Skip to main content
Log in

Genome-wide identification and analysis of membrane-bound O-acyltransferase (MBOAT) gene family in plants

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Membrane bound O-acyl transferase (MBOAT) family is composed of gene members encoding a variety of acyltransferase enzymes, which play important roles in plant acyl lipid metabolism. Here, we present the first genome-enabled identification and analysis of MBOAT gene models in plants. In total, we identified 136 plant MBOAT sequences from 14 plant species with complete genomes. Phylogenetic relationship analyses suggested the plant MBOAT gene models fell into four major groups, two of which likely encode enzymes of diacylglycerol acyltransferase 1 (DGAT1) and lysophospholipid acyltransferase (LPLAT), respectively, with one–three copies of paralogs present in each of the most plant species. A group of gene sequences, which are homologous to Saccharomyces cerevisiae glycerol uptake proteins (GUP), was identified in plants; copy numbers were conserved, with only one copy represented in each of the most plant species; analyses showed that residues essential for acyltransferases were more prone to be conserved than vertebrate orthologs. Among four groups, one was inferred to emerge in land plants and experience a rapid expansion in genomes of angiosperms, which suggested their important roles in adaptation of plants in lands. Sequence and phylogeny analyses indicated that genes in all four groups encode enzymes with acyltransferases. Comprehensive sequence identification of MBOAT family members and investigation into classification provide a complete picture of the MBOAT gene family in plants, and could shed light into enzymatic functions of different MBOAT genes in plants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

ASAT:

Acyl-CoA:sterol acyltransferases

BLAST:

Basic local alignment search tool

DAcT:

Diacylglycerol acetyltransferase

DAG:

Diacylglycerol

DGAT:

Diacylglycerol acyltransferase

GUP:

Glycerol uptake protein

LPCAT:

Lysophosphotidylcholine acyltransferase

LPLAT:

Lysophospholipid acyltransferase

MBOAT:

Membrane bound O-acyltransferase

PC:

Phosphotidylcholine

SAT:

Sterol acyltransferase

TAG:

Triacylglycerol

References

  • Abe Y, Kita Y, Niikura T (2008) Mammalian Gup1, a homolog of Saccharomyces cerevisiae glycerol uptake/transporter 1, acts as a negative regulator for N-terminal palmitoylation of sonic hedgehog. FEBS J 275:318–331

    Article  CAS  PubMed  Google Scholar 

  • Banilas G, Karampelias M, Makariti I, Kourti A, Hatzopoulos P (2011) The olive DGAT2 gene is developmentally regulated and shares overlapping but distinct expression patterns with DGAT1. J Exp Bot 62:521–532

    Article  CAS  PubMed  Google Scholar 

  • Bates PD, Fatihi A, Snapp AR, Carlsson AS, Browse J, Lu CF (2012) Acyl editing and headgroup exchange are the major mechanisms that direct polyunsaturated fatty acid flux into triacylglycerols. Plant Physiol 160:1530–1539

    Article  CAS  PubMed  Google Scholar 

  • Beisson F, Koo AJ, Ruuska S, Schwender J, Pollard M, Thelen JJ, Paddock T, Salas JJ, Savage L, Milcamps A, Mhaske VB, Cho Y, Ohlrogge JB (2003) Arabidopsis genes involved in acyl lipid metabolism. A 2003 census of the candidates, a study of the distribution of expressed sequence tags in organs, and a web-based database. Plant Physiol 132:681–697

    Article  CAS  PubMed  Google Scholar 

  • Benghezal M, Roubaty C, Veepuri V, Knudsen J, Conzelmann A (2007) SLC1 and SLC4 encode partially redundant acyl-coenzyme A 1-acylglycerol-3-phosphate O- acyltransferases of budding yeast. J Biol Chem 282:30845–30855

    Article  CAS  PubMed  Google Scholar 

  • Bleve G, Zacheo G, Cappello MS, Dellaglio F, Grieco F (2005) Subcellular localization and functional expression of the glycerol uptake protein 1 (GUP1) of Saccharomyces cerevisiae tagged with green fluorescent protein. Biochem J 390:145–155

    Article  CAS  PubMed  Google Scholar 

  • Bonangelino CJ, Chavez EM, Bonifacino JS (2002) Genomic screen for vacuolar protein sorting genes in Saccharomyces cerevisiae. Mol Biol Cell 13:2486–2501

