Metabolism of aryloxyphenoxypropionate herbicides in weed species
Abstract
The metabolic detoxication/bioactivation pathways, the levels and activity of enzymes, and endogenous cofactors mediating these reactions in crops have been well documented; however, much less evidence has been accumulated in weed species. The herbicide metabolism as a selectivity factor is summarized with special attention to acetyl-CoA carboxylases (ACCase)-inhibiting aryloxyphenoxypropionate, protoporphyrinogen IX oxidase (PPO) inhibitor, carotenoid biosynthesis inhibitor clomazone, and acetolactate synthase (ALS) inhibitor imidazolinone and sulfonylurea herbicides in various weed species. The metabolism-based herbicide resistance related to these herbicide classes is also discussed along with the role and level of metabolizing enzymes and cofactors in weed species.
Keywords
- Herbicide
- metabolism
- selectivity
- resistance
- weed species
1. Introduction
Metabolism, or biotransformation of herbicides, resulting in detoxication or bioactivation of the parent molecules, is a major factor in herbicide resistance and selectivity in plants. Selectivity, the principal basis of herbicide usage, is influenced by many factors such as application methods, differential absorption, translocation, sequestration in plants, and, at subcellular levels, differences in active site sensitivity, as well as rate of metabolism. Among the factors affecting the active internal concentration of the herbicide, the rate of metabolism seems to be of major importance in the selective action, which, in turn, depends on the activity of detoxifying enzymes and concentration of endogenous substrates. Plants metabolize herbicides through various intermediates, mostly to more polar products and insoluble bound residues. The metabolism of herbicides may occur as a three-phase process in plants. Phase I is primary metabolism to convert biologically active molecules into less active compounds (detoxication) but occasionally into more phytotoxic metabolites (bioactivation). Phase I reactions include oxidation, reduction, and hydrolysis and yield phenolic,
Much is known about herbicide metabolism in crop plants and the effect of biotransformation products on the biological activity. Metabolism that confers herbicide tolerance in crops also occurs in weeds. Metabolic pathways and rates in both crops and weeds must often be considered together to understand the metabolic basis for crop selectivity. The metabolic detoxication/bioactivation pathways, the levels and activity of enzymes, and the endogenous cofactors mediating these reactions in crops have been well documented [1–3]; however, much less evidence has been accumulated in weed species. On the other hand, repeated use of herbicides with similar chemistry may lead to the selection of herbicide-resistant biotypes with an enhanced capacity to degrade herbicides. Weed species that have evolved resistance to herbicides due to enhanced metabolic capacity have been a major issue [4]. Target-site resistance develops by mutation within a gene coding for an herbicide target-site enzyme or by overproduction of the target enzyme. Non-target-site resistance involves mechanisms that minimize the amount of herbicidally active molecule reaching the target site by reduced uptake and translocation, increased sequestration, and enhanced metabolism.
This chapter provides an overview of herbicide metabolism in weeds as a selectivity factor with special attention to ACCase-inhibiting aryloxyphenoxypropionate, protoporphyrinogen IX oxidase (PPO or protox) inhibitor, carotenoid biosynthesis inhibitory clomazone, and acetolactate synthase (ALS) inhibitor imidazolinone and sulfonylurea herbicides. Moreover, the metabolism-based herbicide resistance is also examined with the abovementioned chemistry of herbicides. Finally, the role and level of metabolizing enzymes and cofactors in weed species are discussed.
2. Metabolism and selectivity of ACCase inhibitor aryloxyphenoxypropionate herbicides in weed species
Aryloxyphenoxypropionates such as diclofop-methyl, fenoxaprop-ethyl, fluazifop-butyl, haloxyfop-methyl, and quizalofop-ethyl are highly selective postemergence herbicides for the control of graminaceous weeds. These herbicides are known inhibitors of the acetyl-CoA carboxylases (ACCase) which are crucial for the biosynthesis of fatty acids catalyzing the production of malonyl-CoA from acetyl-CoA and CO2 [5].
