, Volume 244, Issue 6, pp 1217–1227 | Cite as

Climate change increases the risk of herbicide-resistant weeds due to enhanced detoxification

  • Maor Matzrafi
  • Bettina Seiwert
  • Thorsten Reemtsma
  • Baruch Rubin
  • Zvi Peleg
Original Article


Main conclusion

Global warming will increase the incidence of metabolism-based reduced herbicide efficacy on weeds and, therefore, the risk for evolution of non-target site herbicide resistance.

Climate changes affect food security both directly and indirectly. Weeds are the major biotic factor limiting crop production worldwide, and herbicides are the most cost-effective way for weed management. Processes associated with climatic changes, such as elevated temperatures, can strongly affect weed control efficiency. Responses of several grass weed populations to herbicides that inhibit acetyl-CoA carboxylase (ACCase) were examined under different temperature regimes. We characterized the mechanism of temperature-dependent sensitivity and the kinetics of pinoxaden detoxification. The products of pinoxaden detoxification were quantified. Decreased sensitivity to ACCase inhibitors was observed under elevated temperatures. Pre-treatment with the cytochrome-P450 inhibitor malathion supports a non-target site metabolism-based mechanism of herbicide resistance. The first 48 h after herbicide application were crucial for pinoxaden detoxification. The levels of the inactive glucose-conjugated pinoxaden product (M5) were found significantly higher under high- than low-temperature regime. Under high temperature, a rapid elevation in the level of the intermediate metabolite (M4) was found only in pinoxaden-resistant plants. Our results highlight the quantitative nature of non-target-site resistance. To the best of our knowledge, this is the first experimental evidence for temperature-dependent herbicide sensitivity based on metabolic detoxification. These findings suggest an increased risk for the evolution of herbicide-resistant weeds under predicted climatic conditions.


Diclofop-methyl Global warming Herbicide metabolism Non-target-site resistance Temperature-dependent sensitivity Weed management 



Acetyl-CoA carboxylase


Cytochrome P450 monooxygenase


Days after treatment


Hours after treatment


Non-target site


Resistance index


Target site


Temperature sensitivity index


Effective dose required to control 50% of weed population



This study was supported by the Chief Scientist of the Israeli Ministry of Agriculture and Rural Development (Grant Nos. 837-0150-14 and 12-02-0023) and ADAMA Agricultural Solutions. The authors would like to thank M. Sibony, Z Kleinman, T. Kliper, and L. Shaar-Moshe for their assistance with the experiments. The authors would also like to thank Dr. Shiv S. Kaundun (Syngenta) for providing technical-grade pinoxaden. We are also thankful for the insightful comments provided by the anonymous reviewers.

Supplementary material

425_2016_2577_MOESM1_ESM.docx (849 kb)
Supplementary material 1 (DOCX 848 kb)