    Article  CAS  PubMed  Google Scholar 

  • Bosson R, Jaquenoud M, Conzelmann A (2006) GUP1 of Saccharomyces cerevisiae encodes an O-acyltransferase involved in remodeling of the GPI anchor. Mol Biol Cell 17:2636–2645

    Article  CAS  PubMed  Google Scholar 

  • Boyle NR, Page MD, Liu B et al (2012) Three acyltransferases and nitrogen-responsive regulator are implicated in nitrogen starvation-induced triacylglycerol accumulation in Chlamydomonas. J Biol Chem 287:15811–15825

    Article  CAS  PubMed  Google Scholar 

  • Buglino JA, Resh MD (2008) Hhat is a palmitoylacyltransferase with specificity for N- palmitoylation of Sonic Hedgehog. J Biol Chem 283:22076–22088

    Article  CAS  PubMed  Google Scholar 

  • Caffrey DR, Dana PH, Mathur V, Ocano M, Hong EJ, Wang YE, Somaroo S, Caffrey BE, Potluri S, Huang ES (2007) PFAAT version 2.0: a tool for editing, annotating, and analyzing multiple sequence alignments. BMC Bioinfo 8:381

    Article  Google Scholar 

  • Cao H (2011) Structure-function analysis of diacylglycerol acyltransferase sequences from 70 organisms. BMC Res Notes 4:249

    Article  CAS  PubMed  Google Scholar 

  • Chai YC, Hao XM, Yang XH, Allen WB, Li JM, Yan JB, Shen B, Li JS (2012) Validation of DGAT1-2 polymorphisms associated with oil content and development of functional markers for molecular breeding of high-oil maize. Mol Breeding 29:939–949

    Article  CAS  Google Scholar 

  • Chamoun Z, Mann RK, Nellen D, von Kessler DP, Bellotto M, Beachy PA, Basler K (2001) Skinny hedgehog, an acyltransferase required for palmitoylation and activity of the hedgehog signal. Science 293:2080–2084

    Article  CAS  PubMed  Google Scholar 

  • Chan AP, Crabtree J, Zhao Q et al (2010) Draft genome sequence of the oilseed species Ricinus communis. Nature Biotechnol 28:951–956

    Article  CAS  Google Scholar 

  • Chang CCY, Sun J, Chang TY (2011) Membrane-bound O-acyltransferases (MBOATs). Front Biol 6:177–182

    CAS  Google Scholar 

  • Chen Q, Steinhauer L, Hammerlindl J, Keller W, Zou J (2007a) Biosynthesis of phytosterol esters: identification of a sterol O-acyltransferase in Arabidopsis. Plant Physiol 145:974–984

    Article  CAS  PubMed  Google Scholar 

  • Chen QL, Kazachkov M, Zheng ZF, Zou JT (2007b) The yeast acylglycerol acyltransferase LCA1 is a key component of Lands cycle for phosphatidylcholine turnover. FEBS Lett 581:5511–5516

    Article  CAS  PubMed  Google Scholar 

  • Cherry JM, Hong EL, Amundsen C et al (2012) Saccharomyces Genome Database: the genomics resource of budding yeast. Nucleic Acids Res 40:D700–D705

    Article  CAS  PubMed  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2011) ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27:1164–1165

    Article  CAS  PubMed  Google Scholar 

  • Do CB, Mahabhashyam MS, Brudno M, Batzoglou S (2005) ProbCons: probabilistic consistency-based multiple sequence alignment. Genome Res 15:330–340

    Article  CAS  PubMed  Google Scholar 

  • Durrett TP, McClosky DD, Tumaney AW, Elzinga DA, Ohlrogge J, Pollard M (2010) A distinct DGAT with sn-3 acetyltransferase activity that synthesizes unusual, reduced- viscosity oils in Euonymus and transgenic seeds. Proc Natl Acad Sci USA 107:9464–9469

    Article  CAS  PubMed  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  CAS  PubMed  Google Scholar 

  • Goff SA, Ricke D, Lan TH et al (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296:92–100

    Article  CAS  PubMed  Google Scholar 

  • Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Rokhsar DS (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40:D1178–D1186