Diclofop-methyl selectivity between tolerant wheat and susceptible wild oat (
Following widespread applications of ACCase-inhibiting herbicides, resistance to these graminicides developed [4]. In cereal and leguminous grain crop areas of South Australia, a large number of populations of annual ryegrass (
Basis for sensitivity differences among small crabgrass (
The possible mechanism(s) of resistance to fenoxaprop-P-ethyl in late watergrass (
Only few details are available on metabolic fate of fluazifop-butyl in weed species. Fluazifop acid was the major metabolite in quackgrass
A population of crabgrass (
Metabolism of haloxyfop-methyl in intact plants of shattercane (
Selective action of quizalofop-ethyl in a sensitive (Biotype 10) and a less sensitive (Biotype 2) quackgrass (
3. Metabolism and selectivity of protoporphyrinogen IX oxidase inhibitory herbicides in weed species
Protoporphyrinogen oxidase (PPO), the last common enzyme in heme and chlorophyll biosynthesis, is the target of several classes of herbicides acting as inhibitors in both plants and mammals [22]. PPO inhibitor herbicides inhibit the enzyme, protoporphyrinogen oxidase (called also as protox), which is essential for the synthesis of chlorophyll. Susceptible plants accumulate toxic levels of protoporphyrinogen IX (proto IX) which reacts with oxygen and light to form singlet oxygen. Singlet oxygen causes rapid lipid peroxidation, membrane destruction, desiccation, and death. PPO inhibitors belonging to different chemical families have been developed as wide-spectrum agricultural herbicides. PPO inhibitory diphenyl ethers,
Diphenyl ether herbicide types, acifluorfen and lactofen, are used postemergence in soybean for selective control of annual morning glory and other broadleaf weed species. The rate of metabolism of acifluorfen was inversely related to susceptibility of plants such as common ragweed (
The phenyl-triazolinone, carfentrazone-ethyl, is a selective postemergence herbicide against troublesome weeds such as morning glories (
Sulfentrazone, also a phenyl-triazolinone herbicide, exhibits activity toward weeds commonly associated with soybeans. Consistent with field observation, sicklepod (
The
4. Metabolism of carotenoid biosynthesis inhibitor clomazone in weeds
Clomazone belongs to the group of isoxazolidinones, and acts by inhibiting the biosynthesis of photosynthetic pigments of both chlorophyll and carotenoids. Clomazone is not a protox inhibitor herbicide. Clomazone inhibits the 1-deoxy-D-xylulose 5-phosphate (DXP) synthase, the first enzyme of the non-mevalonate isoprenoid pathway in plastids which generates isopentenyl pyrophosphate for the biosynthesis of terpenes and terpenoids [34]. As a consequence of clomazone action impaired chloroplast development and pigment loss occur in susceptible plants. At higher light intensities, reactive singlet oxygen initiates membrane lipid peroxidation in the absence of carotenoids or at extremely reduced carotenoid levels.
Differential metabolism or differential rate of metabolism of clomazone did not appear to explain the tolerance of soybean (48% clomazone metabolized in 4 days) and smooth pigweed (
Rice, a relatively tolerant species, and early watergrass (
5. Metabolism and selectivity of acetolactate synthase (ALS) inhibitor herbicides in weed species
The endogenous ALS (also known as acetohydroxy acid synthase, AHAS) gene is involved in the biosynthesis of branched-chain amino acids (valine, leucine, and isoleucine), catalyzing the formation of 2-acetolactate or 2-aceto-2-hydroxybutyrate [39]. ALS is the site of action of several structurally diverse classes of herbicides such as sulfonylureas, imidazolinones, and triazolopyrimidine sulfonamides [40]. ALS inhibitors are quite unique inhibitors since they do not show structural similarity to the natural substrates, such as pyruvate and α-ketobutyrate, cofactors, such as thiamine diphosphate and flavin adenine dinucleotide, and allosteric effectors, such as valine, leucine, and isoleucine, of the enzyme. Inhibition of ALS results in deficiency of the amino acid pool and triggers a decrease in protein biosynthesis, which eventually leads to reduced rate of cell division. This process eventually kills the plants after showing symptoms in meristematic tissues where biosynthesis of amino acids primarily takes place [41].
5.1. Metabolism of imidazolinone herbicides in weeds
The imidazolinones are important ALS-inhibiting herbicides. The most significant members of this chemistry are imazamethabenz-methyl, imazaquin, imazethapyr, imazapyr, and imazamox. The basic structural requirements for this class include an aromatic/pyridine ring with 5’-carboxylic acid or carboxylic ester function as well as an adjacent
Imazamethabenz-methyl, actually a racemic mixture of
Imazaquin is a broad-spectrum herbicide developed for the use in soybean. Imazaquin can be used both preemergence and postemergence on both broadleaf and grass weeds. In order to understand the selectivity between crop plant and weed absorption, translocation and metabolism of imazaquin in soybean (
Sicklepod (
Jointed goatgrass (
5.2. Metabolism of sulfonylurea herbicides in weeds
Sulfonylureas represent a great advance in crop protection and have revolutionized herbicide research and weed control in the 1980s by introducing an unprecedented mode of herbicide action. The high potency of sulfonylureas decreased the previously applied high herbicide rates from kg/ha to as low as 1 g/ha. These molecules possess remarkably low mammalian toxicity, and advantageous environmental properties. The target site for sulfonylurea herbicides is also the ALS, the first common enzyme responsible for the biosynthesis of the branched-chain amino acids. Sulfonylureas are generally extremely potent inhibitors of ALS, regardless of plant species, and differential sensitivities at the target site play little, if any, role in their selective action [2]. Rather, differential metabolism has been implicated in their crop selectivity.
