Acetyl-Coenzyme A Carboxylase: Quaternary Structure and Inhibition by Graminicidal Herbicides

Abstract Aryloxyphenoxypropionates (AOPPs) and cyclohexanediones (CHDs) are two classes of postemergence herbicides that are used for the control of annual and perennial grasses in broadleaf crops. The herbicidal properties of these distinct chemistries were discovered in the early 1970s, and since that time there has been considerable effort spent to elucidate the mode of action and their respective target sites. Both cyclohexanediones and aryloxyphenoxypropionates show similar species specificity profiles and symptoms in susceptible plants. Based on these similarities, it has been postulated that both classes of herbicides target the same system. It has been proposed (1, 2) that this target site is the biotin-containing enzyme acetyl-coenzyme A carboxylase (E.C. 6.4.1.2). Acetyl-coenzyme A carboxylase (ACCase) is the first dedicated enzyme in thede novofatty acid biosynthetic pathway. ACCase catalyzes the ATP-dependent conversion of acetyl-coenzyme A to malonyl-coenzyme A. First discovered in 1959, ACCase has since been investigated in a variety of mammalian, prokaryotic, and plant species. In all species studied, ACCase plays the same role in fatty acid biosynthesis, despite vast differences in its regulation and protein structure. The implication that ACCase is the target site for the AOPP and CHD classes of herbicides has been supported by the work of many researchers; however, there are discrepancies in the literature with respect to the quaternary structure of ACCase and its role as the only site of action for these herbicides. Similarly, it is commonly believed that resistance to these herbicides is due to an altered form of this enzyme. While it is true that the evidence supporting these hypotheses are convincing, alternative modes of action and mechanisms of resistance have been proposed and cannot be discredited without proper examination. The purpose of this paper is to review the literature on (i) the ACCase quaternary structure in plants compared to prokaryotic and mammalian enzymes, (ii) the regulation of mammalian, prokaryotic, and plant ACCase, (iii) the modes of action of CHDs and AOPPs and their target sites, and (iv) the mechanisms by which plants are rendered susceptible to these classes of graminaceous herbicides.

[1]  D. Wyse,et al.  Dominant mutations causing alterations in acetyl-coenzyme A carboxylase confer tolerance to cyclohexanedione and aryloxyphenoxypropionate herbicides in maize. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[2]  S. Powles,et al.  HERBICIDE MULTIPLE-RESISTANCE IN A LOLIUM-RIGIDUM BIOTYPE IS ENDOWED BY MULTIPLE MECHANISMS - ISOLATION OF A SUBSET WITH RESISTANT ACETYL-COA CARBOXYLASE , 1994 .

[3]  F. Germino,et al.  Screening for in vivo protein-protein interactions. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[4]  B. Kemp,et al.  Insulin activation of acetyl-CoA carboxylase accompanied by inhibition of the 5'-AMP-activated protein kinase. , 1992, The Journal of biological chemistry.

[5]  C. Job,et al.  Kinetics of the two forms of acetyl-CoA carboxylase from Pisum sativum. Correlation of the substrate specificity of the enzymes and sensitivity towards aryloxyphenoxypropionate herbicides. , 1994, European journal of biochemistry.

[6]  T. Morris,et al.  Expression, biotinylation and purification of a biotin-domain peptide from the biotin carboxy carrier protein of Escherichia coli acetyl-CoA carboxylase. , 1994, The Biochemical journal.

[7]  J. Ebel,et al.  Comparison of acetyl-CoA carboxylases from parsley cell cultures and wheat germ. , 1980, Archives of biochemistry and biophysics.

[8]  K. Kim,et al.  Regulation of acetyl-CoA carboxylase gene expression. Insulin induction of acetyl-CoA carboxylase and differentiation of 30A5 preadipocytes require prior cAMP action on the gene. , 1991, The Journal of biological chemistry.

[9]  J. Holtum,et al.  Cross-Resistance to Herbicides in Annual Ryegrass (Lolium rigidum): IV. Correlation between Membrane Effects and Resistance to Graminicides. , 1991, Plant physiology.

[10]  K. Kim,et al.  Critical phosphorylation sites for acetyl-CoA carboxylase activity. , 1994, The Journal of biological chemistry.