  1. Anderson DM, Swanton CJ, Hall JC, Mersey BG (1993) The influence of temperature and relative humidity on the efficacy of glufosinate-ammonium. Weed Res 33:139–147CrossRefGoogle Scholar
  2. Asseng S, Ewert F, Martre P et al (2014) Rising temperatures reduce global wheat production. Nat Clim Change 5:143–147CrossRefGoogle Scholar
  3. Beckie HJ, Tardif FJ (2012) Herbicide cross resistance in weeds. Crop Protect 35:15–28CrossRefGoogle Scholar
  4. Bravin F, Zanin G, Preston C (2001) Diclofop-methyl resistance in populations of Lolium spp. from central Italy. Weed Res 41:49–58CrossRefGoogle Scholar
  5. Caseley JC (1989) Variation in foliar pesticide performance attributable to humidity, dew and rain effects. Asp Appl Biol 21:215–225Google Scholar
  6. Christopher JT, Preston C, Powles SB (1994) Malathion antagonizes metabolism-based chlorsulfuron resistance in Lolium rigidum. Pestic Biochem Physiol 49:172–182CrossRefGoogle Scholar
  7. Cole DJ, Edwards R (2000) Secondary metabolism of agrochemicals in plants. In: Roberts TR (ed) Agrochemicals and plant protection. Wiley, Chichester, pp 107–154Google Scholar
  8. Cotterman JC, Saari LL (1992) Rapid metabolic chlorsulfuron inactivation is the basis for cross-resistance in diclofop-methyl-resistant rigid ryegrass (Lolium rigidum) biotype SR4/84. Pestic Biochem Physiol 43:182–192CrossRefGoogle Scholar
  9. De Lucia M, Panzella L, Pezzella A, Napolitano A, D’Ischia M (2008) Plant catechols and their S-glutathionyl conjugates as antinitrosating agents: expedient synthesis and remarkable potency of 5-S-glutathionylpiceatannol. Chem Res Tox 21:2407–2413CrossRefGoogle Scholar
  10. 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 69:176–187CrossRefPubMedGoogle Scholar
  11. Délye C, Jasieniuk M, Le Corre V (2013) Deciphering the evolution of herbicide resistance in weeds. Trends Genet 29:649–658CrossRefPubMedGoogle Scholar
  12. Easterling DR, Meehl GA, Parmesan C, Changnon SA, Karl TR, Mearns LO (2000) Climate extremes: observations, modelling, and impacts. Science 289:2068–2074CrossRefPubMedGoogle Scholar
  13. Edwards R, Cole DJ (1996) Glutathione transferases in wheat (Triticum) species with activity toward fenoxaprop-ethyl and other herbicides. Pestic Biochem Physiol 54:96–104CrossRefGoogle Scholar
  14. EFSA (2013) Conclusion on the peer review of the pesticide risk assessment of the active substance pinoxaden. EFSA J 11(8):3269. doi: 10.2903/j.efsa.2013.3269 CrossRefGoogle Scholar
  15. Ellis AT, Steckel LE, Main CL, de Melo MSC, West DR, Mueller TC (2010) A survey for diclofop-methyl resistance in italian ryegrass from Tennessee and how to manage resistance in wheat. Weed Tech 24:303–309CrossRefGoogle Scholar
  16. Fantke P, Gillespie BW, Juraske R, Jolliet O (2014) Estimating half-lives for pesticide dissipation from plants. Environ Sci Tech 48:8588–8602CrossRefGoogle Scholar
  17. FAOSTAT (2016) Food and agriculture organization of the united nations-statistics division. Accessed 7 Mar 2016
  18. Gardin JAC, Boucansaud K, Chauvel B, Petit C (2011) Non-target-site-based resistance should be the centre of attention for herbicide resistance research: Alopecurus myosuroides as an illustration. Weed Res 51:433–437CrossRefGoogle Scholar
  19. Ge X, D’Avignon D, Ackerman JJH, Duncan B, Spaur MB, Sammons RD (2011) Glyphosate-resistant horseweed made sensitive to glyphosate: low-temperature suppression of glyphosate vacuolar sequestration revealed by 31P NMR. Pest Manag Sci 67:1215–1221CrossRefPubMedGoogle Scholar
  20. Godfray HCJ, Beddington JR, Crute IR et al (2010) Food security: the challenge of feeding 9 billion people. Science 327:812–818CrossRefPubMedGoogle Scholar
  21. Gornall J, Betts R, Burke E, Clark R, Camp J, Willett K, Wiltshire A (2010) Implications of climate change for agricultural productivity in the early twenty-first century. Philos Trans R Soc B Biol Sci 365:2973–2989CrossRefGoogle Scholar
  22. Griffith SM, Brewer TG, Steiner JJ (2001) Thermal dependence of the apparent Km of glutathione reductase from three wetland grasses and maize. Ann Bot 87:599–603CrossRefGoogle Scholar