A major factor responsible for the selectivity of chlorsulfuron as a postemergence herbicide for small grains is the ability of the monocot plants to metabolize the herbicide [51]. Tolerant monocotyledonous plants such as wheat, oats, barley, wild oats (
Resistance to ALS inhibitor herbicides in weeds was first discovered in 1987 [55, 56]. Since then numerous weed species have become resistant to sulfonylureas and imidazolidines. Several mutations in the ALS gene are capable of conferring resistance to ALS inhibitor herbicides [57]. Metabolism studies with cross-resistant (SLR31) and two susceptible (VLR1 and VLR6) biotypes of rigid ryegrass (
A biotype VLR69 of rigid ryegrass (
Chlorimuron-ethyl is a highly active sulfonylurea herbicide for preemergence and postemergence use in soybeans. Studies on soybean selectivity to chlorimuron-ethyl showed that the selectivity was not based on differential active site sensitivity [62]. ALS from tolerant soybeans is just as sensitive to chlorimuron-ethyl as ALS preparations from diverse sensitive weeds. While the metabolic half-life of chlorimuron ethyl in soybean was 1–3 h following foliar application, in redroot pigweed (
Thifensulfuron-methyl differs from most other sulfonylurea herbicides in several respects. It is a short-residual herbicide, by virtue of its high susceptibility to microbial degradation in the soil. Soybeans metabolize thifensulfuron-methyl relatively rapidly, with half-life of 4–6 h (Table 4) [64]. The very sensitive species, including velvetleaf (
Johnsongrass (
Broadleaf signalgrass (
The physiological basis for nicosulfuron and primisulfuron selectivity in corn, johnsongrass (
Metsulfuron-methyl is an effective herbicide for use against broadleaf weeds and some grasses but is safe for use on wheat. Metabolism of metsulfuron-methyl in wheat and barley yielded a phenolic derivative formed after phenyl ring hydroxylation, a glucosyl conjugate of the phenolic metabolite as well as a hydroxymethyl derivative from hydroxylation of the methyl substituent of the triazine ring [72]. Hydrolysis of the sulfonylurea bridge resulted in several other unconjugated metabolites. Nevertheless, no de-esterified metabolites were detected. On the other hand, soybean seedlings do not metabolize metsulfuron-methyl and are correspondingly quite intolerant of this herbicide (GR50 < 0.5 g/ha). Soybeans exhibit an interesting specificity for de-esterification. The ethyl ester of chlorimuronethyl is de-esterified, while the methyl ester of metsulfuron-methyl is not, even though both compounds possess a phenyl ring. It was speculated that soybeans are incompetent to de-esterify ortho phenyl methyl ester sulfonylureas but are capable of this reaction with certain higher phenyl esters and even the methyl ester of thiophene sulfonylureas [73]. The locoweeds, woolly loco (
Triflusulfuron-methyl is a postemergence sulfonylurea herbicide for the control of annual and perennial broadleaf weeds and grasses in sugar beets. The mechanism of selectivity was studied by comparing the response of sugar beets with that of sensitive weeds such as rapeseed (
6. Metabolizing enzymes in weed species
Metabolism of herbicides in weed species generally produces identical metabolites that were formed in crop plants. Metabolizing enzymes such as glutathione-
Both monocot and dicot weeds contain the level of non-protein thiols (mostly GSH) comparable to that of maize (Table 5) [80]. Since the activity of GST enzymes toward herbicidal substrates in weed species is inferior to that of maize, we can conclude that the contribution of nonenzymatic GSH conjugation can be substantial in the metabolism of herbicide in weed species.