[11]  H. Wood,et al.  Purification of the subunits of transcarboxylase by affinity chromatography on avidin-sepharose. , 1975, The Journal of biological chemistry.

[12]  H. Wood,et al.  Transcarboxylase. 8. Isolation and properties of a biotin-carboxyl carrier protein. , 1969, Proceedings of the National Academy of Sciences of the United States of America.

[13]  D. Wyse,et al.  Selection and characterization of sethoxydim- tolerant maize tissue cultures. , 1990, Plant physiology.

[14]  B. Burns,et al.  Acetyl-CoA carboxylase activity in Helicobacter pylori and the requirement of increased CO2 for growth. , 1995, Microbiology.

[15]  W. Cleland,et al.  Carbon-13 and deuterium isotope effects on the catalytic reactions of biotin carboxylase. , 1988, Biochemistry.

[16]  L. Abu‐Elheiga,et al.  ヒトアセチルCoAカルボキシラーゼ 特性化,分子クローニングおよび2つのイソフォームの証拠 , 1995 .

[17]  J. Markham,et al.  Biotin carboxyl carrier protein and carboxyltransferase subunits of the multi-subunit form of acetyl-CoA carboxylase from Brassica napus: cloning and analysis of expression during oilseed rape embryogenesis. , 1996, The Biochemical journal.

[18]  D. Wyse,et al.  Expression of the Acc1 Gene-Encoded Acetyl-Coenzyme A Carboxylase in Developing Maize (Zea mays L.) Kernels , 1993, Plant physiology.

[19]  S. Chirala,et al.  Cloning of the yeast FAS3 gene and primary structure of yeast acetyl-CoA carboxylase. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[20]  J. Schell,et al.  A Gene Encoding Acetyl-Coenzyme A Carboxylase from Brassica napus , 1994, Plant physiology.

[21]  W. Cleland,et al.  Catalytic mechanism of biotin carboxylase: steady-state kinetic investigations. , 1988, Biochemistry.

[22]  J. Holtum,et al.  Cross-Resistance to Herbicides in Annual Ryegrass (Lolium rigidum) : II. Chlorsulfuron Resistance Involves a Wheat-Like Detoxification System. , 1991, Plant physiology.

[23]  R. H. Shimabukuro,et al.  Effects of diclofop and diclofop-methyl on the membrane potentials of wheat and oat coleoptiles. , 1987, Plant physiology.

[24]  M. Utter,et al.  Pyruvate carboxylase from chicken liver. Steady state kinetic studies indicate a "two-site" ping-pong mechanism. , 1972, The Journal of biological chemistry.

[25]  D. Wyse,et al.  Mechanism of diclofop resistance in an Italian ryegrass (Lolium multiflorum Lam.) biotype , 1992 .

[26]  K. Kim,et al.  Identification of a second human acetyl-CoA carboxylase gene. , 1996, The Biochemical journal.

[27]  W. Cleland,et al.  Rat liver pyruvate carboxylase. II. Kinetic studies of the forward reaction. , 1971, The Journal of biological chemistry.

[28]  S. Powles,et al.  Cross-Resistance to Herbicides in Annual Ryegrass (Lolium rigidum): I. Properties of the Herbicide Target Enzymes Acetyl-Coenzyme A Carboxylase and Acetolactate Synthase. , 1990, Plant physiology.

[29]  Anna Nordlund,et al.  Regulation of intracellular acetyl-CoA carboxylase by ATP depletors mimics the action of the 5'-AMP-activated protein kinase. , 1991, Biochemical and biophysical research communications.

[30]  S. Chirala,et al.  Human acetyl-CoA carboxylase: characterization, molecular cloning, and evidence for two isoforms. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[31]  D. Wyse,et al.  Inhibition of corn acetyl-CoA carboxylase by cyclohexanedione and aryloxyphenoxypropionate herbicides☆ , 1989 .

[32]  H. Wood The reactive group of biotin in catalysis by biotin enzymes , 1976 .

[33]  F. Taroni,et al.  Sequence analysis, biogenesis, and mitochondrial import of the alpha-subunit of rat liver propionyl-CoA carboxylase. , 1989, The Journal of biological chemistry.

