Skip to main content Accessibility help
Hostname: page-component-684899dbb8-gbqfq Total loading time: 0.802 Render date: 2022-05-26T15:06:20.030Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "useRatesEcommerce": false, "useNewApi": true }

Article contents

Herbicide Metabolism: Crop Selectivity, Bioactivation, Weed Resistance, and Regulation

Published online by Cambridge University Press:  25 March 2019

Vijay K. Nandula*
Research Plant Physiologist, Crop Production Systems Research Unit, USDA-ARS, Stoneville, MS, USA
Dean E. Riechers
Professor, Department of Crop Sciences, University of Illinois, Urbana, IL, USA
Yurdagul Ferhatoglu
Former Graduate Student and Professor, Department of Plant and Soil Sciences, University of Kentucky, Lexington, KY, USA
Michael Barrett
Former Graduate Student and Professor, Department of Plant and Soil Sciences, University of Kentucky, Lexington, KY, USA
Stephen O. Duke
Research Leader, Natural Products Utilization Research Unit, USDA-ARS, University, MS, USA
Franck E. Dayan
Professor and Assistant Professor, Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins, CO, USA
Alina Goldberg-Cavalleri
Research Associate, Research Fellow, Research Associate, Senior Research Associate, and Professor, School of Natural and Environmental Sciences, Newcastle University, Newcastle upon Tyne, UK
Catherine Tétard-Jones
Research Associate, Research Fellow, Research Associate, Senior Research Associate, and Professor, School of Natural and Environmental Sciences, Newcastle University, Newcastle upon Tyne, UK
David J. Wortley
Boult Wade Tennant, London, UK
Nawaporn Onkokesung
Research Associate, Research Fellow, Research Associate, Senior Research Associate, and Professor, School of Natural and Environmental Sciences, Newcastle University, Newcastle upon Tyne, UK
Melissa Brazier-Hicks
Research Associate, Research Fellow, Research Associate, Senior Research Associate, and Professor, School of Natural and Environmental Sciences, Newcastle University, Newcastle upon Tyne, UK
Robert Edwards
Research Associate, Research Fellow, Research Associate, Senior Research Associate, and Professor, School of Natural and Environmental Sciences, Newcastle University, Newcastle upon Tyne, UK
Todd Gaines
Professor and Assistant Professor, Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins, CO, USA
Satoshi Iwakami
Assistant Professor, Kyoto University, Kyoto, Japan
Mithila Jugulam
Associate Professor, Department of Agronomy, Kansas State University, Manhattan, KS, USA
Rong Ma
Assistant Professor, Department of Plant Sciences, University of Idaho, Moscow, ID, USA
*Author for correspondence: Vijay Nandula, USDA-ARS, 141 Experiment Station Road, Stoneville, MS 38776. (Email:


Several grass and broadleaf weed species around the world have evolved multiple-herbicide resistance at alarmingly increasing rates. Research on the biochemical and molecular resistance mechanisms of multiple-resistant weed populations indicate a prevalence of herbicide metabolism catalyzed by enzyme systems such as cytochrome P450 monooxygenases and glutathione S-transferases and, to a lesser extent, by glucosyl transferases. A symposium was conducted to gain an understanding of the current state of research on metabolic resistance mechanisms in weed species that pose major management problems around the world. These topics, as well as future directions of investigations that were identified in the symposium, are summarized herein. In addition, the latest information on selected topics such as the role of safeners in inducing crop tolerance to herbicides, selectivity to clomazone, glyphosate metabolism in crops and weeds, and bioactivation of natural molecules is reviewed.

© Weed Science Society of America, 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)