|
|
|
|
|
|
267 ± 17 | 2869 ± 160 | 922 ± 85 | 41 ± 11 |
|
492 ± 28 | 676 ± 43 | 684 ± 79 | N/A |
|
N/A | N/A | N/A | NDb |
|
391 ± 24 | 170 ± 23 | 517 ± 49 | 17 ± 8 |
|
140 ± 11 | 56 ± 8 | 356 ± 39 | 10 ± 4 |
|
309 ± 27 | 59 ± 7 | ND | 51 ± 24 |
|
273 ± 12 | 70 ± 9 | 874 ± 76 | ND |
Maizec | 488 ± 16 | 986 ± 92 | 4567 ± 347 | 67 ± 14 |
The involvement of cytochrome P450 monooxygenases in herbicide detoxication and selectivity has been well demonstrated in plants [84]. However, only few cytochrome P450-mediated herbicide metabolisms were carried out with microsomes from weed species. Microsomes from naphthalic anhydride-treated and untreated shattercane and johnsongrass catalyzed the hydroxylation of bentazon [85]. The results indicated that bentazon hydroxylation in shattercane and johnsongrass is mediated by a constitutive and an inducible cytochrome P450 monooxygenase enzyme. Primisulfuron, but not nicosulfuron, was hydroxylated in woolly cupgrass (
The role of cytochrome P450 monooxygenases in enhanced metabolism of resistant weed species has also been documented [87, 88]. Cytochrome P450 levels in
Since the primisulfuron metabolism in barnyardgrass proceeds through hydroxylation of the pyrimidine moiety followed by formation of glycosyl conjugate we can assume that glycosyl transferases are also present in weed species [71].
References
- 1.
Katagi T, Mikami N. Primary metabolism of agrochemicals in plants. In: Roberts T, editor. Metabolism of agrochemicals in plants.Chichester: Wiley; 2000. pp. 43-106. - 2.
Owen WJ. Herbicide metabolism as basis for selectivity. In: Roberts T, editor. Metabolism of agrochemicals in plants.Chichester: Wiley; 2000. pp. 211-258. - 3.
Rao VS. Principles of weed science. 2nd ed. Enfield: Science Publishers; 2000. 555p. - 4.
Yu Q, Powles S. Metabolism-based resistance and cross resistance in crop weeds: A threat to herbicide sustainability and global crop production. Plant Physiology.2014, 166:1106-1118. - 5.
Shaner DL. Herbicide safety relative to common targets in plants and mammals.Pesticide Management Science.2003, 60:17-24. - 6.
Shimabukuro RH, Walsh WC, Hoerauf RA. Metabolism and selectivity of diclofop-methyl in wild oat and wheat.Journal of Agricultural and Food Chemistry.1979, 27:615-623. - 7.
McFadden JJ, Frear DS, Mansager ER. Aryl hydroxylation of diclofop by a cytochrome P450-dependent monooxygenase from wheat, Pesticide Biochemistry and Physiology.1989, 34:92-100. - 8.
Boldt PF, Putnam AR. Selectivity mechanisms for foliar applications of diclofop-methyl. II. Metabolism. Weed Science. 1981, 29:237-241. - 9.
Holtum JAM, Matthews JM, Hausler RE, Liljegren DR, Powles SB. Cross-resistance to herbicides in annual ryegrass ( Loliumrigidum ). III. On the mechanism of resistance to diclofop-methyl. Plant Physiology.1991, 97:1026-1034. - 10.
Preston C, Tardif FJ, Christopher JT, Powles SB. Multiple resistance to dissimilar herbicide chemistries in a biotype of Loliumrigidum due to enhanced activity of several herbicide degrading enzymes. Pesticide Biochemistry and Physiology.1996, 54:123–134. - 11.
Lefsrud C, Hall JC. Basis for sensitivity differences among crabgrass, oat, and wheat to fenoxaprop-ethyl. Pesticide Biochemistry and Physiology. 1989, 34:218–227. - 12.
Tal JA, Romano ML, Stephenson GR, Schwan AL, Hall JC. Glutathione conjugation: A detoxification pathway for fenoxaprop-ethyl in barley, crabgrass, oat, and wheat. Pesticide Biochemistry and Physiology. 1993, 46:190-199. - 13.
Tal JA, Hall JC, Stephenson GR. Non-enzymatic conjugation of fenoxaprop-ethyl with glutathione and cysteine in several grass species.Weed Research. 1995, 35:133–139. - 14.
Bakkali Y, Ruiz-Santaella JP, Osuna MD, Wagner J, Fischer AJ, De Prado R. Late watergrass ( Echinochloaphyllopogon ): Mechanisms involved in the resistance to fenoxaprop-p-ethyl. Journal of Agricultural and Food Chemistry.2007, 55:4052-8. - 15.
Bakkali Y, Ruiz-Santaella JP, De Prado R, Rodriguez JM, Fischer AJ. Resistance mechanisms to fenoxaprop-p-ethyl in a late watergrass ( Echinochloaphyllopogon ) biotype from California. In: Proceedings of the BCPC International Congress; 31 Oct–2 Nov 2005. Glasgow,Alton: The British Crop Protection Council; 2005. Vol. 1, pp. 181-186. - 16.
Hendley P, Dicks JW, Monaco TJ, Slyfield SM, Tummon OJ, Barrett JC. Translocation andmetabolism of pyridinyloxy-phenoxypropionate herbicides in rhizomatous quackgrass ( Agropyronrepens ). Weed Science. 1985, 33:11-24. - 17.
