transporter G26 is required for male fertility and pollen exine formation in Arabidopsis. Plant Physiol 154:678–690

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raboanatahiry NH, Lu G, Li M (2015) Computational prediction of acyl-CoA binding proteins structure in Brassica napus. PLoS ONE 10:e0129650

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rasmussen JT, Börchers T, Knudsen J (1990) Comparison of the binding affinities of acyl-CoA-binding protein and fatty-acid-binding protein for long-chain acyl-CoA esters. Biochem J 265:849–855

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rasmussen JT, Rosendal J, Knudsen J (1993) Interaction of acyl-CoA binding protein (ACBP) on processes for which acyl-CoA is a substrate, product or inhibitor. Biochem J 292:907–913

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reddy AS, Ranganathan B, Haisler RM, Swize MA (1996) A cDNA encoding acyl-CoA-binding protein from cotton (accession no. U34015). Plant Physiol 111:348 (PGR96-028)

    Article  Google Scholar 

  • Roughan PG, Holland R, Slack CR (1980) The role of chloroplasts and microsomal fractions in polar-lipid synthesis from [1-14C]acetate by cell-free preparations from spinach (Spinacia oleracea) leaves. Biochem J 188:17–24

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rowland O, Zheng H, Hepworth SR, Lam P, Jetter R, Kunst L (2006) CER4 encodes an alcohol-forming fatty acyl-Coenzyme A reductase involved in cuticular wax production in Arabidopsis. Plant Physiol 142:866–877

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ryu SB (2004) Phospholipid-derived signaling mediated by phospholipase A in plants. Trends Plant Sci 9:229–235

    Article  CAS  PubMed  Google Scholar 

  • Samuels L, Kunst L, Jetter R (2008) Sealing plant surfaces: cuticuliar wax formation by epidermal cells. Annu Rev Plant Biol 59:683–707

    Article  CAS  PubMed  Google Scholar 

  • Santiago J, Dupeux F, Round A, Antoni R, Park SY, Jamin M, Cutler SR, Rodrigeuz PL, Márquez JA (2009) The abscisic acid receptor PYR1 in complex with abscisic acid. Nature 462:665–668

    Article  CAS  PubMed  Google Scholar 

  • Seo PJ, Lee SB, Suh MC, Park MJ, Go YS, Park CM (2011) The MYB96 transcription factor regulates cuticular wax biosynthesis under drought conditions in Arabidopsis. Plant Cell 23:1138–1152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi DQ, Liu J, Xiang YH, Ye D, Sundaresan V, Yang WC (2005) SLOW WALKER1, essential for gametogenesis in Arabidopsis, encodes a WD40 protein involved in 18S ribosomal RNA biogenesis. Plant Cell 17:2340–2354

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simpson EE, Williams JP (1979) Galactolipid synthesis in Vicia faba leaves: IV. Site(s) of fatty acid incorporation into the major glycerolipids. Plant Physiol 63:674–676

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Slack CR, Roughan PG (1975) The kinetics of incorporation in vivo of [14C]acetate and [14C]carbon dioxide into the fatty acids of glycerolipids in developing leaves. Biochem J 152:217–228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Slack CR, Roughan PG, Browse J (1979) Evidence for an oleoyl phosphatidylcholine desaturase in microsomal preparations from cotyledons of safflower (Carthamus tinctorius) seed. Biochem J 179:649–656

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith CJ (1996) Accumulation of phytoalexins: defence mechanism and stimulus response system. New Phytol 132:1–45

    Article  CAS  Google Scholar 

  • Soupene E, Fyrst H, Kuypers FA (2008) Mammalian acyl-CoA:lysophosphatidylcholine acyltransferase enzymes. Proc Natl Acad Sci U S A 105:88–93

    Article  CAS  PubMed  Google Scholar 

  • Stymne S, Stobart AK (1984) Evidence for the reversibility of the acyl-CoA:lysophosphatidylcholine acyltransferase in microsomal preparations from developing safflower (Carthamus tinctorius L.) cotyledons and rat liver. Biochem J 223:305–314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stymne S, Stobart AK, Glad G (1983) The role of the acyl-COA pool in the synthesis of polyunsaturated 18-carbon fatty acids and triacylglycerol production in the microsomes of developing safflower seeds. Biochim Biophys Acta 752:198–208

    Article  CAS  PubMed  Google Scholar 

  • Sun Q, Zybailov B, Majeran W, Friso G, Olinares PD, van Wijk KJ (2009) PPDB, the plant proteomics database at Cornell. Nucleic Acids Res 37:D969–D974

    Article  CAS  PubMed  Google Scholar 

  • Suzui N, Nakamura S, Fujiwara T, Hayashi H, Yoneyama T (2006) A putative acyl-CoA-binding protein is a major phloem sap protein in rice (Oryza sativa L.). J Exp Bot 57:2571–2576