Ahrens, WH (1990) Enhancement of soybean (Glycine max) injury and weed control by thifensulfuron insecticide mixtures. Weed Technol 4:524528 CrossRefGoogle Scholar
Anonymous (2018) Command 3ME herbicide label. Accessed: May 11, 2018Google Scholar
Arntz, MA, DeLucia, EH Jordan, N (2000) From fluorescence to fitness: variation in photosynthetic rate affects fecundity and survivorship. Ecology 81:25672576 CrossRefGoogle Scholar
Baerg, RJ, Barrett, M Polge, ND (1996) Insecticide and insecticide metabolite interactions with cytochrome P450 mediated activities in maize. Pestic Biochem Physiol 55:1020 CrossRefGoogle ScholarPubMed
Baerson, SR, Sanchez-Moreiras, A, Pedrol-Bonjoch, N, Schulz, M, Kagan, IA, Agarwal, AK, Reigosa, MJ Duke, SO (2005) Detoxification and transcriptome response in Arabidopsis seedlings exposed to the allelochemical benzoxazolin-2(3H)-one. J Biol Chem 280:2186721881 CrossRefGoogle ScholarPubMed
Bakkali, Y, Ruiz-Santaella, JP, Osuna, MD, Wagner, H, Fischer, AJ DePrado, R (2007) Late watergrass (Echinochloa phyllopogon): mechanisms involved in the resistance to fenoxaprop-p-ethyl. J Agric Food Chem 55:40524058 CrossRefGoogle ScholarPubMed
Barroso, AAM, de S Costa, MG, Neto, NJ, dos Santos, JI, Balbuena, TS, Carbonari, CA Alves PLCA, (2018) Protein identification before and after glyphosate exposure in Lolium multiflorum genotypes. Pest Manag Sci 74:11251133 CrossRefGoogle ScholarPubMed
Beaudegnies, R, Edmunds, AJF, Fraser, TEM, Hall, RG, Hawkes, TR, Mitchell, G, Schaetzer, J, Wendeborn, S Wibley, J (2009) Herbicidal 4-hydroxyphenylpyruvate dioxygenase inhibitors—a review of the triketone chemistry story from a Syngenta perspective. Bioorg Med Chem 17:41344152 CrossRefGoogle Scholar
Behringer, C, Bartsch, K Schaller, A (2011) Safeners recruit multiple signalling pathways for the orchestrated induction of the cellular xenobiotic detoxification machinery in Arabidopsis . Plant Cell Environ 34:19701985 CrossRefGoogle ScholarPubMed
Bernal, J, Martin, MT, Soto, ME, Nozal, MJ, Marotti, I, Dinelli, G Bernal, JL (2012) Development and application of a liquid chromatography-mass spectrometry method to evaluate the glyphosate and aminomethylphosphonic acid dissipation in maize plants after foliar treatment. J Agric Food Chem 60:40174025 CrossRefGoogle ScholarPubMed
Bjarnholt, N, Neilson, EHJ, Crocoll, C, Jørgensen, K, Motawia, MS, Olsen, CE, Dixon, DP, Edwards, R Møller, BL (2018) Glutathione transferases catalyze recycling of auto-toxic cyanogenic glucosides in sorghum. Plant J 94:11091125 CrossRefGoogle ScholarPubMed
Bohm, GMB, Rombaldi, CV, Genovese, MI, Castilhos, D, Alves, BJR Rumjanek, NG (2014) Glyphosate effects on yield, nitrogen fixation, and seed quality in glyphosate-resistant soybean. Crop Sci 54:17371743 CrossRefGoogle Scholar
Bøhn, T, Cuhra, M, Traavik, T, Sanden, M, Fagan, J Primicerio, R (2014) Compositional differences in soybeans on the market: glyphosate accumulates in Roundup Ready GM soybeans. Food Chem 153: 207215 CrossRefGoogle ScholarPubMed
Boutsalis, P, Gill, GS Preston, C (2012) Incidence of herbicide resistance in rigid ryegrass (Lolium rigidum) across southeastern Australia. Weed Technol 26:391398 CrossRefGoogle Scholar
Brazier-Hicks, M, Knight, KM, Sellars, JD, Steel, PG Edwards, R (2018) Testing a chemical series inspired by plant stress oxylipin signaling agents for herbicide safening activity. Pest Manag Sci 74:828836 CrossRefGoogle Scholar
Broster, JC Pratley, JE (2006) A decade of monitoring herbicide resistance in Lolium rigidum in Australia. Aust J Exp Agric 46:11511160 CrossRefGoogle Scholar
Brown, HM (1990) Mode of action, crop selectivity, and soil relations of the sulfonylurea herbicides. Pest Manag Sci 29:263281 CrossRefGoogle Scholar
Burnet, MW, Loveys, BR, Holtum, JA Powles, S (1993) Increased detoxification is a mechanism of simazine resistance in Lolium rigidum . Pestic Biochem Physiol 46:207218 CrossRefGoogle Scholar
Burns, EE, Keith, BK, Rafai, MY, Bothner, B Dyer, WE (2017) Proteomic and biochemical assays of glutathione-related proteins in susceptible and multiple herbicide resistant Avena fatua L. Pestic Biochem Physiol 140:6978 CrossRefGoogle ScholarPubMed
Busi, R, Gaines, TA Powles, S (2017) Phorate can reverse P450 metabolism-based herbicide resistance in Lolium rigidum . Pest Manag Sci 73:410417 CrossRefGoogle ScholarPubMed
Busi, R, Gaines, TA, Vila-Aiub, MM Powles, SB (2014) Inheritance of evolved resistance to a novel herbicide (pyroxasulfone). Plant Sci 217:127134 CrossRefGoogle Scholar
Busi, R, Gaines, TA, Walsh, MJ Powles, SB (2012) Understanding the potential for resistance evolution to the new herbicide pyroxasulfone: field selection at high doses versus recurrent selection at low doses. Weed Res 52:489499 CrossRefGoogle Scholar
Busi, R, Neve, P Powles, S (2013) Evolved polygenic herbicide resistance in Lolium rigidum by low-dose herbicide selection within standing genetic variation. Evol Appl 6:231242 CrossRefGoogle ScholarPubMed
Busi, R, Porri, A, Gaines, TA Powles, SB (2018) Pyroxasulfone resistance in Lolium rigidum is metabolism-based. Pestic Biochem Physiol 148:7480 CrossRefGoogle ScholarPubMed
Busi, R Powles, SB (2013) Cross-resistance to prosulfocarb and triallate in pyroxasulfone-resistant Lolium rigidum . Pest Manag Sci 69:13791384 CrossRefGoogle ScholarPubMed
Busi, R Powles, SB (2016) Cross-resistance to prosulfocarb + S-metolachlor and pyroxasulfone selected by either herbicide in Lolium rigidum . Pest Manag Sci 72:16641672 CrossRefGoogle ScholarPubMed
Busk, PK Möller, BL (2002). Dhurrin synthesis in sorghum is regulated at the transcriptional level and induced by nitrogen fertilization in older plants. Plant Physiol 129:12211231 CrossRefGoogle ScholarPubMed
Chample, JR Shaner, D (1982) Enhanced phytotoxicity of bentazon with organophosphate and carbamate insecticides. Weed Sci 30:324326 Google Scholar
Chang, JM, Knoz, MJ, Aly, EA, Sticker, RE, Wilson, KR, Krog, NE Dickinson, PE (1987) 3-isoxazolidinones and related compounds. A new class of herbicides. Pages 1023 in Baker DR, Fenyes JG, Moberg WK, Cross B, eds. Synthesis and Chemistry of Agrochemicals (ACS Symposium Series 355). Washington, DC: American Chemical Society CrossRefGoogle Scholar
Christeller, JT Galis, I (2014) α-Linolenic acid concentration and not wounding per se is the key regulator of octadecanoid (oxylipin) pathway activity in rice (Oryza sativa L.) leaves. Plant Physiol Biochem 83:117125 CrossRefGoogle Scholar
Christopher, JT, Powles, SB, Liljegren, DR Holtum, JA (1991) Cross-resistance to herbicides in annual ryegrass (Lolium rigidum): II. chlorsulfuron resistance involves a wheat-like detoxification system. Plant Physiol 95:10361043 CrossRefGoogle ScholarPubMed
Christopher, JT, Preston, C Powles, SB (1994) Malathion antagonizes metabolism-based chlorsulfuron resistance in Lolium rigidum . Pestic Biochem Physiol 49:172182 CrossRefGoogle Scholar
Clevenger, KD, Bok, JW, Ye, R, Miley, GP, Verdan, MH, Velk, T, Chen, C, Yang, K, Robey, MT, Gao, P, Lamprecht, M, Thomas, PM, Islam, MN, Palmer, JM, Wu, CC, Keller, NP Kelleher, NL (2017) A scalable platform to identify fungal secondary metabolites and their gene clusters. Nat Chem Biol 13:895901 CrossRefGoogle ScholarPubMed
Conard, S Radosevich, S (1979) Ecological fitness of Senecio vulgaris and Amaranthus retroflexus biotypes susceptible or resistant to atrazine. J Appl Ecol 16:171177 CrossRefGoogle Scholar