Coupland D. Pre-treatment environmental effects on the uptake, translocation, metabolism, and performance of fluazifop-butyl in Elymusrepens . Weed Research. 1989, 29:289-297. - 18.
Hidayat I, Preston C. Enhanced metabolism of fluazifop acid in a biotype of DigitariaSanguinalis resistant to the herbicide fluazifop-p-butyl. Pesticide Biochemistry and Physiology.1997, 57:137–146. - 19.
Buhler DD, Swisher BA, Burnside OC. Behavior of ¹⁴C-haloxyfop-methyl in intact plants and cell cultures. Weed Science. 1985, 33:291-299. - 20.
Tardif FJ, Leroux GD, Translocation of glyphosate and quizalofop and metabolism of quizalofop in quackgrass biotypes ( Elytrigiarepens ). Weed Technology. 1991, 5:525-531. - 21.
Culpepper S, York AC, Jordan DL, Corbin FT, Sheldon YS. Basis for antagonism in mixtures of bromoxynil plus quizalofop-p applied to yellow foxtail ( Setariaglauca ). Weed Technology. 1999, 13:515-519. - 22.
Yu H-B, Cheng X-M, Li B. 1(Heterocyclyl),2,4,5-tetrasubstituted benzenes as protoporphyrinogen-IX oxidase inhibiting herbicides. In: Hasaneen MN, editor. Herbicides – Properties, synthesis and control of weeds. InTech: Rijeka; 2012. pp. 103-118. - 23.
Theodoridis G, Liebl R, Zagar C. Protoporphyrinogen IX oxidase inhibitors. In: Krämer W, Schirmer U, Jeschke P, Witschel M, editors. Modern crop protection compounds, Vol. 1-3, 2nd ed. Weinheim: Wiley; 2012. pp. 165-195. DOI: 10.1002/9783527644179. - 24.
Ritter RL, Coble HD. Penetration, translocation, and metabolism of acifluorfen in soybean ( Glycine max ), common ragweed (Ambrosia artemisiifolia ), and common cocklebur (Xanthium pensylvanicum ). Weed Science. 1981, 29:474-480. - 25.
Frear DS, Swanson HR, Mansager ER. Acifluorfen metabolism in soybean: Diphenylether bond cleavage and the formation of homoglutathione, cysteine, and glucose conjugates. Pesticide Biochemistry and Physiology.1983, 20:299-310. - 26.
Higgins JM, Whitwell T, Corbin FT, Carter GE Jr, Hill HS Jr. Absorption, translocation, and metabolism of acifluorfen and lactofen in pitted morningglory ( Ipomoea lacunosa) and ivyleafmorningglory (Ipomoea hederacea ). Weed Science. 1988, 36:141-145. - 27.
Dayan FE, Duke SO, Weete JD, Hancock HG. Selectivity and mode of action of carfentrazone-ethyl, a novel phenyl triazolinone herbicide.Pesticide Science.1997, 51:65-73. - 28.
Dayan, FE, Weete JD, Hancock HG. Physiological basis for differential sensitivity to sulfentrazone by sicklepod ( Sennaobtusifolia ) and coffee senna (Cassia occidentalis ). Weed Science. 1996, 44:12–17. - 29.
Thomas WE, Troxler SC, Smith WD, Fisher LR, Wilcut JW. Uptake, translocation, and metabolism of sulfentrazone in peanut, prickly sida ( Sidaspinosa ), and pitted morningglory (Ipomoea lacunosa ). Weed Science. 2005, 53:446-450. - 30.
Price AJ, Wilcut JW, Cranmer JR.Physiological behavior of root-absorbed flumioxazin in peanut, ivyleafmorningglory ( Ipomoea hederacea ), and sicklepod (Sennaobtusifolia ). Weed Science. 2004, 52:718-724. - 31.
Flumioxazin. 2013. Available from: http://www.mass.gov/eea/docs/agr/pesticides/aquatic/flumioxazin.pdf [Accessed: 2015-01-14]. - 32.
Tomigahara Y, Matsui M, Matsunaga H, Isobe N, Kaneko H, Nakatsuka I, Yoshitake A, Yamane S. Metabolism of 7-fluoro-6-(3,4,5,6-tetrahydrophthalimido)-4-(2-propynyl)-2H-1,4-benzoxazin-3(4H)-one (S-53482) in rat. 1. Identification of a sulfonic acid type conjugate. Journal of Agricultural and Food Chemistry.1999, 47:305–312. - 33.
