Abstract
Carboxylesterases hydrolyze esters of short-chain fatty acids and have roles in animals ranging from signal transduction to xenobiotic detoxification. In plants, however, little is known of their roles. We have systematically mined the genome from the model plant Arabidopsis thaliana for carboxylesterase genes and studied their distribution in the genome and expression profile across a range of tissues. Twenty carboxylesterase genes (AtCXE) were identified. The AtCXE family shares conserved sequence motifs and secondary structure characteristics with carboxylesterases and other members of the larger α/β hydrolase fold superfamily of enzymes. Phylogenetic analysis of the AtCXE genes together with other plant carboxylesterases distinguishes seven distinct clades, with an Arabidopsis thaliana gene represented in six of the seven clades. The AtCXE genes are widely distributed across the genome (present in four of five chromosomes), with the exception of three clusters of tandemly duplicated genes. Of the interchromosomal duplication events, two have been mediated through newly identified partial chromosomal duplication events that also include other genes surrounding the AtCXE loci. Eighteen of the 20 AtCXE genes are expressed over a broad range of tissues, while the remaining 2 (unrelated) genes are expressed only in the flowers and siliques. Finally, hypotheses for the functional roles of the AtCXE family members are presented based on the phylogenetic relationships with other plant carboxylesterases of known function, their expression profile, and knowledge of likely esterase substrates found in plants.
Similar content being viewed by others
References
SF Altschul TL Madden AA Schäffer J Zhang Z Zhang W Miller DJ Lipman (1997) ArticleTitleGapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res 25 3389–3402 Occurrence Handle9254694
G Blanc A Barakat R Guyot R Cooke M Delseny (2000) ArticleTitleExtensive duplication and reshuffling in the Arabidopsis genome. Plant Cell 12 1093–1101 Occurrence Handle1:CAS:528:DC%2BD3cXlslygtL0%3D Occurrence Handle10899976
R Boskovic KR Tobutt (1998) ArticleTitleInheritance and linkage relationships of isoenzymes in two interspecific cherry progenies. Euphytica 103 273–286 Occurrence Handle10.1023/A:1018664600714 Occurrence Handle1:CAS:528:DyaK1cXntlSqsr0%3D
AM Boutanaev AI Kalmykova YY Shevelyov DI Nurminsky (2002) ArticleTitleLarge clusters of co-expressed genes in the Drosophila genome. Nature 420 666–669 Occurrence Handle10.1038/nature01216 Occurrence Handle1:CAS:528:DC%2BD38XpsVSitbk%3D Occurrence Handle12478293
H Caron B van Schaik M van der Mee F Baas G Riggins P van Sluis MC Hermus R van Asperen K Boon PA Voute S Heisterkamp A van Kampen R Versteeg (2001) ArticleTitleThe human transcriptome map: Clustering of highly expressed genes in chromosomal domains. Science 291 1289–1292 Occurrence Handle1:CAS:528:DC%2BD3MXhtlSgs70%3D Occurrence Handle11181992
BA Cohen RD Mitra JD Hughes GM Church (2000) ArticleTitleA computational analysis of whole-genome expression data reveals chromosomal domains of gene expression. Nat Genet 26 183–186 Occurrence Handle10.1038/79896 Occurrence Handle1:CAS:528:DC%2BD3cXntlGms70%3D Occurrence Handle11017073
M Cygler JD Schrag JL Sussman M Harel I Silman MK Gentry BP Doctor (1993) ArticleTitleRelationship between sequence conservation and three-dimensional structure in a large family of esterases, lipases, and related proteins. Protein Sci 2 366–382 Occurrence Handle1:CAS:528:DyaK3sXksVCitrg%3D Occurrence Handle8453375
A Dansi HD Mignouna J Zoundjihekpon A Sangare R Asiedu N Ahoussou (2000) ArticleTitleUsing isozyme polymorphism to assess genetic variation within cultivated yams (Dioscorea cayenensis/Dioscorea rotundata complex) of the Republic of Benin. Genet Resour Crop Evol 47 371–383 Occurrence Handle10.1023/A:1008718411962