    Article  CAS  PubMed  Google Scholar 

  • Guindon S, Delsuc F, Dufayard JF, Gascuel O (2009) Estimating maximum likelihood phylogenies with PhyML. Methods Mol Biol 537:113–137

    Article  CAS  PubMed  Google Scholar 

  • He X, Turner C, Chen GQ, Lin JT, McKeon TA (2004) Cloning and characterization of a cDNA encoding diacylglycerol acyltransferase from castor bean. Lipids 39:311–318

    Article  CAS  PubMed  Google Scholar 

  • Hobbs DH, Lu C, Hills MJ (1999) Cloning of a cDNA encoding diacylglycerol acyltransferase from Arabidopsis thaliana and its functional expression. FEBS Lett 452:145–149

    Article  CAS  PubMed  Google Scholar 

  • Hofmann K (2000) A superfamily of membrane-bound O-acyltransferases with implications for Wnt signaling. Trends Biochem Sci 25:111–112

    Article  CAS  PubMed  Google Scholar 

  • Holst B, Lunde C, Lages F, Oliveira R, Lucas C, Kielland-Brandt MC (2000) GUP1 and its close homologue GUP2, encoding multimembrane-spanning proteins involved in active glycerol uptake in Saccharomyces cerevisiae. Mol Microbiol 37:108–124

    Article  CAS  PubMed  Google Scholar 

  • Huala E, Dickerman AW, Garcia-Hernandez M et al (2001) The Arabidopsis Information Resource (TAIR): a comprehensive database and web-based information retrieval, analysis, and visualization system for a model plant. Nucleic Acids Res 29:102–105

    Article  CAS  PubMed  Google Scholar 

  • Huang S, Li R, Zhang Z et al (2009) The genome of the cucumber, Cucumis sativus L. Nat Genet 41:1275–1281

    Article  CAS  PubMed  Google Scholar 

  • Ichihara K, Takahashi T, Fujii S (1988) Diacylglycerol acyltransferase in maturing safflower seeds: its influences on the fatty acid composition of triacylglycerol and on the rate of triacylglycerol synthesis. Biochim Biophys Acta 958:125–129

    Article  CAS  PubMed  Google Scholar 

  • Jain S, Stanford N, Bhagwat N, Seiler B, Costanzo M, Boone C, Oelkers P (2007) Identification of a novel lysophospholipid acyltransferase in Saccharomyces cerevisiae. J Biol Chem 282:30562–30569

    Article  CAS  PubMed  Google Scholar 

  • Jako C, Kumar A, Wei Y, Zou J, Barton DL, Giblin EM, Covello PS, Taylor DC (2001) Seed-specific over-expression of an Arabidopsis cDNA encoding a diacylglycerol acyltransferase enhances seed oil content and seed weight. Plant Physiol 126:861–874

    Article  CAS  PubMed  Google Scholar 

  • Lamesch P, Berardini TZ, Li D et al (2012) The arabidopsis information resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res 40:D1202–D1210

    Article  CAS  PubMed  Google Scholar 

  • Li RZ, Yu KS, Hildebrand DF (2010) DGAT1, DGAT2 and PDAT expression in seeds and other tissues of epoxy and hydroxy fatty acid accumulating plants. Lipids 45:145–157

    Article  PubMed  Google Scholar 

  • Liang JJ, Oelkers P, Guo C, Chu PC, Dixon JL, Ginsberg HN, Sturley SL (2004) Overexpression of human diacylglycerol acyltransferase 1, acyl-CoA:cholesterol acyltransferase 1, or acyl-CoA:cholesterol acyltransferase 2 stimulates secretion of apolipoprotein B-containing lipoproteins in McA-RH7777 cells. J Biol Chem 279:44938–44944

    Article  CAS  PubMed  Google Scholar 

  • Li-Beisson Y, Shorrosh B, Beisson F et al (2013) Acyl-lipid metabolism. In: The Arabidopsis Book, vol 11. American Society of Plant Biologists, Rockville, MD, USA, pp e0161

  • Liu Q, Siloto RM, Lehner R, Stone SJ, Weselake RJ (2012) Acyl-CoA:diacylglycerol acyltransferase: molecular biology, biochemistry and biotechnology. Progress Lipid Res 51:350–377