Tomigahara Y, Onogi M, Kaneko H, Nakatsuka I, Yamane S. Metabolism of 7-fluoro-6-(3,4,5,6-tetrahydrophthalimido)-4-(2-propynyl)-2H-1,4-benzoxazin-3(4H)-one (S-53482, flumioxazin) in the rat: II. Identification of reduced metabolites.Journal of Agricultural and Food Chemistry.1999, 47:2429–2438. - 34.
Ferhatoglu Y, Barrett M. Studies of clomazone mode of action. Pesticide Biochemistry and Physiology.2006, 85:7–14. - 35.
Vencill WK, Hatzios KK, Wilson HP. Absorption, translocation, and metabolism of 14C-clomazone in soybean ( Glycine max ) and threeAmaranthus weed species. Journal of Plant Growth Regulation.1990, 9:127-132. - 36.
Liebl RA, Norman MA. Mechanism of clomazone selectivity in corn ( Zea mays ), soybean (Glycine max ), smooth pigweed (Amaranthushybridus ), and velvetleaf (Abutilon theophrasti ). Weed Science. 1991, 39:329-332. - 37.
TenBrook PL, Tjeerdema RS.Biotransformation of clomazone in rice ( Oryza sativa ) and early watergrass (Echinochloaoryzoides ).Pesticide Biochemistry and Physiology.2006, 85:38–45. - 38.
Yasuor H, Zou W, TolstikovVV, Tjeerdema RS, Fischer AJ. Differential oxidative metabolism and 5-ketoclomazone accumulation are involved in Echinochloaphyllopogon resistance to clomazone. Plant Physiology.2010, 153:319–326. - 39.
Duggleby RG, Pang SS. Acetohydroxyacid synthase. Journal of Biochemistry and Molecular Biology. 2000, 33:1–36. - 40.
Krämer W, Schirmer U, Jeschke P, Witschel M, editors. Modern crop protection compounds, volume 1-3. 2nd ed. Weinheim: Wiley; 2012. 1608 p. DOI: 10.1002/9783527644179. - 41.
Zhou Q, Liu W, Zhang Y, Liu KK. Action mechanisms of acetolactate synthase-inhibiting herbicides. Pesticide Biochemistry and Physiology. 2007, 89:89–96. - 42.
Brown MA, Chiu TY, Miller P. Hydrolytic activation versus oxidative degradation of Assert herbicide, an imidazolinone aryl-carboxylate, in susceptible wild oat versus tolerant corn and wheat.Pesticide Biochemistry and Physiology.1987, 27:24–29. - 43.
Nandula VK, Messersmith CG. Imazamethabenz-resistant wild oat ( Avenafatua L. ) is resistant to diclofop-methyl. Pesticide Biochemistry and Physiology.2002, 74:53–61. - 44.
Shaner DL, Robson PA. Absorption, translocation, and metabolism of AC 252 214 in soybean ( Glycine max ), common cocklebur (Xanthium strumarium ), and velvetleaf (Abutilon tbeophrasti ). Weed Science. 1985, 33:469–471. - 45.
Risley MA, Oliver LR. Absorption, translocation, and metabolism of imazaquin in pitted ( Ipomoea lacunosa ) and entireleaf (Ipomoea hederacea var. integriuscula ) morningglory. Weed Science. 1992, 40:503–506. - 46.
Cole TA, Wehtje GR. Wilcut JW, Hicks TV. Behavior of imazethapyr in soybeans ( Glycine max) , peanuts (Arachishypogaea ), and selected weeds. Weed Science. 1989, 37:639–644. - 47.
Nissen SJ, Masters RA, Stougaard RN. Imazethapyr absorption and fate in leafy spurge ( Euphorbia esula ). Weed Science. 1994, 42:158–162. - 48.
Ballard TO, Foley ME, Bauman TT. Absorption, translocation, and metabolism of imazethapyr in common ragweed ( Ambrosia artemisiifolia ) and giant ragweed (Ambrosia trifida ). Weed Science. 1995, 43:572–577. - 49.
Pester TA, Nissen SJ, Westra P. Absorption, translocation, and metabolism of imazamox in jointed goatgrass and feral rye. Weed Science. 2001, 49:607–612. - 50.
Vassios JD, Nissen SJ, Brunk GR. Imazamox absorption, desorption, and metabolism by Eurasian watermilfoil. Journal of Aquatic Plant Management.2011, 49:44–49. - 51.
Sweetser PB, Schow GS, Hutchison JM. Metabolism of chlorsulfuron by plants: Biological basis for selectivity of a new herbicide for cereals. Pesticide Biochemistry and Physiology.1982, 17:18–23. - 52.