Cook, D, Rimando, AM, Clemente, TE, Schröder, J, Dayan, FE, Nanayakkara, NPD, Pan, Z, Noonan, BP, Fishbein, M, Abe, I, Duke, SO Scott, R. Baerson, SR (2010) Alkylresorcinol synthases expressed in Sorghum bicolor root hairs play an essential role in the biosynthesis of the allelopathic benzoquinone sorgoleone. Plant Cell 22:867887 CrossRefGoogle ScholarPubMed
Corrêa, EL, Dayan, FE, Owen, DL, Rimando, AM Duke, SO (2016) Glyphosate-resistant and conventional canola (Brassica napus L.) responses to glyphosate and aminomethylphosponic acid (AMPA) treatment. J Agric Food Chem 64:35083513 CrossRefGoogle Scholar
Costea, M, Weaver, SE Tardif, FJ (2005) The biology of invasive alien plants in Canada. 3. Amaranthus tuberculatus (Moq.) Sauer var. rudis (Sauer) Costea & Tardif. Can J Plant Sci 85:507522 CrossRefGoogle Scholar
Cotterman, J Saari, L (1992) Rapid metabolic inactivation is the basis for cross-resistance to chlorsulfuron in diclofop-methyl-resistant rigid ryegrass (Lolium rigidum) biotype SR484. Pestic Biochem Physiol 43:182192 CrossRefGoogle Scholar
Croteau, R (1992) Clomazone does not inhibit the conversion of isopentyl pyrophosphate to geranyl, farnesyl, or geranyl geranyl pyrophosphate in vitro . Plant Physiol 98:15151517 CrossRefGoogle ScholarPubMed
Culpepper, AS, York, AC, Marth, JL Corbin, FT (2001) Effect of insecticides on clomazone absorption, translocation, and metabolism in cotton. Weed Sci 49:613616 CrossRefGoogle Scholar
Cummins, I, Bryant, DN Edwards, R (2009) Safener responsiveness and multiple herbicide resistance in the weed black-grass (Alopecurus myosuroides). Plant Biotechnol J 7:807820 CrossRefGoogle Scholar
Cummins, I, Cole, DJ Edwards, R (1999) A role for glutathione transferases functioning as glutathione peroxidases in resistance to multiple herbicides in black-grass. Plant J 18:285292 CrossRefGoogle ScholarPubMed
Cummins, I, Dixon, DP, Freitag-Pohl, S, Skipsey, M Edwards, R (2011) Multiple roles for plant glutathione transferases in xenobiotic detoxification. Drug Metab Rev 43:266280 CrossRefGoogle ScholarPubMed
Cummins, I, Wortley, DJ, Sabbadin, F, He, Z, Coxon, CR, Straker, HE, Sellars, JD, Knight, K, Edwards, L, Hughes, D, Kaundun, SS, Hutchings, SJ, Steel, PG Edwards, R (2013) Key role for a glutathione transferase in multiple-herbicide resistance in grass weeds. Proc Natl Acad Sci USA 110:58125817 CrossRefGoogle ScholarPubMed
Cuyamendous, C, Leung, KS, Durand, T, Lee, JC-Y, Oger, C Galano, JM (2015) Synthesis and discovery of phytofurans: metabolites of α-linolenic acid peroxidation. Chem Comm 51:1569615699 CrossRefGoogle ScholarPubMed
Dailey, F Cronan, J (1986) Acetohydroxy acid synthase I, a required enzyme for isoleucine and valine biosynthesis in Escherichia coli K-12 during growth on acetate as the sole carbon source. J Bacteriol 165:453460 CrossRefGoogle ScholarPubMed
Dancer, JE, Hughes, RG Lindell, SD (1997) Adenosine-5′-phosphate deaminase: a novel herbicide target. Plant Physiol 114:119129 CrossRefGoogle ScholarPubMed
Dayan, FE, Duke, SO, Sauldubois, A, Singh, N, McCurdy, CR Cantrell, CL (2007) p-Hydroxyphenylpyruvate dioxygenase is a herbicidal target site for β-triketones from Leptospermum scoparium . Phytochemistry 68:20042014 CrossRefGoogle ScholarPubMed
Dayan, FE, Howell, JL Weidenhamer, JD (2009) Dynamic root exudation of sorgoleone and its in planta mechanism of action. J Exp Bot 60:21072117 CrossRefGoogle ScholarPubMed
Dayan, FE, Kuhajek, JM, Canel, C, Watson, SB Moraes, RM (2003) Podophyllum peltatum possesses a β-glucosidase with high substrate specificity for the aryltetralin lignan podophyllotoxin. Biochim Biophys Acta 1646:157163 CrossRefGoogle ScholarPubMed
Dayan, FE, Rimando, AM, Tellez, MR, Scheffler, BE, Roy, T, Abbas, HK Duke, SO (2002) Bioactivation of the fungal phytotoxin 2,5-anhydro-d-glucitol by glycolytic enzymes is an essential component of its mechanism of action. Z Naturforsch 57C:645653 CrossRefGoogle Scholar
Debban, CL, Okum, S, Pieper, KE, Wilson, A Baucom, RS (2015) An examination of fitness costs of glyphosate resistance in the common morning glory, Ipomoea purpurea. Ecol Evol 5:52845294 CrossRefGoogle ScholarPubMed
de Carvalho, LB, Alves, PLCA, González-Torralva, F, Cruz-Hipolito, HE, Rojano-Delgado, AM, De Prado, R, Gil-Humanes, J, Barro, F de Castro, MDL (2012) Pool of resistance mechanisms to glyphosate in Digitaria insularis . J Agric Food Chem 60:615622 CrossRefGoogle ScholarPubMed
Délye, C (2013) Unravelling the genetic bases of non-target-site-based resistance (NTSR) to herbicides: a major challenge for weed science in the forthcoming decade. Pest Manag Sci 69:176187 CrossRefGoogle Scholar
Délye, C, Causse, R, Gautier, V, Poncet, C Michel, S (2015) Using next-generation sequencing to detect mutations endowing resistance to pesticides: application to acetolactate-synthase (ALS) based resistance in barnyard-grass, a polyploid grass weed. Pest Manag Sci 71:675685 CrossRefGoogle ScholarPubMed
DeRidder, BP Goldsbrough, PB (2006) Organ-specific expression of glutathione S-transferases and the efficacy of herbicide safeners in Arabidopsis . Plant Physiol 140:167175 CrossRefGoogle ScholarPubMed
Diehl, KE, Stoller, EW Barrett, M (1995) In vivo and in vitro inhibition of nicosulfuron metabolism by terbufos metabolites in maize Pestic Biochem Physiol 51:137149 CrossRefGoogle Scholar
Dinelli, G, Marotti, I, Bonetti, A, Catizone, P, Urbano, JM Barnes, J (2008) Physiological and molecular bases of glyphosate resistance in Conyza bonariensis biotypes from Spain. Weed Res 48:257265 CrossRefGoogle Scholar
Dinelli, G, Marotti, I, Bonetti, A, Minelli, M, Catizone, P Barnes, J (2006) Physiological and molecular insight on the mechanisms of resistance to glyphosate in Conyza canadensis (L.) Cronq. biotypes. Pestic Biochem Physiol 86:3041 CrossRefGoogle Scholar
Dixon, DP Edwards, R (2010) Glutathione transferases. Arabidopsis Book 8:e0131, 10.1199/tab.0131 CrossRefGoogle ScholarPubMed
Dixon, DP, Hawkins, T, Hussey, PJ Edwards, R (2009) Enzyme activities and subcellular localization of members of the Arabidopsis glutathione transferase superfamily. J Exp Bot 60:12071218 CrossRefGoogle ScholarPubMed
Dueckershoff, K, Mueller, S, Mueller, MJ Reinders, J (2008) Impact of cyclopentenone-oxylipins on the proteome of Arabidopsis thaliana . Biochim Biophys Acta 1784:19751985 CrossRefGoogle ScholarPubMed
Duhoux, A, Carrère, S, Duhoux, A Délye, C (2017a) Transcriptional markers enable identification of rye-grass (Lolium sp.) plants with non-target-site-based resistance to herbicides inhibiting acetolactate-synthase. Plant Sci 257:2236 CrossRefGoogle Scholar
Duhoux, A, Carrère, S, Gouzy, J, Bonin, L Délye, C (2015) RNA-Seq analysis of rye-grass transcriptomic response to an herbicide inhibiting acetolactate-synthase identifies transcripts linked to non-target-site-based resistance. Plant Mol Biol 87:473487 CrossRefGoogle Scholar
Duhoux, A, Pernin, F, Desserre, D Délye, C (2017b) Herbicide safeners decrease sensitivity to herbicides inhibiting acetolactate-synthase and likely activate non-target-site-based resistance pathways in the major grass weed Lolium sp (rye-grass). Front Plant Sci 8:1310 CrossRefGoogle Scholar
Duke, SO (1988) Glyphosate. Pages 170, in Kearney PC, Kaufman DD, eds. Herbicides—Chemistry, Degradation and Mode of Action. Volume 3. New York: Marcel Dekker Google Scholar