  23. Hamada SHE, Abdel-Lateef MF, Abdelmonem AE et al (2013) Efficiency of certain clodinafop-propargyl formulations in controlling annual grassy weeds in wheat. Ann Agric Sci 58:13–18Google Scholar
  24. Hammerton JL (1967) Environmental factors and susceptibility to herbicides. Weed Sci 15:330–336CrossRefGoogle Scholar
  25. 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 69:996–1000CrossRefPubMedGoogle Scholar
  26. Han H, Yu Q, Vila-Aiub M, Powles SB (2014) Genetic inheritance of cytochrome P450-mediated metabolic resistance to chlorsulfuron in a multiple herbicide resistant Lolium rigidum population. Crop Prot 65:57–63CrossRefGoogle Scholar
  27. Heap I (2016) The international survey of herbicide resistant weeds. Accessed 31 May 2016
  28. Holtum JAM, Matthews JM, Häusler RE, Liljegren DR, Powles SB (1991) Cross-resistance to herbicides in annual ryegrass (Lolium rigidum). Plant Physiol 97:1026–1034CrossRefPubMedPubMedCentralGoogle Scholar
  29. HRAC (2016) Classification of herbicides according to mode of action. Accessed 31 May 2016
  30. Jang S, Marjanovic J, Gornicki P (2013) Resistance to herbicides caused by single amino acid mutations in acetyl-CoA carboxylase in resistant populations of grassy weeds. New Phytol 197:1110–1116CrossRefPubMedGoogle Scholar
  31. Kleinman Z, Ben-Ami G, Rubin B (2016) From sensitivity to resistance–factors affecting the response of Conyza spp. to glyphosate. Pest Manag Sci. doi: 10.1002/ps.4187 Google Scholar
  32. Kreuz K, Fonné-Pfister R (1992) Herbicide-insecticide interaction in maize: malathion inhibits cytochrome P450-dependent primisulfuron metabolism. Pestic Biochem Physiol 43:232–240CrossRefGoogle Scholar
  33. Kreuz K, Tommasini R, Martinoia E (1996) Old enzymes for a new job. Plant Physiol 111:349–353PubMedPubMedCentralGoogle Scholar
  34. Kuk YI, Burgos NR, Talbert RE (2000) Cross- and multiple resistance of diclofop-resistant Lolium spp. Weed Sci 48:412–419CrossRefGoogle Scholar
  35. Lamichhane JR, Barzman M, Booij K et al (2014) Robust cropping systems to tackle pests under climate change. A review. Agron Sustain Dev 35:443–459CrossRefGoogle Scholar
  36. Lasat MM, DiTomaso JM, Hart JJ, Kochian LV (1996) Resistance to paraquat in Hordeum glaucum is temperature dependent and not associated with enhanced apoplasmic binding. Weed Res 36:303–309CrossRefGoogle Scholar
  37. Leclère D, Havlík P, Fuss S et al (2014) Climate change induced transformations of agricultural systems: insights from a global model. Environ Res Lett 9:1–14CrossRefGoogle Scholar
  38. Lelieveld J, Proestos Y, Hadjinicolaou P et al (2016) Strongly increasing heat extremes in the Middle East and North Africa (MENA) in the 21st century. Clim Change 137:245–260CrossRefGoogle Scholar
  39. Llewellyn R, Powles S (2001) High levels of herbicide resistance in rigid ryegrass (Lolium rigidum) in the wheat belt of Western Australia. Weed Technol 15:242–248CrossRefGoogle Scholar
  40. Mahan JR, Dotray PA, Light GG, Dawson KR (2006) Thermal dependence of bioengineered glufosinate tolerance in cotton. Weed Sci 54:1–5CrossRefGoogle Scholar
  41. Matzrafi M, Gadri Y, Frenkel E, Rubin B, Peleg Z (2014) Evolution of herbicide resistance mechanisms in grass weeds. Plant Sci 229:43–52CrossRefPubMedGoogle Scholar
  42. McFadden JJ, Frear DS, Mansager ER (1989) Aryl hydroxylation of diclofop by a cytochrome P450 dependent monooxygenase from wheat. Pestic Biochem Physiol 34:92–100CrossRefGoogle Scholar
  43. Muehlebach M, Cederbaum F, Cornes D et al (2011) Aryldiones incorporating a [1,4,5] oxadiazepane ring. Part 2: chemistry and biology of the cereal herbicide pinoxaden. Pest Manag Sci 67:1499–1521CrossRefPubMedGoogle Scholar
  44. Nandula VK, Messersmith CG (2002) Imazamethabenz-resistant wild oat (Avena fatua L.) is resistant to diclofop-methyl. Pestic Biochem Physiol 74:53–61CrossRefGoogle Scholar
  45. Noctor G, Mhamdi A, Chaouch S et al (2012) Glutathione in plants: an integrated overview. Plant Cell Environ 35:454–484CrossRefPubMedGoogle Scholar
  46. Oerke EC (2006) Crop losses to pests. J Agric Sci 144:31–43CrossRefGoogle Scholar