Müller F, Kang BH, Maruska FT. Fate of chlorsulfuron in cultivated plants and weeds and reasons for selectivity. Mededelingen Faculteit Landbouwwetenschappen Rijksuniversiteit Gent. 1984, 49/3b:1091–1108. - 53.
Hageman LH, Behrens R. Basis for response differences of two broadleaf weeds to chlorsulfuron. Weed Science. 1984, 32:162–167. - 54.
Hutchison JM, Shapiro R, Sweetser PB. Metabolism of chlorsulfuron by tolerant broadleaves. Pesticide Biochemistry and Physiology. 1984, 22:243–247. - 55.
Mallory-Smith CA, Thill DC, Dial MJ. Identification of sulfonylurea herbicide-resistant prickly lettuce ( Lactuca serriola ). Weed Technology. 1990, 4:163–168. - 56.
Primiani MM, Conerman JC, Saari LL. Resistance of kochia ( Kochia scoparia ) to sulfonylurea and imidazolinone herbicides. Weed Technology. 1990, 4:169–172. - 57.
Saari LL, Maxwell CA. Target-site resistance for acetolactate sythase inhibitor herbicides. In: De Prado R, Jorrin J, Garcia-Torres L, editors. Weed and crop resistance to herbicides. Dordrecht: Kluwer; 1997. pp. 81–88. - 58.
Christopher JT, Powles SB, Holtum JAM, Liljegren DR. Cross-resistance to herbicides in annual ryegrass ( Loliumrigidum ). II. Chlorsulfuron resistance involves a wheat-like detoxification system. Plant Physiology.1991, 95:1036–1043. - 59.
Cotterman JC, Saari LL. Rapid metabolic inactivation is the basis for cross-resistance to chlorsulfuron in diclofop-methyl-resistant rigid ryegrass ( Lolium rigidurn ) biotype SR4/84. Pesticide Biochemistry and Physiology. 1992, 43:182–192. - 60.
Burnet MWM, Christopher JT, Holtum JAM, Powles SB. Identification of two mechanisms of sulfonylurea resistance within one population of rigid ryegrass ( Lolium rigidum ) using a selective germination medium. Weed Science. 1994, 42:468–473. - 61.
Preston C, Tardif FJ, Christopher JT, Powles SB. Multiple resistance to dissimilar herbicide chemistries in a biotype of Loliumrigidum due to enhanced activity of several herbicide degrading enzymes. Pesticide Biochemistry and Physiology.1996, 54:123–134. - 62.
Brown HM, Neighbors SM. Soybean metabolism of chlorimuron ethyl: Physiological basis for soybean selectivity. Pesticide Biochemistry and Physiology.1987, 29:112–120. - 63.
Brown HM, Fuesler TP, Ray TB, Strachan SD. Role of plant metabolism in crop selectivity of herbicides. In: Frehse H, editor. Pesticide chemistry: Advances in international research, development and legislation. Weinheim: VCH; 1991. pp. 257–266. - 64.
Brown HM, Wittenbach EA, Forney DR, Strachan SD. Basis for soybean tolerance to thifensulfuron methyl. Pesticide Biochemistry and Physiology. 1990, 37:303–313. - 65.
Walker LM, Hatzios KK, Wilson HP. Absorption, translocation, and metabolism of 14C-thifensulfuron in soybean ( Glycine max ), spurred anoda (Anoda cristata ), and velvetleaf (Abutilon theophrasti ). Journal of Plant Growth Regulation. 1994, 13:27–32. - 66.
Obrigawitch TT, Kenyon WH, Kuratle H. Effect of application timing on rhizome johnsongrass ( Sorghum halepense ) control with DPX-V9360. Weed Science. 1990, 38:45–49. - 67.
Hinz JRR, Owen MDK. Nicosulfuron and primisulfuron selectivity in corn ( Zea mays ) and two annual grass weeds. Weed Science. 1996, 44:219–223. - 68.
Gallaher K, Mueller TC, Hayes RM, Schwartz O, Barrett M. Absorption, translocation, and metabolism of primisulfuron and nicosulfuron in broadleaf signalgrass ( Brachiariaplatyphylla ) and corn. Weed Science. 1999, 47:8–12. - 69.
Sidhu SS, Yu J, McCullough P. Nicosulfuron absorption, translocation, and metabolism in annual bluegrass and four turfgrass species. Weed Science. 2014, 62:433–440. DOI: http://dx.doi.org/10.1614/WS-D-13-00182.1. - 70.
Carey JB, Penner D, Kells JJ. Physiological basis for nicosulfuron and primisulfuron selectivity in five plant species. Weed Science. 1997, 45:22–30. - 71.
Neighbors S, Privalle LS. Metabolism of primisulfuron by barnyard grass.Pesticide Biochemistry and Physiology.1990, 37:145–153. - 72.