Duke, SO (2011) Glyphosate degradation in glyphosate-resistant and -susceptible crops and weeds. J Agric Food Chem 59:58355841 CrossRefGoogle ScholarPubMed
Duke, SO (2012) Why have no new herbicide modes of action appeared in recent years? Pest Manag Sci 68:505512 CrossRefGoogle ScholarPubMed
Duke, SO (2018) The history and current status of glyphosate. Pest Manag Sci 74:10271034 CrossRefGoogle ScholarPubMed
Duke, SO Dayan, FE (2015) Discovery of new herbicide modes of action with natural phytotoxins. Pages 7992 in Maienfisch P, Stevenson TM, eds. Discovery and Synthesis of Crop Protection Products (American Chemical Society Symposium Series 1204). Washington, DC: American Chemical Society Google Scholar
Duke, SO Kenyon, WH (1986) Effects of dimethazone (FMC 57020) on chloroplast development. II. Pigment synthesis and photosynthetic function in cowpea (Vigna unguiculate L.) primary leaves. Pestic Biochem Physiol 25:1117 CrossRefGoogle Scholar
Duke, SO, Rimando, AM, Pace, PF, Reddy, KN Smeda, RJ (2003) Isoflavone, glyphosate, and aminomethylphosphonic acid levels in seed of glyphosate-treated, glyphosate-resistant soybean. J Agric Food Chem 51:340344 CrossRefGoogle ScholarPubMed
Duke, SO, Rimando, AM, Reddy, KN, Cizdziel, JV, Bellaloui, N, Shaw, DR, Williams, MM Maul, JE (2018) Lack of transgene and glyphosate effects on yield, and mineral and amino acid content of glyphosate-resistant soybean. Pest Manag Sci 74:11661173 CrossRefGoogle ScholarPubMed
Durand, T, Bultel-Poncé, V, Guy, A, El Fangour, S, Rossi, JC Galano, JM (2011) Isoprostanes and phytoprostanes: bioactive lipids. Biochimie 93:5260 CrossRefGoogle ScholarPubMed
El-Naggar, SF, Creekmore, RW, Schocken, MJ, Rosen, RT Robinson, RA (1992) Metabolism of clomazone herbicide in soybean. J Agric Food Chem 40:880883 CrossRefGoogle Scholar
Evans, AF, O’Brien, SR, Ma, R, Hager, AG, Riggins, CW, Lambert, KN Riechers, DE (2017) Biochemical characterization of metabolism-based atrazine resistance in Amaranthus tuberculatus and identification of an expressed GST associated with resistance. Plant Biotechnol J 15:12381249 CrossRefGoogle ScholarPubMed
Feng, PCC, Tran, M, Chiu, T, Sammons, RD, Heck, GR CaJacob, CA (2004) Investigations into glyphosate-resistant horseweed (Conyza canadensis): retention, uptake, translocation, and metabolism. Weed Sci 52:498505 CrossRefGoogle Scholar
Ferguson, GM, Hamill, AS Tardif, FJ (2001) ALS inhibitor resistance in populations of Powell amaranth and redroot pigweed. Weed Sci 49:448453 CrossRefGoogle Scholar
Ferhatoglu, Y, Avdiushko, S Barrett, M (2005) The basis for the safening of phorate insecticide phorate in cotton and inhibitors of cytochrome P450s Pestic Biochem Physiol 81:5970 CrossRefGoogle Scholar
Ferhatoglu, Y Barrett, M (2006) Studies of clomazone mode of action. Pestic Biochem Physiol 85:714 CrossRefGoogle Scholar
Figueiredo, MR, Leibhart, LJ, Reicher, ZJ, Tranel, PJ, Nissen, SJ, Westra, P, Bernards, ML, Kruger, GR, Gaines, TA Jugulam, M (2018) Metabolism of 2,4-dichlorophenoxyacetic acid contributes to resistance in a common waterhemp (Amaranthus tuberculatus) population. Pest Manag Sci 74:23562362 CrossRefGoogle Scholar
Fischer, AJ, Ateh, CM, Bayer, DE Hill, JE (2000a) Herbicide-resistant Echinochloa oryzoides and E. phyllopogon in California Oryza sativa fields. Weed Sci 48:225230 CrossRefGoogle Scholar
Fischer, AJ, Bayer, DE, Carriere, MD, Ateh, CM Yim, K-O (2000b) Mechanisms of resistance to bispyribac-sodium in an Echinochloa phyllopogon accession. Pestic Biochem Physiol 68:156165 CrossRefGoogle Scholar
Flagel, LE Wendel, JF (2009) Gene duplication and evolutionary novelty in plants. New Phytol 183:557564 CrossRefGoogle ScholarPubMed
Foes, MJ, Liu, L, Vigue, G, Stoller, EW, Wax, LM Tranel, PJ (1999) A kochia (Kochia scoparia) biotype resistant to triazine and ALS-inhibiting herbicides. Weed Sci 47:2027 Google Scholar
Fonne-Pfister, R, Chemla, P, Ward, E, Girardet, M, Kreuz, KE, Honzatko, RB, Fromm, HJ, Schar, H-P, Grutter, MG Cowan-Jacob, SW (1996) The mode of action and structure of a herbicide in complex with its target: Binding of activated hydantocidin to the feedback regulation site of adenylosuccinate synthetase. Proc Natl Acad Sci USA 93:94319436 CrossRefGoogle ScholarPubMed
Frear, DS (1968) Microsomal N-demethylation, by a cotton leaf oxidase system, of 3-(4′-chlorophenyl)-1,1-dimethylurea (Monuron). Science 162:674675 CrossRefGoogle Scholar
Frear, DS, Swanson, HR Tanaka, FS (1969) N-demethylation of substituted 3-(phenyl)-1-methylureas: isolation and characterization of a microsomal mixed function oxidase from cotton. Phytochemistry 8:21572169 CrossRefGoogle Scholar
Gaines, TA, Lorentz, L, Figge, A, Herrmann, J, Maiwald, F, Ott, M-C, Han, H, Busi, R, Yu, Q, Powles, SB Beffa, R (2014) RNA-Seq transcriptome analysis to identify genes involved in metabolism-based diclofop resistance in Lolium rigidum . Plant J 78:865876 CrossRefGoogle ScholarPubMed
Gao, Q-M, Zhu, S, Pradeep Kachroo, P Kachroo, A (2015) Signal regulators of systemic acquired resistance. Front Plant Sci 6:228 CrossRefGoogle ScholarPubMed
Gardin, JA, Gouzy, J, Carrere, S Delye, C (2015) ALOMYbase, a resource to investigate non-target-site-based resistance to herbicides inhibiting acetolactate-synthase (ALS) in the major grass weed Alopecurus myosuroides (black-grass). BMC Genomics 16:590 CrossRefGoogle Scholar
Gonzalez, VM, Kazimir, J, Nimbal, C, Weston, LA Cheniae, GM (1997) Inhibition of a photosystem II electron transfer reaction by the natural product sorgoleone. J Agric Food Chem 45:14151421 CrossRefGoogle Scholar
Gonzalez-Torralva, F, Gil-Humanes, J, Barro, F, Brants, I De Prado, R (2012a) Target site mutation and reduced translocation are present in a glyphosate-resistant Lolium multiflorum Lam. biotype from Spain. Plant Physiol Biochem 58:1622 CrossRefGoogle Scholar
Gonzalez-Torralva, F, Rojano-Delgado, AM, de Castro, MDL, Muellender, N De Prado, R (2012b) Two non-target mechanisms are involved in glyphosate-resistant horseweed (Conyza canadensis L. Cronq.) biotypes. J Plant Physiol 169:16731679 CrossRefGoogle Scholar
Goodrich, LV, Butts-Wilmsmeyer, CJ, Bollero, GB Riechers, DE (2018) Sequential pyroxasulfone applications with fluxofenim reduce sorghum injury and increase weed control. Agron J 110:19151924 CrossRefGoogle Scholar
Govindarajan, S, Mannervik, B, Silverman, JA, Wright, K, Regitsky, D, Hegazy, U, Purcell, TJ, Welch, M, Minshull, J Gustafsson, C (2015) Mapping of amino acid substitutions conferring herbicide resistance in wheat glutathione transferase. ACS Synth Biol 4:221227 CrossRefGoogle ScholarPubMed
Gray, JA, Balke, NE Stoltenberg, DE (1996) Increased glutathione conjugation of atrazine confers resistance in a Wisconsin velvetleaf (Abutilon theophrasti) biotype. Pestic Biochem Physiol 55:157171 CrossRefGoogle Scholar
Green, JM (2009) Evolution of glyphosate-resistant crop technology. Weed Sci 57:108117 CrossRefGoogle Scholar
Gronwald, JW (1994) Resistance to photosystem II: inhibiting herbicides. Pages 2760 in Powles SB, Holtum JAM, eds. Herbicide Resistance in Plants: Biology and Biochemistry. Boca Raton, FL: CRC Press Google Scholar
Grossmann, K Ehrhardt, T (2007) On the mechanism of action and selectivity of the corn herbicide topramezone: a new inhibitor of 4-hydroxyphenylpyruvate dioxygenase. Pest Manag Sci 63:429439 CrossRefGoogle ScholarPubMed