    Article  CAS  Google Scholar 

  • Lung SC, Weselake RJ (2006) Diacylglycerol acyltransferase: a key mediator of plant triacylglycerol synthesis. Lipids 41:1073–1088

    Article  CAS  PubMed  Google Scholar 

  • Ni L, Snyder M (2001) A genomic study of the bipolar bud site selection pattern in Saccharomyces cerevisiae. Mol Biol Cell 12:2147–2170

    Article  CAS  PubMed  Google Scholar 

  • Nykiforuk CL, Furukawa-Stoffer TL, Huff PW, Sarna M, Laroche A, Moloney MM, Weselake RJ (2002) Characterization of cDNAs encoding diacylglycerol acyltransferase from cultures of Brassica napus and sucrose-mediated induction of enzyme biosynthesis. Biochim Biophys Acta 1580:95–109

    Article  CAS  PubMed  Google Scholar 

  • Oelkers P, Cromley D, Padamsee M, Billheimer JT, Sturley SL (2002) The DGA1 gene determines a second triglyceride synthetic pathway in yeast. J Biol Chem 277:8877–8881

    Article  CAS  PubMed  Google Scholar 

  • Paterson AH, Bowers JE, Bruggmann R et al (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457:551–556

    Article  CAS  PubMed  Google Scholar 

  • Pruitt KD, Tatusova T, Maglott DR (2007) NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res 35:D61–D65

    Article  CAS  PubMed  Google Scholar 

  • Riekhof WR, Wu J, Jones JL, Voelker DR (2007) Identification and characterization of the major lysophosphatidylethanolamine acyltransferase in Saccharomyces cerevisiae. J Biol Chem 282:28344–28352

    Article  CAS  PubMed  Google Scholar 

  • Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542

    Article  PubMed  Google Scholar 

  • Sandager L, Gustavsson MH, Stahl U, Dahlqvist A, Wiberg E, Banas A, Lenman M, Ronne H, Stymne S (2002) Storage lipid synthesis is non-essential in yeast. J Biol Chem 277:6478–6482

    Article  CAS  PubMed  Google Scholar 

  • Schnable PS, Ware D, Fulton RS et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115

    Article  CAS  PubMed  Google Scholar 

  • Shindou H, Shimizu T (2009) Acyl-CoA:lysophospholipid acyltransferases. J Biol Chem 284:1–5

    Article  CAS  PubMed  Google Scholar 

  • Shindou H, Eto M, Morimoto R, Shimizu T (2009) Identification of membrane O- acyltransferase family motifs. Biochem Biophys Res Comm 383:320–325

    Article  CAS  PubMed  Google Scholar 

  • Shockey JM, Gidda SK, Chapital DC, Kuan JC, Dhanoa PK, Bland JM, Rothstein SJ, Mullen RT, Dyer JM (2006) Tung tree DGAT1 and DGAT2 have nonredundant functions in triacylglycerol biosynthesis and are localized to different subdomains of the endoplasmic reticulum. Plant Cell 18:2294–2313

    Article  CAS  PubMed  Google Scholar 

  • Sonnhammer EL, Durbin R (1995) A dot-matrix program with dynamic threshold control suited for genomic DNA and protein sequence analysis. Gene 167:GC1–10

    Article  CAS  PubMed  Google Scholar 

  • Sprecher H (2001) Differences in the regulation of the biosynthesis and esterification of 20- versus 22-carbon polyunsaturated fatty acids. World Rev Nut Dietetics 88:190–195

    Article  CAS  Google Scholar 

  • Stahl U, Stalberg K, Stymne S, Ronne H (2008) A family of eukaryotic lysophospholipid acyltransferases with broad specificity. FEBS Lett 582:305–309

    Article  CAS  PubMed  Google Scholar 

  • Stalberg K, Stahl U, Stymne S, Ohlrogge J (2009) Characterization of two Arabidopsis thaliana acyltransferases with preference for lysophosphatidylethanolamine. BMC Plant Biol 9:60

    Article  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. Biochemical J 223:305–314

    CAS  Google Scholar 

  • Tamaki H, Shimada A, Ito Y, Ohya M, Takase J, Miyashita M, Miyagawa H, Nozaki H, Nakayama R, Kumagai H (2007) LPT1 encodes a membrane-bound O- acyltransferase involved in the acylation of lysophospholipids in the yeast Saccharomyces cerevisiae. J Biol Chem 282:34288–34298