    Article  CAS  PubMed  Google Scholar 

  • Szostkiewicz I, Richter K, Kepka M, Demmel S, Ma Y, Korte A, Assaad FF, Christman A, Grill E (2010) Closely related receptor complexes differ in their ABA selectivity and sensitivity. Plant J 61:25–35

    Article  CAS  PubMed  Google Scholar 

  • Takato H, Shimidzu M, Ashizawa Y, Takei H, Suzuki S (2013) An acyl-CoA-binding protein from grape that is induced through ER stress confers morphological changes and disease resistance in Arabidopsis. J Plant Physiol 170:591–600

    Article  CAS  PubMed  Google Scholar 

  • Testerink C, Munnik T (2005) Phosphatidic acid: a multifunctional stress signaling lipid in plants. Trends Plant Sci 10:368–375

    Article  CAS  PubMed  Google Scholar 

  • Tjellström H, Yang Z, Allen DK, Ohlrogge JB (2012) Rapid kinetic labeling of Arabidopsis cell suspension cultures: implications for models of lipid export from plastids. Plant Physiol 158:601–611

    Article  PubMed  CAS  Google Scholar 

  • Tolbert NE, Essner E (1981) Microbodies: peroxisomes and glyoxysomes. J Cell Biol 91:271s–283s

    Article  CAS  PubMed  Google Scholar 

  • van de Loo FJ, Turner S, Somerville C (1995) Expressed sequence tags from developing castor seeds. Plant Physiol 108:1141–1150

    Google Scholar 

  • van Dongen JT, Licausi F (2015) Oxygen sensing and signaling. Annu Rev Plant Biol 66:345–367

    Article  PubMed  CAS  Google Scholar 

  • Viehweger K, Dordschbal B, Roos W (2002) Elicitor-activated phospholipase A2 generates lysophosphatidylcholines that mobilize the vacuolar H+ pool for pH signaling via the activation of Na+-dependent proton fluxes. Plant Cell 14:1509–1525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wajapeyee N, Serra RW, Zhu X, Mahalingam M, Green MR (2008) Oncogenic BRAF induces senescence and apoptosis through pathways mediated by the secreted protein IGFBP7. Cell 132:363–374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Walz C, Giavalisco P, Schad M, Juenger M, Klose J, Kehr J (2004) Proteomics of curcurbit phloem exudate reveals a network of defence proteins. Phytochemistry 65:1795–1804

    Article  CAS  PubMed  Google Scholar 

  • Wang X (2001) Plant phospholipases. Annu Rev Plant Physiol Plant Mol Biol 52:211–231

    Article  CAS  PubMed  Google Scholar 

  • Wen J, Gong M, Chen K, Duan X, Qi Y, Wang X, Xin Y, Deng M (2014) Cloning and expression analysis of a new acyl-CoA-binding protein (JcACBP) identified from Jatropha curcas L. Xibei Zhiwu Xuebao 34:2159–2164

    CAS  Google Scholar 

  • Xia Y, Yu K, Gao QM, Wilson EV, Navarre D, Kachroo P, Kachroo A (2012) Acyl CoA binding proteins are required for cuticle formation and plant responses to microbes. Front Plant Sci 3:224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao S, Chye ML (2009) An Arabidopsis family of six acyl-CoA-binding proteins has three cytosolic members. Plant Physiol Biochem 47:479–484

    Article  CAS  PubMed  Google Scholar 

  • Xiao S, Chye ML (2010) The Arabidopsis thaliana ACBP3 regulates leaf senescence by modulating phospholipid metabolism and ATG8 stability. Autophagy 6:802–804

    Article  PubMed  Google Scholar 

  • Xiao S, Chye ML (2011a) New roles for acyl-CoA-binding proteins (ACBPs) in plant development, stress responses and lipid metabolism. Prog Lipid Res 50:141–151

    Article  CAS  PubMed  Google Scholar 

  • Xiao S, Chye ML (2011b) Overexpression of Arabidopsis ACBP3 enhances NPR1-dependent plant resistance to Pseudomonas syringae pv tomato DC3000. Plant Physiol 156:2069–2081

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao S, Gao W, Chen QF, Ramalingam S, Chye ML (2008a) Overexpression of membrane-associated acyl-CoA-binding protein ACBP1 enhances lead tolerance in Arabidopsis. Plant J 54:141–151

    Article  CAS  PubMed  Google Scholar 

  • Xiao S, Li HY, Zhang JP, Chan SW, Chye ML (2008b) Arabidopsis acyl-CoA-binding proteins ACBP4 and ACBP5 are subcellularly localized to the cytosol and ACBP4 depletion affects membrane lipid composition. Plant Mol Biol 68:571–583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao S, Chen QF, Chye ML (2009) Light-regulated Arabidopsis ACBP4 and ACBP5 encode cytosolic acyl-CoA-binding proteins that bind phosphatidylcholine and oleoyl-CoA ester. Plant Physiol Biochem 47:926–933