Grossmann, K Kwiatkowski, J (1993) Selective induction of ethylene and cyanide biosynthesis appears to be involved in the selectivity of the herbicide quinclorac between rice and barnyardgrass. J Plant Physiol 142:457466 CrossRefGoogle Scholar
Guo, J, Riggins, CW, Hausman, NE, Hager, AG, Riechers, DE, Davis, AS Tranel, PJ (2015) Nontarget-site resistance to ALS inhibitors in waterhemp (Amaranthus tuberculatus). Weed Sci 63:399407 CrossRefGoogle Scholar
Guo, L, Qiu, J, Ye, C, Jin, G, Mao, L, Zhang, H, Yang, X, Peng, Q, Wang, Y, Jia, L, Lin, Z, Li, G, Fu, F, Liu, C, Chen, L, Shen, E, Wang, W, Chu, Q, Wu, D, Wu, S, Xia, C, Zhang, Y, Zhou, X, Wang, L, Wu, L, Song, W, Wang, Y, Shu, Q, Aoki, D, Yumoto, E, Yokota, T, Miyamoto, K, Okada, K, Kim, D-S, Cai, D, Zhang, C, Lou, Y, Qian, Q, Yamaguchi, H, Yamane, H, Kong, C-H, Timko, MP, Bai, L Fan, L (2017) Echinochloa crus-galli genome analysis provides insight into its adaptation and invasiveness as a weed. Nature communications 18:1031 CrossRefGoogle Scholar
Guttieri, MJ, Eberlein, CV Thill, DC (1995) Diverse mutations in the acetolactate synthase gene confer chlorsulfuron resistance in kochia (Kochia scoparia) biotypes. Weed Sci 43:175178 Google Scholar
Hager, AG, Wax, LM, Stoller, EW Bollero, GA (2002) Common waterhemp (Amaranthus rudis) interference in soybean. Weed Sci 50:607610 CrossRefGoogle Scholar
Halkier, BA Möller, BL (1989) Biosynthesis of the cyanogenic glucoside dhurrin in seedlings of Sorghum bicolor (L.) Moench and partial purification of the enzyme system involved. Plant Physiol 90:15521559 CrossRefGoogle ScholarPubMed
Hammer, PE, Hinson, TK, Duck, NB Koziel, (2007) May 10. Methods to confer herbicide resistance. US patent application 20070107078 A1, 1-53Google Scholar
Han, H, Yu, Q, Cawthray, GR Powles, SB (2013) Enhanced herbicide metabolism induced by 2,4-D in herbicide susceptible Lolium rigidum provides protection against diclofop-methyl. Pest Manag Sci 69:9961000 CrossRefGoogle ScholarPubMed
Han, H, Yu, Q, Owen, MJ, Cawthray, GR Powles, SB (2016) Widespread occurrence of both metabolic and target site herbicide resistance mechanisms in Lolium rigidum populations. Pest Manag Sci 72:255263 CrossRefGoogle ScholarPubMed
Han, H, Zhu, B, Fu, X, You, S, Wang, B, Li, Z, Zhao, W, Peng, R Yao, Q (2015) Overexpression of d-amino acid oxidase from Bradyrhizobium japonicum, enhances resistance to glyphosate in Arabidopsis thaliana . Plant Cell Rep 34:20432051 CrossRefGoogle ScholarPubMed
Handayani, VDS, Tanno, Y, Yamashita, M, Tobina, H, Ichihara, M, Ishida, Y Sawada, H (2017) influence of weed management measures on glyphosate resistance and endophyte infection in naturalized Italian ryegrass (Lolium multiflorum). Weed Biol Manag 17:8490 CrossRefGoogle Scholar
Hausman, NE, Singh, S, Tranel, PJ, Riechers, DE, Kaundun, SS, Polge, ND, Thomas, DA Hager, AG (2011) Resistance to HPPD-inhibiting herbicides in a population of waterhemp (Amaranthus tuberculatus) from Illinois, United States. Pest Manag Sci 67:258261 CrossRefGoogle Scholar
Heap, I (2018) The International Survey of Herbicide Resistant Weeds. Accessed: May 7, 2018Google Scholar
Hoagland, RE (1980) Effects of glyphosate on metabolism of phenolic compounds. VI. Effects of glyphosine and glyphosate metabolites on phenlalanine ammonia-lyase activity, growth, and protein, chlorophyll, and anthocyanin levels in soybean (Glycine max) seedlings. Weed Sci 28:393400 Google Scholar
Horak, MJ Peterson, DE (1995) Biotypes of Palmer amaranth (Amaranthus palmeri) and common waterhemp (Amaranthus rudis) are resistant to imazethapyr and thifensulfuron. Weed Technol 9:192195 CrossRefGoogle Scholar
Hou, Q, Ufer, G Bartels, D (2016) Lipid signalling in plant responses to abiotic stress. Plant Cell Environ 39:10291048 CrossRefGoogle ScholarPubMed
Huffman, J, Hausman, NE, Hager, AG, Riechers, DE Tranel, PJ (2015) Genetics and inheritance of nontarget-site resistances to atrazine and mesotrione in a waterhemp (Amaranthus tuberculatus) population from Illinois. Weed Sci 63:799809 CrossRefGoogle Scholar
Iwakami, S, Endo, M, Saika, H, Okuno, J, Nakamura, N, Yokoyama, M, Watanabe, H, Toki, S, Uchino, A Inamura, T (2014a) Cytochrome P450 CYP81A12 and CYP81A21 are associated with resistance to two acetolactate synthase inhibitors in Echinochloa phyllopogon . Plant Physiol 165:618629 CrossRefGoogle Scholar
Iwakami, S, Uchino, A, Kataoka, Y, Shibaike, H, Watanabe, H Inamura, T (2014b) Cytochrome P450 genes induced by bispyribac-sodium treatment in a multiple-herbicide resistant biotype of Echinochloa phyllopogon . Pest Manag Sci 70:549558 CrossRefGoogle Scholar
Iwakami, S, Uchino, A, Watanabe, H, Yamasue, Y Inamura, T (2012) Isolation and expression of genes for acetolactate synthase and acetyl-CoA carboxylase in Echinochloa phyllopogon, a polyploid weed species. Pest Manag Sci 68:10981106 CrossRefGoogle ScholarPubMed
Kaloumenos, NS, Chatzilazaridou, SL, Mylona, PV, Polidoros, AN Eleftherohorinos, IG (2012) Target-site mutation associated with cross-resistance to ALS-inhibiting herbicides in late watergrass (Echinochloa oryzicola Vasing). Pest Manag Sci 69:865873 CrossRefGoogle Scholar
Kaundun, SS, Hutchings, S-J, Dale, RP, Howell, A, Morris, JA, Kramer, VC, Shivrain, VK Mcindoe, E (2017) Mechanism of resistance to mesotrione in an Amaranthus tuberculatus population from Nebraska, USA. PloS One 12:e0180095, 10.1371/journal.pone.0180095 CrossRefGoogle Scholar
Keith, BK, Burns, EE, Bothner, B, Carey, CC, Mazurie, AJ, Hilmer, JK, Biyiklioglu, S, Budak, H Dyer, WE (2017) Intensive herbicide use has selected for constitutively elevated levels of stress-responsive mRNAs and proteins in multiple herbicide-resistant Avena fatua L. Pest Manag Sci 73:22672281 CrossRefGoogle ScholarPubMed
Kihara, J, Bationo, A, Waswa, B, Kimetu, J, Vanlauwe, B, Okeyo, J, Mukalama, J Martius, C (2012) Effect of reduced tillage and mineral fertilizer application on maize and soybean productivity. Exp Agric 48:159175 CrossRefGoogle Scholar
Komoßa, D, Gennity, I Sandermann, H (1992) Plant metabolism of herbicides with C-P bonds: glyphosate. Pestic Biochem Physiol 43:8594 CrossRefGoogle Scholar
Koo, AJ (2018) Metabolism of the plant hormone jasmonate: a sentinel for tissue damage and master regulator of stress response. Phytochem Rev 17:5180 CrossRefGoogle Scholar
Koskinen, WC, Marek, LJ Hall, KE (2016) Analysis of glyphosate and aminomethylphosponic acid in water, plant materials and soil. Pest Manag Sci 72:423432.CrossRefGoogle Scholar
Kraehmer, H, Laber, B, Rosinger, C Schulz, A (2014) Herbicides as weed control agents: state of the art. I. Weed control research and safener technology: the path to modern agriculture. Plant Physiol 166:11191131 CrossRefGoogle ScholarPubMed
Kreuz, K Fonne-Pfister, R (1992) Herbicide-insecticide interaction in maize: malathion inhibits cytochrome P450-dependent primisulfuron metabolism. Pestic Biochem Physiol 43:232240 CrossRefGoogle Scholar
Kryuchkova, YV, Burygin, GL, Gogoleva, NE, Gogolev, YV, Chernyshova, MP, Makarov, OE, Fedorov, EE Turkovskaya, OV (2014) Isolation and characterization of a glyphosate-degrading rhizosphere strain, Enterobacter cloacae K7. Microbiol Res 169:99105 CrossRefGoogle ScholarPubMed
Kuklinsky-Sobral, J, Araújo, W, Mendes, R, Pizzirani-Kleiner, A Azevedo, J (2005) Isolation and characterization of endophytic bacteria from soybean (Glycine max) grown in soil treated with glyphosate herbicide. Plant Soil 273:9199 CrossRefGoogle Scholar