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed  Google Scholar 

  • Vogel JP, Garvin DF, Mockler TC et al (2010) Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 463:763–768

    Article  CAS  Google Scholar 

  • Wang HW, Zhang JS, Gai JY, Chen SY (2006) Cloning and comparative analysis of the gene encoding diacylglycerol acyltransferase from wild type and cultivated soybean. Theor Appl Genet 112:1086–1097

    Article  CAS  PubMed  Google Scholar 

  • Wang LP, Shen WY, Kazachkov M, Chen GQ, Chen QL, Carlsson AS, Stymne S, Weselake RJ, Zou JT (2012) Metabolic interactions between the Lands Cycle and the Kennedy Pathway of glycerolipid synthesis in Arabidopsis developing seeds. Plant Cell 24:4652–4669

    Article  CAS  PubMed  Google Scholar 

  • Weselake RJ, Shah S, Tang MG et al (2008) Metabolic control analysis is helpful for informed genetic manipulation of oilseed rape (Brassica napus) to increase seed oil content. J Exp Bot 59:3543–3549

    Article  CAS  PubMed  Google Scholar 

  • Willert K, Brown JD, Danenberg E, Duncan AW, Weissman IL, Reya T, Yates JR, Nusse R (2003) Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature 423:448–452

    Article  CAS  PubMed  Google Scholar 

  • Xu JY, Francis T, Mietkiewska E, Giblin EM, Barton DL, Zhang Y, Zhang M, Taylor DC (2008) Cloning and characterization of an acyl-CoA-dependent diacylglycerol acyltransferase 1 (DGAT1) gene from Tropaeolum majus, and a study of the functional motifs of the DGAT protein using site-directed mutagenesis to modify enzyme activity and oil content. Plant Biotechnol J 6:799–818

    Article  CAS  PubMed  Google Scholar 

  • Yen CLE, Monetti M, Burri BJ, Farese RV (2005) The triacylglycerol synthesis enzyme DGAT1 also catalyzes the synthesis of diacylglycerols, waxes, and retinyl esters. J Lipid Res 46:1502–1511

    Article  CAS  PubMed  Google Scholar 

  • Yen CL, Stone SJ, Koliwad S, Harris C, Farese RV Jr (2008) Thematic review series: glycerolipids. DGAT enzymes and triacylglycerol biosynthesis. J Lipid Res 49:2283–2301

    Article  CAS  PubMed  Google Scholar 

  • Yu C, Kennedy NJ, Chang CC, Rothblatt JA (1996) Molecular cloning and characterization of two isoforms of Saccharomyces cerevisiae acyl-CoA:sterol acyltransferase. J Biol Chem 271:24157–24163

    Article  CAS  PubMed  Google Scholar 

  • Yu K, Li R, Hatanaka T, Hildebrand D (2008) Cloning and functional analysis of two type 1 diacylglycerol acyltransferases from Vernonia galamensis. Phytochemistry 69:1119–1127

    Article  CAS  PubMed  Google Scholar 

  • Zhang FY, Yang MF, Xu YN (2005) Silencing of DGAT1 in tobacco causes a reduction in seed oil content. Plant Sci 169:689–694

    Article  CAS  Google Scholar 

  • Zhang G, Liu X, Quan Z et al (2012) Genome sequence of foxtail millet (Setaria italica) provides insights into grass evolution and biofuel potential. Nat Biotechnol 30:549–554

    Article  CAS  PubMed  Google Scholar 

  • Zheng P, Allen WB, Roesler K et al (2008) A phenylalanine in DGAT is a key determinant of oil content and composition in maize. Nat Genet 40:367–372

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The work was supported by the Fundamental Scientific Research Funds for CATAS-TCGRI (1630032013009), and Preservation and Utilization of Agricultural and Biological Resources Program from the Department of Agriculture of China (2130135).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Peng Wang or Zhunian Wang.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, P., Wang, Z., Dou, Y. et al. Genome-wide identification and analysis of membrane-bound O-acyltransferase (MBOAT) gene family in plants. Planta 238, 907–922 (2013). https://doi.org/10.1007/s00425-013-1939-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-013-1939-4

Keywords

Navigation