    Article  CAS  PubMed  Google Scholar 

  • Xiao S, Gao W, Chen QF, Chan SW, Zheng SX, Ma J, Wang M, Welti R, Chye ML (2010) Overexpression of Arabidopsis acyl-CoA binding protein ACBP3 promotes starvation-induced and age-dependent leaf senescence. Plant Cell 22:1463–1482

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xie Z, Nair Y, Klionsky DJ (2008) Atg8 controls phagophore expansion during autophagosome formation. Mol Biol Cell 19:3290–3298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xie LJ, Yu LJ, Chen QF, Wang FZ, Huang L, Xia FN, Zhu TR, Wu JX, Yin J, Liao B et al (2015) Arabidopsis acyl-CoA-binding protein ACBP3 participates in plant response to hypoxia by modulating very-long-chain fatty acid metabolism. Plant J 81:53–67

    Article  CAS  PubMed  Google Scholar 

  • Xue Y, Xiao S, Kim J, Lung SC, Chen L, Tanner JA, Suh MC, Chye ML (2014) Arabidopsis membrane-associated acyl-CoA-binding protein ACBP1 is involved in stem cuticle formation. J Exp Bot 65:5473–5483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yurchenko OP, Nykiforuk CL, Moloney MM, Ståhl U, Banaś A, Stymne S, Weselake RJ (2009) A 10-kDa acyl-CoA-binding protein (ACBP) from Brassica napus enhances acyl exchange between acyl-CoA and phosphatidylcholine. Plant Biotechnol J 7:602–610

    Article  CAS  PubMed  Google Scholar 

  • Yurchenko O, Singer SD, Nykiforuk CL, Gidda S, Mullen RT, Moloney MM, Weselake RJ (2014) Production of a Brassica napus low-molecular mass acyl-coenzyme A-binding protein in Arabidopsis alters the acyl-coenzyme A pool and acyl composition of oil in seeds. Plant Physiol 165:550–560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang W, Qin C, Zhao J, Wang X (2004) Phospholipase Dα1-derived phosphatidic acid interacts with ABI1 phosphatase 2C and regulates abscisic acid signaling. Proc Natl Acad Sci U S A 101:9508–9513

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang JY, Broeckling CD, Sumner LW, Wang ZY (2007) Heterologous expression of two Medicago truncatula putative ERF transcription factor genes, WXP1 and WXP2, in Arabidopsis led to increased leaf wax accumulation and improved drought tolerance, but differential response in freezing tolerance. Plant Mol Biol 64:265–278

    Article  CAS  PubMed  Google Scholar 

  • Zheng SX, Xiao S, Chye ML (2012) The gene encoding Arabidopsis acyl-CoA-binding protein 3 is pathogen inducible and subject to circadian regulation. J Exp Bot 63:2985–3000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol 136:2621–2632

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zolman BK, Yoder A, Bartel B (2000) Genetic analysis of indole-3-butyric acid responses in Arabidopsis thaliana reveals four mutant classes. Genetics 156:1323–1337

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 β-oxidation. Plant Physiol 127:1266–1278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

MLC is grateful to the Wilson and Amelia Wong Endowment Fund, the Research Grants Council of the Hong Kong Special Administrative Region, China (HKU765511M and HKU765813M), University Grants Committee, Hong Kong (AoE/M-05/12 and CUHK2/CRF/11G), and CRCG awards (104003169 and 104003561) from the University of Hong Kong (HKU) for supporting her work on plant ACBPs. SCL is supported by a HKU postdoctoral fellowship and CRCG award (Small Project Funding #201309176052).

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The authors declare that they have no conflict of interest.

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  1. School of Biological Sciences, The University of Hong Kong, Pokfulam, Hong Kong, China

    Shiu-Cheung Lung & Mee-Len Chye

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  1. Shiu-Cheung Lung
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Correspondence to Mee-Len Chye.

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Suppl. Fig. 1

Microarray data comparing the spatiotemporal expression of AtACBPs. Microarray data from the Genevestigator database (https://genevestigator.com/; Zimmermann et al. 2004) are available for AtACBP1, AtACBP2, AtACBP4, AtACBP5 and AtACBP6. (a) Time course of the gene expression of AtACBPs at different stages of development. (b) Heat map comparing tissue-specific expression of AtACBPs. (GIF 174 kb)

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Lung, SC., Chye, ML. Deciphering the roles of acyl-CoA-binding proteins in plant cells. Protoplasma 253, 1177–1195 (2016). https://doi.org/10.1007/s00709-015-0882-6

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