Labrou, NE, Papageorgiou, AC, Pavli, O Flemetakis, E (2015) Plant GSTome: structure and functional role in xenome network and plant stress response. Curr Opin Biotechnol 32:186194 CrossRefGoogle ScholarPubMed
Larrieu, A Vernoux, T (2016) How does jasmonate signaling enable plants to adapt and survive? BMC Biol 14:79 CrossRefGoogle ScholarPubMed
Lehtovaara, P (1978) Oxidation of glycine by Phaseolus leghaemoglobin with associated catabolic reactions at the haem. Biochem J 176:351358 CrossRefGoogle ScholarPubMed
Lichtenthaler, HK (1999) The 1-deoxy-d-xylulose-5-phosphate pathway of isoprenoid biosynthesis in plants. Ann Rev Plant Physiol 50:4765 CrossRefGoogle ScholarPubMed
Lichtenthaler, HK, Schwender, J, Disch, A Rohmer, M (1997) Biosynthesis of isoprenoids in higher plant chloroplasts proceeds via a mevalonate independent pathway. FEBS Lett 400:271274 CrossRefGoogle Scholar
Loeffler, C, Berger, S, Guy, A, Durand, T, Bringmann, G, Dreyer, M, von Rad, U, Durner, J Mueller, MJ (2005) B1-phytoprostanes trigger plant defense and detoxification responses. Plant Physiol 137:328340 CrossRefGoogle ScholarPubMed
Lutzov, M, Beyer, P Kleining, H (1990) The herbicide Command does not inhibit prenyl diphosphate-forming enzymes in plastids. Z Naturforsch 45C:856858 CrossRefGoogle Scholar
Lygin, AV, Kaundun, SS, Morris, JA, McIndoe, E, Hamilton, AR Riechers, DE (2018) Metabolic pathway of topramezone in multiple-resistant waterhemp (Amaranthus tuberculatus) differs from naturally tolerant maize. Front Plant Sci, 10.3389/fpls.2018.01644CrossRefGoogle Scholar
Ma, R, Evans, AF, O’Brien, SR, Obenland, O, Lygin, AV, Kaundun, SS Riechers, DE (2018) Biochemical and molecular mechanisms conferring metabolic resistance to multiple herbicides in Amaranthus tuberculatus . Abstr Weed Sci Soc Amer 58:247 Google Scholar
Ma, R, Evans, AF Riechers, DE (2016) Differential responses to atrazine applied preemergence and postemergence in two populations of atrazine-resistant waterhemp (Amaranthus tuberculatus) from Illinois. Agron J 108:11961202 CrossRefGoogle Scholar
Ma, R, Kaundun, SS, Tranel, PJ, Riggins, CW, McGinness, DL, Hager, AG, Hawkes, T, McIndoe, E Riechers, DE (2013) Distinct detoxification mechanisms confer resistance to mesotrione and atrazine in a population of waterhemp. Plant Physiol 163:363377 CrossRefGoogle Scholar
Ma, R, Skelton, JJ Riechers, DE (2015) Measuring rates of herbicide metabolism in dicot weeds with an excised leaf assay. J Visual Exp 103:e53236, 10.3791/53236 Google Scholar
Manalil, S, Busi, R, Renton, M Powles, SB (2011) Rapid evolution of herbicide resistance by low herbicide dosages. Weed Sci 59:210217 CrossRefGoogle Scholar
Manalil, S, Busi, R, Renton, M Powles, SB (2012) An herbicide-susceptible rigid ryegrass (Lolium rigidum) population made even more susceptible. Weed Sci 60:101105 CrossRefGoogle Scholar
Maor, R Shirasu, K (2005) The arms race continues: battle strategies between plants and fungal pathogens. Curr Op Microbiol 8:399404 CrossRefGoogle ScholarPubMed
Matsumoto, H, Riechers, DE, Lygin, AV, Baluska, F Sivaguru, M (2015) Aluminum signaling and potential links with safener-induced detoxification in plants. Pages 135 in Panda S, Baluška F, eds. Aluminum Stress Adaptation in Plants (Signaling and Communication in Plants 24). Cham, Switzerland: Springer International Google Scholar
Matzenbacher, FO, Bortoly, ED, Kalsing, A Merotto, A (2014) Distribution and analysis of the mechanisms of resistance of barnyardgrass (Echinochloa crus-galli) to imidazolinone and quinclorac herbicides. J Agric Sci 153:10441058 CrossRefGoogle Scholar
Miller, KD, Irzyk, GP, Fuerst, E, McFarland, JE, Barringer, M, Cruz, S, Eberle, WJ Föry, W (1996) Identification of metabolites of the herbicide safener benoxacor isolated from suspension-cultured Zea mays cells 3 and 24 hours after treatment. J Agric Food Chem 44:33353341 CrossRefGoogle Scholar
Mitchell, G, Bartlett, DW, Fraser, TEM, Hawkes, TR, Holt, DC, Townson, JK Wichert, RA (2001) Mesotrione: a new selective herbicide for use in maize. Pest Manag Sci 57:120128 3.0.CO;2-E>CrossRefGoogle ScholarPubMed
Moore, RC Purugganan, MD (2005) The evolutionary dynamics of plant duplicate genes. Curr Opin Plant Biol 8:122128 CrossRefGoogle ScholarPubMed
Mosblech, A, Feussner, I Heilmann, I (2009) Oxylipins: structurally diverse metabolites from fatty acid oxidation. Plant Physiol Biochem 47:511517 CrossRefGoogle ScholarPubMed
Mougin, C, Polge, N, Scalla, R Cabanne, F (1991) Interaction of various agrichemicals with cytochrome P450 dependent monooxygenases of wheat cells. Pestic Biochem Physiol 40:111 CrossRefGoogle Scholar
Mueller, MJ (2004) Archetype signals in plants: the phytoprostanes. Curr Opin Plant Biol 7:441448 CrossRefGoogle ScholarPubMed
Mueller, MJ Berger, S (2009) Reactive electrophilic oxylipins: pattern recognition and signalling. Phytochemistry 70:15111521 CrossRefGoogle ScholarPubMed
Mueller, S, Hilbert, B, Dueckershoff, K, Roitsch, T, Krischke, M, Mueller, MJ Berger, S (2008) General detoxification and stress responses are mediated by oxidized lipids through TGA transcription factors in Arabidopsis . Plant Cell 20:768785 CrossRefGoogle ScholarPubMed
Nakka, S, Godar, AS, Thompson, CR, Peterson, DE Jugulam, M (2017a) Rapid detoxification via glutathione S transferase (GST)-conjugation confers high level of atrazine resistance in Palmer amaranth (Amaranthus palmeri). Pest Manag Sci 73:22362243 CrossRefGoogle Scholar
Nakka, S, Godar, AS, Wani, PS, Thompson, CR, Peterson, DE, Roelofs, J Jugulam, M (2017b) Physiological and molecular characterization of hydroxyphenylpyruvate dioxygenase (HPPD)-inhibitor resistance in Palmer amaranth (Amaranthus palmeri S. Wats.). Front Plant Sci 8:555 CrossRefGoogle Scholar
Nakka, S, Thompson, CR, Peterson, DE Jugulam, M (2017c) Target site-based and non-target site based resistance to ALS inhibitors in Palmer amaranth (Amaranthus palmeri). Weed Sci 65:681689 CrossRefGoogle Scholar
Nandula, VK, Reddy, KN, Koger, CH, Poston, DH, Rimando, AM Duke, SO (2012) Multiple resistance to glyphosate and pyrithiobac in Palmer amaranth (Amaranthus palmeri) from Mississippi and response to flumiclorac. Weed Sci 60:179188 CrossRefGoogle Scholar
Nandula, VK, Reddy, KN, Rimando, AM, Duke, SP Poston, DH (2007) Glyphosate-resistant and -susceptible soybean (Glycine max) and canola (Brassica napus) dose response and metabolism relationships with glyphosate. J Agric Food Chem 55:35403545 CrossRefGoogle ScholarPubMed
Ndikuryayo, F, Moosavi, B, Yang, W-C Yang, G-F (2017) 4-Hydroxyphenylpyruvate dioxygenase inhibitors: from chemical biology to agrochemicals. J Agric Food Chem 65:85238537 CrossRefGoogle ScholarPubMed
Nelson, DR, Schuler, MA, Paquette, SM, Werck-Reichhart, D Bak, S (2004) Comparative genomics of rice and Arabidopsis. Analysis of 727 cytochrome P450 genes and pseudogenes from a monocot and a dicot. Plant Physiol 135:756772 CrossRefGoogle Scholar
Neve, P Powles, S (2005) Recurrent selection with reduced herbicide rates results in the rapid evolution of herbicide resistance in Lolium rigidum . Theor Appl Genet 110:11541166 CrossRefGoogle ScholarPubMed
Nicolia, A, Ferradini, N, Molla, G, Biagetti, E, Pollegioni, L, Veronesi, F Rosellini, D (2014) Expression of an evolved engineered variant of a bacterial glycine oxidase leads to glyphosate resistance in alfalfa. J Biotechnol 184:201208.CrossRefGoogle ScholarPubMed