Anderson JJ, Priester TM, Shalaby LM. Metabolism of metsulfuron methyl in wheat and barley.Journal of Agricultural and Food Chemistry.1989, 37:1429–1434. - 73.
Brown HM, Wittenbach EA, Forney DR, Strachan SD. Basis for soybean tolerance to thifensulfuron methyl. Pesticide Biochemistry and Physiology. 1990, 37:303–313. - 74.
Sterling TM, Jochem HS. Uptake, translocation, and metabolism of picloram and metsulfuron methyl by two locoweed species. Weed Science. 1995, 43:13–17. - 75.
Wittenbach VA, Koeppe MK, Lichtner FT, Zimmerman WT, Reiser RW. Basis of selectivity of triflusulfuron methyl in sugar beets ( Beta vulgaris ). Pesticide Biochemistry and Physiology, 1994, 49:72–81. - 76.
Cole DJ, Edwards R. Secondary metabolism of agrochemicals in plants. In: Roberts T, editor. Metabolism of agrochemicals in plants.Chichester: Wiley; 2000. pp. 107–154. - 77.
Anderson MP, Gronwald JW. Atrazine resistance in a velvetleaf ( Abutilon theophrasti ) biotype due to enhanced glutathione S-transferase activity.Plant Physiology. 1991. 96:104–109. - 78.
Hatton PJ, Dixon D, Cole DJ, Edwards R. Glutathione transferase activities and herbicide selectivity in maize and associated weed species. Pesticide Science.1996, 46:267–275. - 79.
Andrews CJ, Skipsey M, Townson JK, Morris C, Jepson I, Edwards R. Glutathione transferase activities toward herbicides used selectively in soybean. Pesticide Science.1997, 51:213–222. - 80.
Hatton PJ, Cummins I, Price LJ, Cole DJ, Edwards R. Glutathione transferases and herbicide detoxification in suspension-cultured cells of giant foxtail ( Setariafaberii ). Pesticide Science.1998, 53:209–216. - 81.
Cummins I, Bryant DN, Edwards R. Safener responsiveness and multiple herbicide resistance in the weed black-grass ( Alopecurusmyosuroides ). Plant Biotechnology Journal.2009, 7:807–820. - 82.
Del Buono D, Scarponi L, Espen L. Glutathione S-transferases in Festucaarundinacea : Identification, characterization and inducibility by safenerbenoxacor. Phytochemistry.2007, 68:2614–2624. - 83.
Jablonkai I, Hulesch A, Dutka F. Influence of herbicides and safeners on glutathione content and glutathione S-transferase activities of monocot and dicot weeds. In: DePrado R, Jorrin, Garcia-Torres L, Marshall G, editors. Proceedings of the International Symposium on Weed and Crop Resistance to Herbicides.Cordoba (Spain); 1995. pp. 89–91. - 84.
Siminszky B. Plant cytochrome P450-mediated herbicide metabolism. Phytochemistry Reviews. 2006, 5:445–458. - 85.
Burton JD, Maness EP. Constitutive and inducible bentazon hydroxylation in shuttercane ( Sorghum bicolor ) and Johnsongrass (Sorghum halapense ).Pesticide Biochemistry and Physiology.1992, 44:40–49. - 86.
Hinz JRR, Owen MDK, Barrett M. Nicosulfuron, primisulfuron, and bentazon hydroxylation by corn ( Zea mays ), woolly cupgrass (Eriochloavillosa ), and shattercane (Sorghum bicolor ) cytochrome P-450. Weed Science. 1997, 45:474–480.Burnett MWM, Loveys BR, Holtum JAM, Powles SB. A mechanism of chlortoluron resistance inLoliumrigidum .Planta.1993, 190:182–189. - 87.
Burnett MWM, Loveys BR, Holtum JAM, Powles SB. A mechanism of chlortoluron resistance in Loliumrigidum .Planta.1993, 190:182–189. - 88.
Burnett MWM, Loveys BR, Holtum JAM, Powles SB. Identification of two mechanisms of sulfonylurea resistance within one population of rigid ryegrass ( Loliumrigidum ) using a selective germination medium. Weed Science. 1994, 42:153–157. - 89.
Jablonkai I, Hulesch A. Cytochrome P450 levels of monocot and dicot weeds and influence of herbicides, safeners and P450 inhibitors on enzyme contents. In: Brown H, Cussans GW, Devine MD, Duke SO, Fernandez-Quintanilla, Helweg A, Labrada RE, Landes M, Kudsk P, Streibig JC, editors. Proceedings of the 2nd International Weed Control Congress.Copenhagen (Denmark); 1996. Vol. 3, p. 789–794.