Plant Physiology 132:1065-1076 (2003)
© 2003 American Society of Plant Biologists
GENETICS AND MOLECULAR EVOLUTION
Arabidopsis Contains a Large Superfamily of Acyl-Activating Enzymes. Phylogenetic and Biochemical Analysis Reveals a New Class of Acyl-Coenzyme A Synthetases1
Jay M. Shockey,
Martin S. Fulda and
John Browse*
Institute of Biological Chemistry, Washington State University, Pullman, Washington 99164–6340 (J.M.S., M.S.F., J.B.); and Department for Plant Biochemistry, Albrecht-von-Haller-Institute for Plant Sciences, Georg-August-University Goettingen, Justus-von-Liebig-Weg 11, 37077 Goettingen, Germany (M.S.F.)
Acyl-activating enzymes are a diverse group of proteins that catalyze the activation of many different carboxylic acids, primarily through the formation of a thioester bond. This group of enzymes is found in all living organisms and includes the acyl-coenzyme A synthetases, 4-coumarate:coenzyme A ligases, luciferases, and non-ribosomal peptide synthetases. The members of this superfamily share little overall sequence identity, but do contain a 12-amino acid motif common to all enzymes that activate their acid substrates using ATP via an enzyme-bound adenylate intermediate. Arabidopsis possesses an acyl-activating enzyme superfamily containing 63 different genes. In addition to the genes that had been characterized previously, 14 new cDNA clones were isolated as part of this work. The protein sequences were compared phylogenetically and grouped into seven distinct categories. At least four of these categories are plant specific. The tissue-specific expression profiles of some of the genes of unknown function were analyzed and shown to be complex, with a high degree of overlap. Most of the plant-specific genes represent uncharacterized aspects of carboxylic acid metabolism. One such group contains members whose enzymes activate short- and medium-chain fatty acids. Altogether, the results presented here describe the largest acyl-activating enzyme family present in any organism thus far studied at the genomic level and clearly indicate that carboxylic acid activation metabolism in plants is much more complex than previously thought.
Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.103.020552.
1 This work was supported in part by a National Science Foundation postdoctoral fellowship to J.S. (grant no. BIR–9627559), by Dow Chemical Company/Dow AgroSciences (grant to J.B.), by the U.S. Department of Agriculture (grant no. USDA–NRI 2001–35318–10186 to J.B.), and by the Agricultural Research Center at Washington State University.
* Corresponding author; e-mail jab{at}wsu.edu; fax 509–335–2293.
Received January 16, 2003;
returned for revision February 8, 2003;
accepted March 19, 2003.
This article has been cited by other articles:
|
|
|
|
 
S. Reumann, S. Quan, K. Aung, P. Yang, K. Manandhar-Shrestha, D. Holbrook, N. Linka, R. Switzenberg, C. G. Wilkerson, A. P.M. Weber, et al.
In-Depth Proteome Analysis of Arabidopsis Leaf Peroxisomes Combined with in Vivo Subcellular Targeting Verification Indicates Novel Metabolic and Regulatory Functions of Peroxisomes
Plant Physiology,
May 1, 2009;
150(1):
125 - 143.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. de Azevedo Souza, S. S. Kim, S. Koch, L. Kienow, K. Schneider, S. M. McKim, G. W. Haughn, E. Kombrink, and C. J. Douglas
A Novel Fatty Acyl-CoA Synthetase Is Required for Pollen Development and Sporopollenin Biosynthesis in Arabidopsis
PLANT CELL,
February 1, 2009;
21(2):
507 - 525.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. Linka, F. L. Theodoulou, R. P. Haslam, M. Linka, J. A. Napier, H. E. Neuhaus, and A. P.M. Weber
Peroxisomal ATP Import Is Essential for Seedling Development in Arabidopsis thaliana
PLANT CELL,
December 1, 2008;
20(12):
3241 - 3257.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Y. Arai, M. Hayashi, and M. Nishimura
Proteomic Identification and Characterization of a Novel Peroxisomal Adenine Nucleotide Transporter Supplying ATP for Fatty Acid {beta}-Oxidation in Soybean and Arabidopsis
PLANT CELL,
December 1, 2008;
20(12):
3227 - 3240.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
G. Wang, L. Tian, N. Aziz, P. Broun, X. Dai, J. He, A. King, P. X. Zhao, and R. A. Dixon
Terpene Biosynthesis in Glandular Trichomes of Hop
Plant Physiology,
November 1, 2008;
148(3):
1254 - 1266.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Lin and D. J. Oliver
The Role of Acetyl-Coenzyme A Synthetase in Arabidopsis
Plant Physiology,
August 1, 2008;
147(4):
1822 - 1829.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. Kienow, K. Schneider, M. Bartsch, H.-P. Stuible, H. Weng, O. Miersch, C. Wasternack, and E. Kombrink
Jasmonates meet fatty acids: functional analysis of a new acyl-coenzyme A synthetase family from Arabidopsis thaliana
J. Exp. Bot.,
February 10, 2008;
(2008)
erm325v1.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Reumann, L. Babujee, C. Ma, S. Wienkoop, T. Siemsen, G. E. Antonicelli, N. Rasche, F. Luder, W. Weckwerth, and O. Jahn
Proteome Analysis of Arabidopsis Leaf Peroxisomes Reveals Novel Targeting Peptides, Metabolic Pathways, and Defense Mechanisms
PLANT CELL,
October 1, 2007;
19(10):
3170 - 3193.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Footitt, D. Dietrich, A. Fait, A. R. Fernie, M. J. Holdsworth, A. Baker, and F. L. Theodoulou
The COMATOSE ATP-Binding Cassette Transporter Is Required for Full Fertility in Arabidopsis
Plant Physiology,
July 1, 2007;
144(3):
1467 - 1480.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. J. K. Koo, H. S. Chung, Y. Kobayashi, and G. A. Howe
Identification of a Peroxisomal Acyl-activating Enzyme Involved in the Biosynthesis of Jasmonic Acid in Arabidopsis
J. Biol. Chem.,
November 3, 2006;
281(44):
33511 - 33520.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
G. A. Tuskan, S. DiFazio, S. Jansson, J. Bohlmann, I. Grigoriev, U. Hellsten, N. Putnam, S. Ralph, S. Rombauts, A. Salamov, et al.
