Abstract
In banana, ethylene production for ripening is accompanied by a dramatic increase in 1-aminocyclopropane-1-carboxylate (ACC) content, transcript level of Musa acuminata ACC synthase 1 (MA-ACS1) and the enzymatic activity of ACC synthase 1 at the onset of the climacteric period. MA-ACS1 catalyses the conversion of S-adenosyl-L-methionine (SAM) to ACC, the key regulatory step in ethylene biosynthesis. Multiple sequence alignments of 1- aminocyclopropane-1-carboxylate synthase (ACS) amino acid sequences based on database searches have indicated that MA-ACS1 is a highly conserved protein across the plant kingdom. This report describes an in silico analysis to provide the first important insightful information about the sequential, structural and phylogenetic characteristics of MA-ACS1. The three-dimensional structure of MA-ACS1, constructed based on homology modelling, in combination with the available data enabled a comparative mechanistic analysis of MA-ACS1 to explain the catalytic roles of the conserved and non-conserved active site residues. We have further demonstrated that, as in apple and tomato, banana- ACS1 (MA-ACS1) forms a homodimer and a complex with cofactor pyridoxal-5′-phosphate (PLP) and inhibitor aminoethoxyvinylglycine (AVG). We have also predicted that the residues from the PLP-binding pocket, essential for ligand binding, are mostly conserved across the MA-ACS1 structure and the competitive inhibitor AVG binds at a location adjacent to PLP.
Similar content being viewed by others
Abbreviations
- AATase:
-
aspartate aminotransferase
- ACC:
-
1-aminocyclopropane-1-carboxylate
- AVG:
-
aminoethoxyvinylglycine
- CDD:
-
Conserved Domain Database
- DOPE:
-
discrete optimized protein energy
- MA-ACS1 :
-
Musa acuminata ACC synthase 1
- MACC:
-
N-manonyl ACC
- MTA:
-
5′ methylthioadenosine
- MVG:
-
methoxyvinylglycine
- PLP:
-
pyridoxal-5′-phosphate
- RMSD:
-
root mean square deviation
- SAM:
-
S-adenosyl-L-methionine
- TATase:
-
tyrosine aminotransferase
References
Alexander L and Grierson D 2002 Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening; J. Exp. Bot. 53 2039–2055
Altschul S F, Madden T L, Schaffer A A, Zhang J, Zhang Z, Miller W and Lipman D J 1997 D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs; Nucleic Acids Res. 25 3389–3402
Baker D and Sali A 2001 Protein structure prediction and structural genomics; Science 294 93–96
Ballesteros J A, Shi L and Javitch J A 2001 Structural mimicry in G protein coupled receptors: implications of the high-resolution structure of rhodopsin for structure-function analysis of rhodopsin-like receptors; Mol. Pharmacol. 60 1–19
Barry C S, Llop-Tous M I and Grierson D 2000 The regulation of 1- aminocyclopropane-1-carboxylic acid synthase gene expression during the transition from system-1 to system-2 ethylene synthesis in tomato; Plant Physiol. 123 979–986
Berezin C, Glaser F, Rosenberg Y, Paz I, Pupko T, Fariselli P, Casadio R and Ben-Tal N 2004 ConSeq: the identification of functionally and structurally important residues in protein sequences; Bioinformatics 20 1322–1324
Blom N, Gammeltoft S and Brunak S 1999 Sequence and structurebased prediction of eukaryotic protein phosphorylation sites; J. Mol. Biol. 294 1351–1362
Bohne-Lang A and Vonder Lieth C W 2005 GlyProt: in silico glycosylation of proteins; Nucleic Acids Res. 33 W214–W219
Boller T, Herner R C and Kende H 1979 Assay for and enzymatic formation of an ethylene precursor, 1-aminocyclopropane-1-carboxylic acid (tomatoes); Planta 145 293–303
Bourdon H, Trumpp-Kallmeyer S, Schreuder H, Hoflack J, Hibert M and Wermuth C G 1997 Modelling of the binding site of the human m1 muscarinic receptor: experimental validation and refinement; J. Comput. Aided Mol. Des. 11 317–332
Capitani G, Eliot A C, Gut H, Khomutov R M, Kirsch J F and Grutter M G 2003 Structure of 1-aminocyclopropane-1-carboxylate synthase in complex with an amino-oxy analogue of the substrate: implications for substrate binding; Biochem. Biophys. Acta 1647 55–60
Capitani G, Hohenester E, Feng L, Storici P, Kirsch J F and Jansonius J N 1999 Structure of 1-aminocyclopropane-1-carboxylate synthase, a key enzyme in the biosynthesis of the plant hormone ethylene; J. Mol. Biol. 294 745–756
Capitani G, Mc Carthy D L, Gut H, Grutter M G and Kirsch J F 2002 Apple of 1-aminocyclopropane-1-carboxylate synthase in complex with the inhibitor L-aminoethoxyvinylglycine. Evidence for a ketimine intermediate; J. Biol. Chem. 277 49735–49742