E Eeiner WN Aldridge FCG Hoskin (1989) Enzymes hydrolysing organophosphorous compounds. John Wiley & Sons New York
JC Fachinello S Musacchi S Zuccherelli S Sansavini (2000) ArticleTitleIsoenzymatic variability in pear tissues for fingerprinting. Pesqui Agropecu Bras 35 1427–1432
Felsenstein J (1993) PHYLIP—Phylogeny inference package (version 3.6a2). Distributed by the author (evolution.genetics. washington.edu/phylip.html)
J Hemingway (2000) ArticleTitleThe molecular basis of two contrasting metabolic mechanisms of insecticide resistance. Insect Biochem Mol Biol 30 1009–1015 Occurrence Handle10.1016/S0965-1748(00)00079-5 Occurrence Handle1:CAS:528:DC%2BD3cXmtlOgtr8%3D Occurrence Handle10989287
E Huala A Dickerman M Garcia-Hernandez D Weems L Reiser F LaFond D Hanley D Kiphart J Zhuang W Huang L Mueller D Bhattacharyya D Bhaya B Sobral B Beavis C Somerville S Rhee (2001) ArticleTitleThe 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 Occurrence Handle1:CAS:528:DC%2BD3MXjtlWntLo%3D Occurrence Handle11125061
Y Ichinose Y Hisayasu S Sanematsu Y Ishiga H Seki K Toyoda T Shiraishi T Yamada (2001) ArticleTitleMolecular cloning and functional analysis of pea cDNA E86 encoding homologous protein to hypersensitivity-related hsr203J. Plant Sci 160 997–1006 Occurrence Handle10.1016/S0168-9452(01)00343-0 Occurrence Handle1:CAS:528:DC%2BD3MXisF2kurc%3D Occurrence Handle11297797
AL Kahler RW Allard (1970) ArticleTitleGenetics of isozyme variants in barley. I. Esterases. Crop Sci 10 444–448 Occurrence Handle1:CAS:528:DyaE3cXlt1Ort7s%3D
YS Kim HH Lee MK Ko CE Song CY Bae YH Lee BJ Oh (2001) ArticleTitleInhibition of fungal appressorium formation by pepper (Capsicum annuum) esterase. Mol Plant Microbe Interact 14 80–85 Occurrence Handle1:CAS:528:DC%2BD3MXot1Oh Occurrence Handle11194875
A Kozik E Kochetkova R Michelmore (2002) ArticleTitleGenomePixelizer—A visualization program for comparative genomics within and between species. Bioinformatics 18 335–336 Occurrence Handle10.1093/bioinformatics/18.2.335 Occurrence Handle1:CAS:528:DC%2BD38XitFentr8%3D Occurrence Handle11847088
HM Ku T Vision J Liu SD Tanksley (2000) ArticleTitleComparing sequenced segments of the tomato and Arabidopsis genomes: Large-scale duplication followed by selective gene loss creates a network of synteny. Proc Nat Acad Sci USA 97 9121–9126 Occurrence Handle10.1073/pnas.160271297 Occurrence Handle1:CAS:528:DC%2BD3cXls12ks70%3D Occurrence Handle10908680
J Li J Chory (1998) Preparation of DNA from Arabidopsis. JM Martinez-Zapater J Salinas (Eds) Arabidopsis protocols. Humana Press Totowa, NJ 55–60
T MacDonald JL Brewbaker (1974) ArticleTitleIsoenzyme polymorphism in flowering plants. IX. The E5-E10 esterase loci of maize. J Hered 65 37–42 Occurrence Handle1:CAS:528:DyaE2cXksVOmsr0%3D
AG Manganaris FH Alston (1992) ArticleTitleGenetics of esterase isoenzymes in Malus. Theor Appl Genet 83 467–475
Nicholas KB, Nicholas HBJ (1997) GeneDoc: A tool for editing and annotating multiple sequence alignments (version2.6.002). Distributed by the authors (www.psc.edu/biomed/genedoc/ )
JG Oakeshott C Collet RW Phillis KM Nielsen RJ Russell GK Chambers V Ross RC Richmond (1987) ArticleTitleMolecular cloning and characterization of esterase-6, a serine hydrolase of Drosophila. Proc Natl Acad Sci USA 84 3359–3363 Occurrence Handle1:CAS:528:DyaL2sXls12kt7s%3D Occurrence Handle3106966
JG Oakeshott TM Boyce RJ Russell MJ Healy (1995) ArticleTitleMolecular insights into the evolution of an enzyme: Esterase 6 in Drosophila. Trends Ecol Evol 10 103–110 Occurrence Handle10.1016/S0169-5347(00)89003-5
JG Oakeshott C Claudianos RJ Russell GC Robin (1999) ArticleTitleCarboxyl/cholinesterases: A case study of the evolution of a successful multigene family. Bioessays 21 1031–1042 Occurrence Handle10.1002/(SICI)1521-1878(199912)22:1<1031::AID-BIES7>3.3.CO;2-A Occurrence Handle1:STN:280:DC%2BD3c%2FkslOhsg%3D%3D Occurrence Handle10580988