Ober, D (2005) Seeing double: gene duplication and diversification in plant secondary metabolism. Trends Plant Sci 10:444449 CrossRefGoogle ScholarPubMed
Oettmeier, W (1999) Herbicide resistance and supersensitivity in photosystem II. Cell Mol Life Sci 55:12551277 CrossRefGoogle ScholarPubMed
Okazaki, Y Saito, K (2014) Roles of lipids as signaling molecules and mitigators during stress response in plants. Plant J 79:584596 CrossRefGoogle ScholarPubMed
Osuna, MD, Vidotto, F, Fischer, AJ, Bayer, DE, De Prado, R Ferrero, A (2002) Cross-resistance to bispyribac-sodium and bensulfuron-methyl in Echinochloa phyllopogon and Cyperus difformis . Pestic Biochem Physiol 73:917 CrossRefGoogle Scholar
Owen, M, Martinez, N Powles, S (2014) Multiple herbicide-resistant Lolium rigidum (annual ryegrass) now dominates across the Western Australian grain belt. Weed Res 54:314324 CrossRefGoogle Scholar
Pan, G, Zhang, X, Liu, K, Zhang, J, Wu, X, Zhu, J Tu, J (2006) Map-based cloning of a novel rice cytochrome P450 gene CYP81A6 that confers resistance to two different classes of herbicides. Plant Mol Biol 61:933943 CrossRefGoogle ScholarPubMed
Pan, L, Wang, Z, Cai, J, Gao, H, Zhao, H Dong, L (2016) High-throughput sequencing reveals differential regulation of miRNAs in fenoxaprop-P-ethyl resistant Beckmannia syzigachne . Sci Rep 6:28725 CrossRefGoogle ScholarPubMed
Patzoldt, WL Tranel, PJ (2007) Multiple ALS mutations confer herbicide resistance in waterhemp (Amaranthus tuberculatus). Weed Sci 55:421428 CrossRefGoogle Scholar
Pollegioni, L, Schonbrunn, E Siehl, D (2011) Molecular basis of glyphosate resistance—different approaches through protein engineering. FEBS Lett 278:27532766 CrossRefGoogle ScholarPubMed
Powles, SB Yu, Q (2010) Evolution in action: plants resistant to herbicides. Annu Rev Plant Biol 61:317347 CrossRefGoogle ScholarPubMed
Preston, C (2004) Herbicide resistance in weeds endowed by enhanced detoxification: complications for management. Weed Sci 52:448453 CrossRefGoogle Scholar
Preston, C Powles, SB (1998) Amitrole inhibits diclofop metabolism and synergises diclofop-methyl in a diclofop-methyl-resistant biotype of Lolium rigidum . Pestic Biochem Physiol 62:179189 CrossRefGoogle Scholar
Reddy, KN, Cizdziel, JV, Williams, MM, Maul, JE, Rimando, AM Duke, SO (2018) Glyphosate resistance technology has minimal effect on maize mineral nutrition and yield. J Agric Food Chem 66:1013910146 CrossRefGoogle Scholar
Reddy, KN, Duke, SO Rimando, AM (2004) Aminomethylphosphonic acid, a metabolite of glyphosate, causes injury in glyphosate-treated, glyphosate-resistant soybean. J Agric Food Chem 52:51395143 CrossRefGoogle ScholarPubMed
Reddy, KN, Rimando, AM, Duke, SO Nandula, VK (2008) Aminomethylphosphonic acid accumulation in plant species treated with glyphosate. J Agric Food Chem 56:21252130 CrossRefGoogle ScholarPubMed
Riar, DS, Norsworthy, JK, Bond, JA, Bararpour, MT, Wilson, MJ Scott, RC (2012) Resistance of barnyardgrass (Echinochloa crus-galli) populations to acetolactate synthase-inhibiting herbicides. Int J Agron, 10.1155/2012/893953Google Scholar
Riar, DS, Norsworthy, JK, Srivastava, V, Nandula, V, Bond, JA Scott, RC (2013) Physiological and molecular basis of acetolactate synthase-inhibiting herbicide resistance in barnyardgrass (Echinochloa crus-galli). J Agric Food Chem 61:278289 CrossRefGoogle Scholar
Ribeiro, DN, Nandula, VK, Dayan, FE, Rimando, AM, Duke, SO, Reddy, KN Shaw, DR (2015) Possible glyphosate resistance mechanisms in pitted morningglory (Ipomoea lacunosa). J Agric Food Chem 63:16891697 CrossRefGoogle Scholar
Riechers, DE Green, JM (2017) Crop selectivity and herbicide safeners: historical perspectives and development, safener-regulated gene expression, signaling, and new research directions. Pages 123143 in Jugulam M, ed. Biology, Physiology and Molecular Biology of Weeds. Boca Raton, FL: CRC Press CrossRefGoogle Scholar
Riechers, DE, Kreuz, K Zhang, Q (2010) Detoxification without intoxication: herbicide safeners activate plant defense gene expression. Plant Physiol 153:313 CrossRefGoogle ScholarPubMed
Riechers, DE, Ma, R, Baek, Y, Goodrich, L, Lygin, AV Brown, PJ (2018) Herbicide safener-regulated transcripts and metabolites reveal complex signaling, defense, and detoxification pathways in grain sorghum shoots. Abstr Weed Sci Soc Amer 58:238 Google Scholar
Riechers, DE, Zhang, Q, Xu, FX Vaughn, KC (2003) Tissue-specific expression and localization of safener-induced glutathione S-transferase proteins in Triticum tauschii . Planta 217:831840 CrossRefGoogle ScholarPubMed
Rishi, A, Muni, S, Kapur, V, Nelson, ND Goyal, A (2004) Identification and analysis of safener-inducible expressed sequence tags in Populus using a cDNA microarray. Planta 220:296306 CrossRefGoogle ScholarPubMed
Rojano-Delgado, AM, Cruz-Hipolito, H, de Prado, R, de Castro, MDL Franco, AR (2012) Limited uptake, translocation and enhanced metabolic degradation contribute to glyphosate tolerance in Mucuna pruriens var. utilis plants. Phytochemistry 73:3441 CrossRefGoogle ScholarPubMed
Ruiz-Santaella, JP, De Prado, R, Wagner, J, Fischer, AJ Gerhards, R (2006) Resistance mechanisms to cyhalofop-butyl in a biotype of Echinochloa phyllopogon (Stapf) Koss. from California. J Plant Dis Protect 20:95100 Google Scholar
Ruiz-Santaella, JP, Fisher, AJ De Prado, R (2003) Alternative control of two biotypes of Echinochloa phyllopogon susceptible and resistant to fenoxaprop-ethyl. Commun Agric Appl Biol Sci 68:403407 Google ScholarPubMed
Saika, H, Horita, J, Taguchi-Shiobara, F, Nonaka, S, Nishizawa-Yokoi, A, Iwakami, S, Hori, K, Matsumoto, T, Tanaka, T, Itoh, T, Yano, M, Kaku, K, Shimizu, T Toki, S (2014) A novel rice cytochrome P450 gene, CYP72A31, confers tolerance to acetolactate synthase-inhibiting herbicides in rice and Arabidopsis . Plant Physiol 166:12321240 CrossRefGoogle ScholarPubMed
Sammons, RD Gaines, TA (2014) Glyphosate resistance: state of knowledge. Pest Manag Sci 70:13671377 CrossRefGoogle ScholarPubMed
Sandell, L, Amit, J Kruger, GR (2012) Evaluation of a putative HPPD-resistant Palmer amaranth (Amaranthus palmeri) population in Nebraska. Page 82 in Proceedings of the 67th Annual Meeting of the North Central Weed Science Society. St Louis, MO: North Central Weed Science SocietyGoogle Scholar
Scarabel, L, Varotto, S Sattin, M (2007) A European biotype of Amaranthus retroflexus cross-resistant to ALS inhibitors and response to alternative herbicides. Weed Res 47:527533 CrossRefGoogle Scholar
Schueffler, A Anke, T (2014) Fungal natural products in research and development. Nat Prod Rep 31:14251448 CrossRefGoogle ScholarPubMed
Shaner, D (1991) Mechanisms of resistance to acetolactate synthase/acetohydroxyacid synthase inhibitors. Pages 187198 in Duke SO, ed. Herbicide Resistance in Weeds and Crops. New York: Lewis CrossRefGoogle Scholar
Sibony, M, Michel, A, Haas, H, Rubin, B Hurle, K (2001) Sulfometuron-resistant Amaranthus retroflexus: cross-resistance and molecular basis for resistance to acetolactate synthase-inhibiting herbicides. Weed Res 41:509522 CrossRefGoogle Scholar
Sibony, M Rubin, B (2003) Molecular basis for multiple resistance to acetolactate synthase-inhibiting herbicides and atrazine in Amaranthus blitoides (prostrate pigweed). Planta 216:10221027 Google Scholar
Siehl, DL, Castle, LA, Gorton, R Keenan, RJ (2007) The molecular basis of glyphosate resistance by an optimized microbial acetyltransferase. J Biol Chem 15:1144611455 CrossRefGoogle Scholar