Christen P and Metzler D 1985 Transaminases (New York: Wiley)
Clendennen K S and May D G 1997 Differential gene expression in ripening banana fruit; Plant Physiol. 115 463–469
Colovos C and Yeates T O 1993 Verification of protein structures: patterns of nonbonded atomic interactions; Protein Sci. 2 1511–1519
Escherich A, Lutz J, Escrieut C, Fourmy D, Van Neuren A S and Muller G 2000 Peptide/benzodiazepine hybrids as ligands of CCK(A) and CCK(B) receptors; Biopolymers 56 55–76
Feng L and Kirsch J F 2000 L-Vinylglycine is an alternative substrate as well as mechanism based inhibitor of 1-aminocyclopropane-1-carboxylate synthase; Biochemistry 39 2436–2444
Garcia-Nieto R, Perez C and Gago F 2000 Automated docking and molecular dynamics simulations of nimesulide in the cyclooxygenase active site of human prostaglandinendoperoxide synthase-2 (COX-2); J. Comput. Aided Mol. Des. 14 147–160
Gribskov M, Burgess R R and Devereux J 1986 PEPPLOT, a protein secondary structure analysis program for the UWGCG sequence analysis software package; Nucleic Acids Res. 14 327–334
Guex N and Peitsch M C 1997 SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling; Electrophoresis 18 2714–2723
Hall T A 1991 BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT; Nucleic Acids Symposium Series 41 95–98
Huai Q, Xia Y, Chen Y, Callahan B, Li N and Ke H 2001 Crystal structures of 1-aminocyclopropane-1-carboxylate (ACC) synthase in complex with aminoethoxyvinylglycine and pyridoxal-5-phosphate provide new insight into catalytic mechanisms; J. Biol. Chem. 276 38210–38216
Huang F C, Do Y Y and Huang P L 2006 Genomic organization of a diverse ACC synthase gene family in banana and expression characteristics of the gene member involved in ripening of banana fruits; J. Agric. Food Chem. 54 3859–3868
Hyodo H and Tanaka K 1986 Inhibition of 1-aminocyclopropane-1-carboxylic acid synthase activity by polyamines, their related compounds and metabolites of S-adenosylmethionine; Plant Cell Physiol. 27 391–398
Jakubowicz M 2002 Structure, catalytic activity and evolutionary relationships of 1-aminocyclopropane-1-carboxylate synthase, the key enzyme of ethylene synthesis in higher plants; Acta Biochim. Polon. 49 757–774
Jansonius J N 1998 Structure, evolution and action of vitamin-B6 dependent enzymes; Curr. Opin. Struc. Biol. 8 759–769
John P 1991 How plant molecular biologists reveal a surprising relationship between two enzymes, which took an enzyme out of a membrane where it was not located and put it into a soluble phase where it could be studied; Plant Mol. Biol. Rep. 9 192–194
Kalé L, Skeel R, Bhandarkar M, Brunner R, Gursoy A, Krawetz N, Phillips J, Shinozaki A et al. 1999 NAMD2: greater scalability for parallel molecular dynamics; J. Comp. Physiol. 151 283–312
Kende H 1989 Ripening of climacteric fruits initiated at low ethylene levels; Plant Physiol. 91 1–4
Kende H 1993 Enzymes of ethylene biosynthesis; Annu. Rev. Plant Physiol. Plant Mol. Biol. 44 283–307
Kiyama R, Tamura Y, Watanabe F, Tsuzuki H, Ohtani M and Yodo M 1999 Homology modeling of gelatinase catalytic domains and docking simulations of novel sulfonamide inhibitors; J. Med. Chem. 42 1723–1738
Laemmli U K 1970 Cleavage of structural proteins during the assembly of the head of bacteriophage T4; Nature (London) 227 680–685
Laskoswki R A, MacArthur M W, Moss D S and Thornton J M 1993 PROCHECK: a program to check the stereochemical quality of protein structures; J. Appl. Crystallogr. 26 283–291
Le Novere N, Grutter T and Changeux J P 2002 Models of the extracellular domain of the nicotinic receptors and of agonist- and Ca2+-binding sites; Proc. Natl. Acad. Sci. USA 99 3210–3215
Liu X, Shiomi S, Nakatsuka A, Kubo Y, Nakamura R and Inaba A 1999 Characterization of ethylene biosynthesis associated with ripening in banana fruit; Plant Physiol. 121 1257–1265
Lizada M C C and Yang S F 1979 A simple sensitive assay for 1-aminocyclopropane-1-carboxylic acid; Anal. Biochem. 100 140–145
Luthy R, Bowie J U and Eisenberg D 1992 Assessment of protein models with three-dimensional profiles; Nature (London) 356 83–85
Marchler-Bauer A, Anderson J B, DeWeese-Scott C, Fedorova N D, Geer L Y, He S, Hurwitz D I, Jackson J D, et al. 2003 CDD: a curated Entrez database of conserved domain alignments; Nucleic Acids Res. 31 383–387
Marti-Renom M A, Stuart A, Fiser A, Sanchez R, Melo F and Sali A 2000 Comparative protein structure modeling of genes and genomes; Annu. Rev. Biophys. Biomol. Struct. 29 291–325