[34]  T. Monaco,et al.  Effect of fenoxaprop, haloxyfop and sethoxydim on acetyl coenzyme A carboxylase from rice, barnyardgrass and sprangletop , 1991 .

[35]  R. Fischer,et al.  Inhibition of acetyl-coenzyme A carboxylase by the novel grass-selective herbicide 3-(2,4-dichlorophenyl)-perhydroindolizine-2,4-dione , 1991 .

[36]  J. Ohlrogge,et al.  In vivo pools of free and acylated acyl carrier proteins in spinach. Evidence for sites of regulation of fatty acid biosynthesis. , 1991, The Journal of biological chemistry.

[37]  C. Georgopoulos,et al.  The lethal phenotype caused by null mutations in the Escherichia coli htrB gene is suppressed by mutations in the accBC operon, encoding two subunits of acetyl coenzyme A carboxylase , 1992, Journal of bacteriology.

[38]  B. Gerwick Potential Mechanisms for Bentazon Antagonism by Haloxyfop , 1988, Weed Science.

[39]  E. Wurtele,et al.  Genomic organization of 251 kDa acetyl-CoA carboxylase genes in Arabidopsis: tandem gene duplication has made two differentially expressed isozymes. , 1995, Plant & cell physiology.

[40]  H. Kondo,et al.  Acetyl-CoA carboxylase from Escherichia coli: gene organization and nucleotide sequence of the biotin carboxylase subunit. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[41]  J. Moss,et al.  Acetyl coenzyme A carboxylase system of Escherichia coli. Purification and properties of the biotin carboxylase, carboxyltransferase, and carboxyl carrier protein components. , 1974, The Journal of biological chemistry.

[42]  H. Hoppe,et al.  Inhibition of fatty acid biosynthesis in isolated bean and maize chloroplasts by herbicidal phenoxy-phenoxypropionic acid derivatives and structurally related compounds , 1985 .

[43]  E. Stobbe,et al.  The Basis of the Antagonistic Effect of 2,4-D on Diclofop-Methyl Toxicity to Wild Oat (Avena fatua) , 1980, Weed Science.

[44]  W. Cleland,et al.  Rat liver pyruvate carboxylase. 3. Isotopic exchange studies of the first partial reaction. , 1971, The Journal of biological chemistry.

[45]  J. Ohlrogge,et al.  The pea chloroplast membrane-associated protein, IEP96, is a subunit of acetyl-CoA carboxylase. , 1996, The Plant journal : for cell and molecular biology.

[46]  J. Cronan,et al.  Growth rate regulation of Escherichia coli acetyl coenzyme A carboxylase, which catalyzes the first committed step of lipid biosynthesis , 1993, Journal of bacteriology.

[47]  M. Lane,et al.  Acetyl coenzyme A carboxylase system of Escherichia coli. Studies on the mechanisms of the biotin carboxylase- and carboxyltransferase-catalyzed reactions. , 1974, The Journal of biological chemistry.

[48]  D. Hardie,et al.  Evidence that AMP triggers phosphorylation as well as direct allosteric activation of rat liver AMP-activated protein kinase. A sensitive mechanism to protect the cell against ATP depletion. , 1991, European journal of biochemistry.

[49]  N. Martini,et al.  Molecular Cloning of cDNAs or Genes Encoding Proteins Involved in de novo Fatty Acid Biosynthesis in Plants , 1994 .

[50]  R. Douce,et al.  Localization and characterization of two structurally different forms of acetyl-CoA carboxylase in young pea leaves, of which one is sensitive to aryloxyphenoxypropionate herbicides. , 1994, The Biochemical journal.

[51]  J. Holtum,et al.  Resistant Acetyl-CoA Carboxylase is a Mechanism of Herbicide Resistance in a Biotype of Avena sterilis ssp. ludoviciana , 1994 .

[52]  T. Konishi,et al.  Acetyl-CoA carboxylase in higher plants: most plants other than gramineae have both the prokaryotic and the eukaryotic forms of this enzyme. , 1996, Plant & cell physiology.

[53]  N. Iritani Nutritional and hormonal regulation of lipogenic-enzyme gene expression in rat liver. , 1992, European journal of biochemistry.