DL Ollis E Cheah M Cygler B Dijkstra F Frolow SM Franken M Harel SJ Remington I Silman J Schrag JL Sussman KHG Verschueren A Goldman (1992) ArticleTitleThe alpha/beta hydrolase fold. Protein Eng 5 197–211 Occurrence Handle1:CAS:528:DyaK38Xlt1OhtL8%3D Occurrence Handle1409539
RDM Page (1996) ArticleTitleTREEVIEW: An application to display phylogenetic trees on personal computers. Comput Appl Biosci 12 357–358 Occurrence Handle1:STN:280:ByiD2MfgtlA%3D Occurrence Handle8902363
SB Petersen F Drablos (1996) A sequence analysis of lipases, esterases and related proteins. P Woolley SB Petersen (Eds) Lipases: Their structure, biochemistry and application. Cambridge University Press Cambridge 23–48
E Pichersky J Gershenzon (2002) ArticleTitleThe formation and function of plant volatiles: Perfumes for pollinator attraction and defense. Curr Opin Plant Biol 5 237–243
D Pontier L Godiard Y Marco D Roby (1994) ArticleTitle hsr203J, a tobacco gene whose activation is rapid, highly localized and specific for incompatible plant/pathogen interactions. Plant J 5 507–521 Occurrence Handle1:CAS:528:DyaK2MXhsl2gsQ%3D%3D Occurrence Handle8012404
D Pontier M Tronchet P Rogowsky E Lam D Roby (1998) ArticleTitleActivation of hsr203, a plant gene expressed during incompatible plant-pathogen interactions, is correlated with programmed cell death. Mol Plant Microbe Interact 11 544–554 Occurrence Handle1:CAS:528:DyaK1cXjsFSmsro%3D Occurrence Handle9612953
H Ranson C Claudianos F Ortelli C Abgrall J Hemingway MV Sharakhova MF Unger FH Collins R Feyereisen (2002) ArticleTitleEvolution of supergene families associated with insecticide resistance. Science 298 179–181 Occurrence Handle10.1126/science.1076781 Occurrence Handle1:CAS:528:DC%2BD38XnsFSgsrg%3D Occurrence Handle12364796
E Richly J Kurth D Leister (2002) ArticleTitleMode of amplification and reorganization of resistance genes during recent Arabidopsis thaliana evolution. Mol Biol Evol 19 76–84 Occurrence Handle1:CAS:528:DC%2BD38XhtFCitg%3D%3D Occurrence Handle11752192
PJ Roy JM Stuart J Lund SK Kim (2002) ArticleTitleChromosomal clustering of muscle-expressed genes in Caenorhabditis elegans. Nature 418 975–979 Occurrence Handle10.1038/nature01012 Occurrence Handle1:CAS:528:DC%2BD38XmsFWkt78%3D Occurrence Handle12214599
RJ Russell GC Robin P Kostakos RD Newcomb TM Boyce KM Medveczky JG Oakeshott (1996) ArticleTitleMolecular cloning of an alpha-esterase gene cluster on chromosome 3r of Drosophila melanogaster. Insect Biochem Mol Biol 26 235–247 Occurrence Handle10.1016/0965-1748(95)00081-X Occurrence Handle1:CAS:528:DyaK28XitVKrtrc%3D Occurrence Handle8900595
H Sandermann Jr (1992) ArticleTitlePlant metabolism of xenobiotics. Trends Biochem Sci 17 82–84 Occurrence Handle10.1016/0968-0004(92)90507-6 Occurrence Handle1:STN:280:By2B38bot1Y%3D Occurrence Handle1566333
T Satoh M Hosokawa (1998) ArticleTitleThe mammalian carboxylesterases: From molecules to functions. Annu Rev Pharmacol Toxicol 38 257–288
H Schoof P Zaccaria H Gundlach K Lemcke S Rudd G Kolesov R Arnold HW Mewes KF Mayer (2002) ArticleTitleMIPS Arabidopsis thaliana Database (MAtDB): An integrated biological knowledge resource based on the first complete plant genome. Nucleic Acids Res 30 91–93 Occurrence Handle10.1093/nar/30.1.91 Occurrence Handle1:CAS:528:DC%2BD38Xht12kt70%3D Occurrence Handle11752263
C Simillion K Vandepoele MC Van Montagu M Zabeau Y Van De Peer (2002) ArticleTitleThe hidden duplication past of Arabidopsis thaliana. Proc Natl Acad Sci USA 99 13627–13632 Occurrence Handle10.1073/pnas.212522399 Occurrence Handle1:CAS:528:DC%2BD38XotVKmsbY%3D Occurrence Handle12374856