The genome of black cottonwood, Populus trichocarpa (Torr. & Gray).
Science,
September 15, 2006;
313(5793):
1596 - 1604.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Footitt, J. Marquez, H. Schmuths, A. Baker, F. L. Theodoulou, and M. Holdsworth
Analysis of the role of COMATOSE and peroxisomal beta-oxidation in the determination of germination potential in Arabidopsis
J. Exp. Bot.,
August 1, 2006;
57(11):
2805 - 2814.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. U. Igamberdiev and L. A. Kleczkowski
Equilibration of adenylates in the mitochondrial intermembrane space maintains respiration and regulates cytosolic metabolism
J. Exp. Bot.,
July 1, 2006;
57(10):
2133 - 2141.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. Schneider, L. Kienow, E. Schmelzer, T. Colby, M. Bartsch, O. Miersch, C. Wasternack, E. Kombrink, and H.-P. Stuible
A New Type of Peroxisomal Acyl-Coenzyme A Synthetase from Arabidopsis thaliana Has the Catalytic Capacity to Activate Biosynthetic Precursors of Jasmonic Acid
J. Biol. Chem.,
April 8, 2005;
280(14):
13962 - 13972.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Li, A. L. Schilmiller, G. Liu, G. I. Lee, S. Jayanty, C. Sageman, J. Vrebalov, J. J. Giovannoni, K. Yagi, Y. Kobayashi, et al.
Role of {beta}-Oxidation in Jasmonate Biosynthesis and Systemic Wound Signaling in Tomato
PLANT CELL,
March 1, 2005;
17(3):
971 - 986.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
F. L. Theodoulou, K. Job, S. P. Slocombe, S. Footitt, M. Holdsworth, A. Baker, T. R. Larson, and I. A. Graham
Jasmonic Acid Levels Are Reduced in COMATOSE ATP-Binding Cassette Transporter Mutants. Implications for Transport of Jasmonate Precursors into Peroxisomes
Plant Physiology,
March 1, 2005;
137(3):
835 - 840.
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. E. Turner, K. Greville, E. C. Murphy, and M. A. Hooks
Characterization of Arabidopsis Fluoroacetate-resistant Mutants Reveals the Principal Mechanism of Acetate Activation for Entry into the Glyoxylate Cycle
J. Biol. Chem.,
January 28, 2005;
280(4):
2780 - 2787.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. L. Fatland, B. J. Nikolau, and E. S. Wurtele
Reverse Genetic Characterization of Cytosolic Acetyl-CoA Generation by ATP-Citrate Lyase in Arabidopsis
PLANT CELL,
January 1, 2005;
17(1):
182 - 203.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Reumann, C. Ma, S. Lemke, and L. Babujee
AraPerox. A Database of Putative Arabidopsis Proteins from Plant Peroxisomes
Plant Physiology,
September 1, 2004;
136(1):
2587 - 2608.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. G. Jones, J. Hughes, A. Tregova, J. Milne, A. B. Tomsett, and H. A. Collin
Biosynthesis of the flavour precursors of onion and garlic
J. Exp. Bot.,
August 1, 2004;
55(404):
1903 - 1918.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Fulda, J. Schnurr, A. Abbadi, E. Heinz, and J. Browse
Peroxisomal Acyl-CoA Synthetase Activity Is Essential for Seedling Development in Arabidopsis thaliana
PLANT CELL,
February 1, 2004;
16(2):
394 - 405.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