[54]  H. Hoppe Veränderungen der Membranpermeabilität, des Kohlenhydratgehaltes, des Lipidgehaltes and der Lipidzusammensetzung in Keimwurzelspitzen von Zea mays L. nach Behandlung mit Diclofop-methyl , 1980 .

[55]  D. Winkler,et al.  A molecular graphics study of factors influencing herbicidal activity of oximes of 3-acyl-tetrahydro-2H-pyran-2,4-diones , 1989 .

[56]  D. Hardie,et al.  Inactivation of acetyl-CoA carboxylase and activation of AMP-activated protein kinase in muscle during exercise. , 1996, The American journal of physiology.

[57]  D. Wyse,et al.  Mechanism of Inheritance of Diclofop Resistance in Italian Ryegrass (Lolium multiflorum) , 1992, Weed Science.

[58]  C. G. Kannangara,et al.  Fat metabolism in higher plants. LIV. A procaryotic type acetyl CoA carboxylase in spinach chloroplasts. , 1972, Archives of biochemistry and biophysics.

[59]  A. Rendina,et al.  Inhibition of acetyl-coenzyme A carboxylase by two classes of grass-selective herbicides , 1990 .

[60]  A. Slabas,et al.  Plant acetyl-CoA carboxylase. , 1986, Biochemical Society transactions.

[61]  M. Devine,et al.  Investigation of the mechanism of diclofop resistance in two biotypes of Avena fatua , 1992 .

[62]  P. Stumpf,et al.  Regulation of Plant Acetyl-CoA Carboxylase by Adenylate Nucleotides. , 1983, Plant physiology.

[63]  M. Yamada,et al.  The light-dependent step of de novo synthesis of long chain fatty acids in spinach chloroplasts , 1979 .

[64]  R. Haselkorn,et al.  Wheat acetyl-coenzyme A carboxylase: cDNA and protein structure. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[65]  R. Winz,et al.  Isolation of cDNAs from Brassica napus encoding the biotin-binding and transcarboxylase domains of acetyl-CoA carboxylase: assignment of the domain structure in a full-length Arabidopsis thaliana genomic clone. , 1994, Biochemical Journal.

[66]  V. Buneva,et al.  Interaction of ATP with acetyl-CoA carboxylase from rat liver. The role of the polyphosphate chain. Affinity labelling with alkylating amides of ATP and ADP. , 1990, Biochimie.

[67]  T. Hashimoto,et al.  Kinetic studies on the reaction mechanism and the citrate activation of liver acetyl coenzyme A carboxylase. , 1971, European journal of biochemistry.

[68]  J. Ohlrogge,et al.  Regulation of plant Fatty Acid biosynthesis : analysis of acyl-coenzyme a and acyl-acyl carrier protein substrate pools in spinach and pea chloroplasts. , 1992, Plant physiology.

[69]  P. Attwood,et al.  Bicarbonate-dependent ATP cleavage catalysed by pyruvate carboxylase in the absence of pyruvate. , 1992, The Biochemical journal.

[70]  H. G. Wood,et al.  Transcarboxylase: role of biotin, metals, and subunits in the reaction and its quaternary structure. , 1976, CRC critical reviews in biochemistry.

[71]  A. Appleby,et al.  Antagonism of Haloxyfop Activity in Tall Fescue (Festuca arundinacea) by Dicamba and Bentazon , 1991, Weed Science.

[72]  P. Andrews,et al.  Analysis of the biotin-binding site on acetyl-CoA carboxylase from rat. , 1989, European journal of biochemistry.

[73]  C. Preston,et al.  Multiple resistance to dissimilar herbicide chemistries in a biotype of Lolium rigidum due to enhanced activity of several herbicide degrading enzymes , 1996 .

[74]  D. Wyse,et al.  Inhibition of plant acetyl-coenzyme A carboxylase by the herbicides sethoxydim and haloxyfop. , 1987, Biochemical and biophysical research communications.

[75]  J. Cronan,et al.  The gene encoding the biotin carboxylase subunit of Escherichia coli acetyl-CoA carboxylase. , 1992, The Journal of biological chemistry.

[76]  B. Kemper,et al.  Structure of the rabbit cytochrome P450IIC3 gene, a constitutive member of the P450IIC subfamily. , 1990, Biochemistry.