PT Spellman GM Rubin (2002) ArticleTitleEvidence for large domains of similarly expressed genes in the Drosophila genome. J Biol 1 5.1–5.8 Occurrence Handle10.1186/1475-4924-1-5
R Stracke M Werber B Weisshaar (2001) ArticleTitleThe R2R3-MYB gene family in Arabidopsis thaliana. Curr Opin Plant Biol 4 447–456 Occurrence Handle10.1016/S1369-5266(00)00199-0 Occurrence Handle1:CAS:528:DC%2BD3MXmvFKgt74%3D Occurrence Handle11597504
C Stuhlfelder F Lottspeich MJ Mueller (2002) ArticleTitlePurification and partial amino acid sequences of an esterase from tomato. Phytochemistry 60 233–240 Occurrence Handle10.1016/S0031-9422(02)00126-7 Occurrence Handle1:CAS:528:DC%2BD38XjvVakuro%3D Occurrence Handle12031441
JL Sussman M Harel F Frolow C Oefner A Goldman L Toker I Silman (1991) ArticleTitleAtomic structure of acetylcholinesterase from Torpedo californica: A prototypic acetylcholine-binding protein. Science 253 872–879 Occurrence Handle1:CAS:528:DyaK3MXlslyitrc%3D Occurrence Handle1678899
SD Tanksley CM Rick (1980) ArticleTitleGenetics of esterases in species of Lycopersicon. Theor Appl Genet 56 209–219 Occurrence Handle1:CAS:528:DyaL3cXhslOmt7c%3D
P Taylor Z Radic (1994) ArticleTitleThe cholinesterases: From genes to proteins. Annu Rev Pharmacol Toxicol 34 281–320 Occurrence Handle1:CAS:528:DyaK2cXltVamsLo%3D Occurrence Handle8042853
InstitutionalAuthorNameThe Arabidopsis Genome Initiative (2000) ArticleTitleAnalysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408 796–815 Occurrence Handle11130711
JD Thompson TJ Gibson F Plewniak F Jeanmougin DG Higgins (1997) ArticleTitleThe ClustalX windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acid Res 24 4876–4882 Occurrence Handle10.1093/nar/25.24.4876
M Tronchet B Ranty Y Marco D Roby (2001) ArticleTitle HSR203 antisense suppression in tobacco accelerates development of hypersensitive cell death. Plant J 27 115–127 Occurrence Handle10.1046/j.1365-313x.2001.01072.x Occurrence Handle1:CAS:528:DC%2BD3MXmsVyjtrs%3D Occurrence Handle11489189
JM Turner NA Larsen A Basran CF, 3r Barbas NC Bruce IA Wilson RA Lerner (2002) ArticleTitleBiochemical characterization and structural analysis of a highly proficient cocaine esterase. Biochemistry 41 12297–12307 Occurrence Handle10.1021/bi026131p Occurrence Handle1:CAS:528:DC%2BD38XntFejtL0%3D Occurrence Handle12369817
TJ Vision DG Brown DB Shmoys RT Durrett SD Tanksley (2000) ArticleTitleSelective mapping: A strategy for optimizing the construction of high-density linkage maps. Genetics 155 407–420 Occurrence Handle1:STN:280:DC%2BD3c3ltlWhsA%3D%3D Occurrence Handle10790413
RG Vogt LM Riddiford GD Prestwich (1985) ArticleTitleKinetic properties of a sex pheromone-degrading enzyme: The sensillar esterase of Antheraea polyphemus. Proc Natl Acad Sci USA 82 8827–8831 Occurrence Handle1:CAS:528:DyaL28XhtVCqurc%3D Occurrence Handle3001718
AR Walden C Walter RC Gardner (1999) ArticleTitleGenes expressed in Pinus radiata male cones include homologs to anther-specific and pathogenesis response genes. Plant Physiol 121 1103–1116 Occurrence Handle10.1104/pp.121.4.1103 Occurrence Handle1:CAS:528:DyaK1MXotFyju74%3D Occurrence Handle10594098
Acknowledgements
We gratefully acknowledge Julie Nicolls for her assistance in glasshouse work and Revel Drummond for help with cDNA preparation. S.D.G.M. is the recipient of a Bright Futures Enterprise Scholarship from the Foundation for Research, Science and Technology (New Zealand). Funding for this work has been provided by The Foundation for Research, Science and Technology (C06X0207).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Marshall, S.D., Putterill, J.J., Plummer, K.M. et al. The Carboxylesterase Gene Family from Arabidopsis thaliana . J Mol Evol 57, 487–500 (2003). https://doi.org/10.1007/s00239-003-2492-8
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s00239-003-2492-8