Mehta P K, Hale T I and Christen P 1993 Aminotransferases: demonstration of homology and division into evolutionary subgroups; Eur. J. Biochem. 214 549–561
Nakatsuka A, Murachi S, Okunishi H, Shiomi S, Nakano R, Kubo Y and Inaba A 1998 Differential expression and internal feedback regulation of 1-aminocyclopropane-1-carboxylate synthase, 1-aminocyclopropane-1-carboxylate oxidase and ethylene receptor genes in tomato fruit during development and ripening; Plant Physiol. 118 1295–1305
Rong S B, Zhang J, Neale J H, Wroblewski J T, Wang S and Kozikowski A P 2002 Molecular modeling of the interactions of glutamate carboxypeptidase II with its potent NAAG-based inhibitors; J. Med. Chem. 45 4140–4152
Roy Choudhury S, Roy S, Saha P P, Singh S K and Sengupta D N 2008a Characterization of differential ripening pattern in association with ethylene biosynthesis in the fruits of five naturally occurring banana cultivars and detection of a GCC-box specific DNA binding protein; Plant Cell Rep. 27 1235–1249
Roy Choudhury S, Roy S and Sengupta D N 2008b Characterization of transcriptional profiles of MA-ACS1 and MA-ACO1 genes in response to ethylene, auxin, wounding, cold and different photoperiods during ripening in banana fruit; J. Plant Physiol. 165 1865–1878
Sambrook J, Fritsch E F and Maniatis T 1989 Molecular cloning: a laboratory manual (New York: Cold Spring Harbor Laboratory, Cold Spring Harbor Press)
Satoh S, Mori H and Imaseki H 1993 Monomeric and dimeric forms and the mechanism based inactivation of 1-aminocyclopropane-1-carboxylate synthase; Plant Cell Physiol. 34 753–760
Schultz J, Milpetz F, Bork P and Ponting C P 1998 SMART, a simple modular architecture research tool: identification of signaling domains; Proc. Natl. Acad. Sci. USA 95 5857–5864
Shen M-Y and Sali A 2006 Statistical potential for assessment and prediction of protein structures; Protein Sci. 15 2507–2524
Singh S K, Roy Choudhury S, Roy S and Sengupta D N 2008 Sequential, structural, and phylogenetic study of BRCT module in plants; J. Biomol. Struct. Dyn. 26 235–245
Sorokine A, Prilusky J, Abola E E and Edelman M 1999 Automated analysis of interatomic contacts in proteins; Bioinformatics 15 327–332
Tamura K, Dudley J, Nei M and Kumar S 2007 MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0; Mol. Biol. Evol. 24 1596–1599
Thompson J D, Higgins D J and Gibson T J 1994 CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice; Nucleic Acids Res. 22 4673–4680
Tiraboschi G, Jullian N, Thery V, Antonczak S, Fournie-Zaluski M C and Roques B P 1999 A three-dimensional construction of the active site (region 507–749) of human neutral endopeptidase (EC.3.4.24.11); Protein Eng. 12 141–149
Vriend G and Sander C 1993 Quality-control of protein models- directional atomic contact analysis; J. Appl. Crystallogr. 26 47–60
Weisel M, Proschak E and Schneider G 2007 PocketPicker: analysis of ligand binding-sites with shape descriptors; Chem. Cent. J. 1 7
Wills R B H, Warton M A D, Mussa M D N and Chew L P 2001 Ripening of climacteric fruits initiated at low ethylene levels; Aust. J. Exp. Agric. 41 89–92
Wong W S, Ning W P, Xu L, Kung S D, Yang S F and Li N 1999 Identification of two chilling-regulated 1-aminocyclopropane 1-carboxylate synthase genes from citrus fruit; Plant Mol. Biol. 41 587–600
Yang S F and Hoffman N E 1984 Ethylene biosynthesis and its regulation in higher plants; Annu. Rev. Plant Physiol. 35 155–189
Yu X, Chen M and Liu C 2008 Nucleocytoplasmic-localized acyltransferases catalyze the malonylation of 7-Oglycosidic (iso) flavones in Medicago truncatula; Plant J. 55 382–396
Author information
Authors and Affiliations
Corresponding author
Additional information
These authors have contributed equally to this work.
Supplementary figures and table pertaining to this article are available on the Journal of Biosciences Website at http://www.ias.ac.in/jbiosci/June2010/pp281-294/suppl.pdf
Rights and permissions
About this article
Cite this article
Choudhury, S.R., Singh, S.K., Roy, S. et al. An insight into the sequential, structural and phylogenetic properties of banana 1-aminocyclopropane-1-carboxylate synthase 1 and study of its interaction with pyridoxal-5′-phosphate and aminoethoxyvinylglycine. J Biosci 35, 281–294 (2010). https://doi.org/10.1007/s12038-010-0032-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12038-010-0032-4