[77]  D. Dennis,et al.  Acetyl-coenzyme A carboxylase from the developing endosperm of Ricinus communis. II. A two-site kinetic mechanism. , 1983, Archives of biochemistry and biophysics.

[78]  R. Dixon,et al.  Molecular cloning, characterization, and elicitation of acetyl-CoA carboxylase from alfalfa. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[79]  D. Wyse,et al.  Kinetics of inhibition of acetyl-coenzyme A carboxylase by sethoxydim and haloxyfop☆ , 1991 .

[80]  Alison M. Smith,et al.  Purification and Characterization of Acetyl CoA Carboxylase from Developing Pea Embryos , 1992 .

[81]  P. Wheeler,et al.  Lipid synthesis in mycobacteria: characterization of the biotin carboxyl carrier protein genes from Mycobacterium leprae and M. tuberculosis , 1994, Journal of bacteriology.

[82]  T. Konishi,et al.  Compartmentalization of two forms of acetyl-CoA carboxylase in plants and the origin of their tolerance toward herbicides. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[83]  M. Takagi,et al.  Biochemical Effects of Sethoxydim in Excised Root Tips of Corn (Zea mays) , 1987, Weed Science.

[84]  A. Rendina,et al.  Kinetic characterization, stereoselectivity, and species selectivity of the inhibition of plant acetyl-CoA carboxylase by the aryloxyphenoxypropionic acid grass herbicides. , 1988, Archives of biochemistry and biophysics.

[85]  D. Dennis,et al.  Acetyl-coenzyme A carboxylase from the developing endosperm of Ricinus communis. I. Isolation and characterization. , 1983, Archives of biochemistry and biophysics.

[86]  J. Cronan,et al.  The genes encoding the two carboxyltransferase subunits of Escherichia coli acetyl-CoA carboxylase. , 1992, The Journal of biological chemistry.

[87]  Graminicide resistance of acetyl-CoA carboxylase from ornamental grasses , 1993 .

[88]  R. Aebersold,et al.  Unique structural features and differential phosphorylation of the 280-kDa component (isozyme) of rat liver acetyl-CoA carboxylase. , 1994, The Journal of biological chemistry.

[89]  W. Cleland,et al.  Derivation of rate equations for multisite ping-pong mechanisms with ping-pong reactions at one or more sites. , 1973, The Journal of biological chemistry.

[90]  B. Nikolau,et al.  Purification and characterization of maize leaf acetyl-coenzyme A carboxylase. , 1984, Archives of biochemistry and biophysics.

[91]  N. Balke,et al.  Herbicidal disruption of proton gradient development and maintenance by plasmalemma and tonoplast vesicles from oat root , 1988 .

[92]  Fatty Acid Metabolism , 1988 .

[93]  J. M. Ditomaso Membrane Response to Diclofop Acid Is pH Dependent and Is Regulated by the Protonated Form of the Herbicide in Roots of Pea and Resistant and Susceptible Rigid Ryegrass , 1993, Plant physiology.

[94]  E. Wurtele,et al.  Differential Accumulation of Biotin Enzymes during Carrot Somatic Embryogenesis. , 1992, Plant physiology.

[95]  W. Brattin,et al.  Isolation of the Subunits of Transcarboxylase and Reconstitution of the Active Enzyme from the Subunits , 1975 .

[96]  H. Wood,et al.  Transcarboxylase. IX. Parameters effecting dissociation and reassociation of the enzyme. , 1970, The Journal of biological chemistry.

[97]  C. Preston,et al.  Resistance to Acetyl-Coenzyme a Carboxylase-Inhibiting Herbicides Endowed by a Single Major Gene Encoding a Resistant Target Site in a Biotype of Lolium rigidum , 1996 .

[98]  D. L. Wyse,et al.  Characterization of Maize Acetyl-Coenzyme A Carboxylase , 1993, Plant physiology.

[99]  K. Kim,et al.  Structural features of the acetyl-CoA carboxylase gene: mechanisms for the generation of mRNAs with 5' end heterogeneity. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[100]  H. Hoppe Differential effect of diclofop-methyl on fatty acid biosynthesis in leaves of sensitive and tolerant plant species , 1985 .