Skipsey, M, Knight, KM, Brazier-Hicks, M, Dixon, DP, Steel, PG Edwards, R (2011) Xenobiotic responsiveness of Arabidopsis thaliana to a chemical series derived from a herbicide safener. J Biol Chem 286:3226832276 CrossRefGoogle ScholarPubMed
Song, J-S, Lim, S-H, Yook, M-J, Kim, J-W Kim, D-S (2017) Cross-resistance of Echinochloa species to acetolactate synthase inhibitor herbicides. Weed Biol Manag 17:91102 CrossRefGoogle Scholar
Steckel, LE (2007) The dioecious Amaranthus spp.: here to stay. Weed Technol 21:567570 CrossRefGoogle Scholar
Steckel, LE Sprague, CL (2004) Common waterhemp interference in corn. Weed Sci 52:359364 CrossRefGoogle Scholar
Takeda, S, Erbes, DL, Sweetser, PB, Hay, JV Yuyama, T (1986) Mode of herbicidal and selective action of DPX-F5384 between rice and weeds. J Weed Sci Tech 31:157163 CrossRefGoogle Scholar
Taki, N, Sasaki-Sekimoto, Y, Obayashi, T, Kikuta, A, Kobayashi, K, Ainai, T, Yagi, K, Sakurai, N, Suzuki, H, Masuda, T, Takamiya, K-I, Shibata, D, Kobayashi, Y Ohta, H (2005) 12-Oxophytodienoic acid triggers expression of a distinct set of genes and plays a role in wound-induced gene expression in Arabidopsis . Plant Physiol 139:12681283 CrossRefGoogle Scholar
Tétard-Jones, C Edwards, R (2016) Potential roles for microbial endophytes in herbicide tolerance in plants. Pest Manag Sci 72:203209 CrossRefGoogle ScholarPubMed
Tétard-Jones, C, Sabbadin, F, Moss, S, Hull, R, Neve, P Edwards, R (2018) Unique changes in protein expression in black-grass associated with multiple routes to non-target site resistance towards herbicides. Plant J, 10.1111/tpj.13892Google Scholar
Theodoulou, FL, Clark, IM, He, X-L, Pallett, KE, Cole, DJ Hallahan, DL (2003) Co-induction of glutathione S-transferases and multidrug resistance associated protein by xenobiotics in wheat. Pest Manag Sci 59:202214 CrossRefGoogle ScholarPubMed
Thom, R, Cummins, I, Dixon, DP, Edwards, R, Cole, DJ Lapthorn, AJ (2002) Structure of a tau class glutathione S-transferase from wheat active in herbicide detoxification. Biochemistry 41:70087020 CrossRefGoogle ScholarPubMed
Thompson, C, Peterson, D Lally, N (2012) Characterization of HPPD resistant Palmer amaranth. Proceedings of the 52nd Annual Conference of the Weed Science Society of America. Waikoloa, HI: Weed Science Society of AmericaGoogle Scholar
Tranel, PJ, Wright, TR Heap, IM (2016) Mutations in herbicide-resistant weeds to ALS inhibitors. Accessed March 23, 2018Google Scholar
Varanasi, VK, Godar, AS, Currie, RS, Dille, AJ, Thompson, CR, Stahlman, PW Jugulam, M (2015) Field-evolved resistance to four modes of action of herbicides in a single kochia (Kochia scoparia L. Schrad.) population. Pest Manag Sci 71:12071212 CrossRefGoogle Scholar
Veldhuis, LJ, Hall, LM, O’Donovan, JT, Dyer, W Hall, JC (2000) Metabolism-based resistance of a wild mustard (Sinapis arvensis L.) biotype to ethametsulfuron-methyl. J Agric Food Chem 48:29862990 CrossRefGoogle ScholarPubMed
Verhoeven, KJF, Biere, A, Harvey, JA van der Putten, WH (2009) Plant invaders and their novel natural enemies: who is naïve? Ecology Lett 12:107117 CrossRefGoogle ScholarPubMed
Weimer, MR, Balke, NE Buhler, DD (1992) Herbicide clomazone does not inhibit in-vitro geranylgeranyl synthesis to mevanolate. Plant Physiol 98:427432 CrossRefGoogle ScholarPubMed
Whaley, CM, Wilson, HP Westwood, JH (2006) ALS resistance in several smooth pigweed (Amaranthus hybridus) biotypes. Weed Sci 54:828832 CrossRefGoogle Scholar
Whaley, CM, Wilson, HP Westwood, JH (2007) A new mutation in plant ALS confers resistance to five classes of ALS-inhibiting herbicides. Weed Sci 55:8390 CrossRefGoogle Scholar
Wild, A Ziegler, C (1989) The effect of bialaphos on ammonium-assimilation and photosynthesis. I. Effect on the enzymes of ammonium-assimilation. Z Naturforsch 44C:97102 Google Scholar
Williams, J (2000) Current and future grass herbicides in rice. Pages 123–128 in Proceedings of the California Weed Science SocietyGoogle Scholar
Wright, AA, Nandula, VK, Grier, L, Showmaker, KC, Bond, JA, Peterson, DG, Ray, JD Shaw, DR (2016) Characterization of fenoxaprop-P-ethyl-resistant junglerice (Echinochloa colona) from Mississippi. Weed Sci 64:588595 CrossRefGoogle Scholar
Wright, AA, Rodriguez-Carres, M, Sasidharan, R, Koski, L, Peterson, DG, Nandula, VK, Ray, JD, Bond, JA Shaw, DR (2018) Multiple herbicide resistant junglerice (Echinochloa colona): identification of genes potentially involved in resistance through differential gene expression analysis. Weed Sci 66:347354 CrossRefGoogle Scholar
Wright, AA, Sasidharan, R, Koski, L, Rodriguez-Carres, M, Peterson, DG, Nandula, VK, Ray, JD, Bond, JA Shaw, DR (2017) Transcriptomic changes in Echinochloa colona in response to treatment with the herbicide imazamox. Planta 247:369379 CrossRefGoogle ScholarPubMed
Yan, Y, Christensen, S, Isakeit, T, Engelberth, J, Meeley, R, Hayward, A, Emery, RJN Kolomiets, MV (2012) Disruption of OPR7 and OPR8 reveals the versatile functions of jasmonic acid in maize development and defense. Plant Cell 24:14201436 CrossRefGoogle ScholarPubMed
Yasuor, H, Milan, M, Eckert, JW Fischer, AJ (2012) Quinclorac resistance: a concerted hormonal and enzymatic effort in Echinochloa phyllopogon . Pest Manag Sci 68:108115 CrossRefGoogle ScholarPubMed
Yasuor, H, Osuna, MD, Ortiz, A, Saldain, NE, Eckert, JW Fischer, AJ (2009) Mechanism of resistance to penoxsulam in late watergrass [Echinochloa phyllopogon (Stapf) Koss.]. J Agric Food Chem 57:36533660 CrossRefGoogle Scholar
Yasuor, H, Tenbrook, PL, Tjeerdema, RS Fischer, AJ (2008) Responses to clomazone and 5-ketoclomazone by Echinochloa phyllopogon resistant to multiple herbicides in Californian rice fields. Pest Manag Sci 64:10311039 CrossRefGoogle ScholarPubMed
Yasuor, H, Zou, W, Tolstikov, VV, Tjeerdema, RS Fischer, AJ (2010) Differential oxidative metabolism and 5-ketoclomazone accumulation are involved in Echinochloa phyllopogon resistance to clomazone. Plant Physiol 153:319326 CrossRefGoogle ScholarPubMed
Yu, Q, Han, H, Cawthray, GR, Wang, SF Powles, SB (2013) Enhanced rates of herbicide metabolism in low herbicide-dose selected resistant Lolium rigidum . Plant Cell Environ 36:818827 CrossRefGoogle ScholarPubMed
Yu, Q Powles, S (2014) Metabolism-based herbicide resistance and cross-resistance in crop weeds: a threat to herbicide sustainability and global crop production. Plant Physiol 166:11061118 CrossRefGoogle ScholarPubMed
Zhang, Q, Xu, FX, Lambert, KN Riechers, DE (2007) Safeners coordinately induce the expression of multiple proteins and MRP transcripts involved in herbicide metabolism and detoxification in Triticum tauschii seedling tissues. Proteomics 7:12611278 CrossRefGoogle ScholarPubMed
Zhao, N, Li, W, Bai, S, Guo, WL, Yuan, GH, Wang, F, Liu, WT Wang, JX (2017) Transcriptome profiling to identify genes involved in mesosulfuron-methyl resistance in Alopecurus aequalis . Front Plant Sci 8:1391 CrossRefGoogle ScholarPubMed
Supplementary material: File

Nandula et al. supplementary material

Figure S1

Download Nandula et al. supplementary material(File)
File 315 KB
Supplementary material: File

Nandula et al. supplementary material

Table S2

Download Nandula et al. supplementary material(File)
File 15 KB
Supplementary material: File

Nandula et al. supplementary material

Table S1

Download Nandula et al. supplementary material(File)
File 14 KB
Cited by