  47. Papapanagiotou AP, Paresidou MI, Kaloumenos NS, Eleftherohorinos IG (2015) ACCase mutations in Avena sterilis populations and their impact on plant fitness. Pestic Biochem Physiol 123:40–48CrossRefPubMedGoogle Scholar
  48. Pavlostathis SG, Didem OT (2007) Temperature and pH effect on the microbial reductive transformation of pentachloronitrobenzene. J Agric Food Chem 55:5390–5398CrossRefPubMedGoogle Scholar
  49. Petit C, Bay G, Pernin F, Délye C (2010) Prevalence of cross- or multiple resistance to the acetyl-coenzyme A carboxylase inhibitors fenoxaprop, clodinafop and pinoxaden in black-grass (Alopecurus myosuroides Huds.) in France. Pest Manag Sci 66:168–177PubMedGoogle Scholar
  50. Rivers J, Warthmann N, Pogson B, Borevitz J (2015) Genomic breeding for food, environment and livelihoods. Food Security 7:375–382CrossRefGoogle Scholar
  51. Robinson MA, Letarte J, Cowbrough MJ, Sikkema PH, Tardif FJ (2015) Winter wheat (Triticum aestivum L.) response to herbicides as affected by application timing and temperature. Can J Plant Sci 95:325–333CrossRefGoogle Scholar
  52. Saari LL, Cotterman JC, Primiani MM (1990) Mechanism of sulfonylurea herbicide resistance in the broadleaf weed, Kochia scorpia. Plant Physiol 93:55–61CrossRefPubMedPubMedCentralGoogle Scholar
  53. Scarabel L, Panozzo S, Varotto S, Sattin M (2011) Allelic variation of the ACCase gene and response to ACCase-inhibiting herbicides in pinoxaden-resistant Lolium spp. Pest Manag Sci 67:932–941CrossRefPubMedGoogle Scholar
  54. Schlenker W, Roberts MJ (2009) Nonlinear temperature effects indicate severe damages to US crop yields under climate change. Proc Natl Acad Sci USA 106:15594–15598CrossRefPubMedPubMedCentralGoogle Scholar
  55. Seefeldt SS, Jensen JE, Fuerst EP (1995) Feature log-logistic analysis of herbicide dose-response relationships. Weed Technol 9:218–227Google Scholar
  56. Solomon S, Qin D, Manning M et al (2007) Climate change 2007. In: Solomon S, Qin D, Manning M et al (eds) The physical science basis: Contribution of Working Group I to the Fourth Assessment Report of the IPCC. Cambridge University, New York, pp 1–8Google Scholar
  57. Stott P (2016) How climate change affects extreme weather events. Science 352:1517–1518CrossRefPubMedGoogle Scholar
  58. Tal AJ, Hall JC, Stephenson GR (1995) Non-enzymatic conjugation of fenoxaprop-ethyl with glutathione and cysteine in several grass species. Weed Res 35:133–139CrossRefGoogle Scholar
  59. Tester M, Langridge P (2010) Breeding technologies to increase crop production in a changing world. Science 327:818–822CrossRefPubMedGoogle Scholar
  60. Tripathi A, Tripathi DK, Chauhan DK, Kumar N, Singh GS (2016) Paradigms of climate change impacts on some major food sources of the world: a review on current knowledge and future prospects. Agric Ecosyst Environ 216:356–373CrossRefGoogle Scholar
  61. Tripathy L, Dash SK, Dash DK, Murmu S (2015) Effect of chemicals on weed control in spray Chrysanthemum. J Crop Weed 11:217–219Google Scholar
  62. Viger PR, Eberlein CV, Fuerst EP, Gronwald JW (1991) Effects of CGA-154281 and temperature on metolachlor absorption and metabolism, glutathione content, and glutathione-s-transferase activity in corn. Weed Sci 39:324–328Google Scholar
  63. Walther G, Post E, Convey P et al (2002) Ecological responses to recent climate change. Nature 416:389–395CrossRefPubMedGoogle Scholar
  64. Wenger J, Niderman T (2007) Acetyl-CoA carboxylase inhibitors. In: Krämer W, Schirmer U (eds) Modern crop protection compounds, vol 3. Wiley-VCH, Weinheim, pp 335–357CrossRefGoogle Scholar
  65. Yu Q, Han H, Nguyen L, Forster JW, Powles SB (2009) Paraquat resistance in a Lolium rigidum population is governed by one major nuclear gene. Theor Appl Genet 118:1601–1608CrossRefPubMedGoogle Scholar
  66. Yu Q, Han H, Cawthray GR, Wang SF, Powles SB (2012) Enhanced rates of herbicide metabolism in low herbicide-dose selected resistant Lolium rigidum. Plant Cell Environ 36:818–827CrossRefPubMedGoogle Scholar
  67. Yuan JS, Tranel PJ, Stewart CN (2006) Non-target-site herbicide resistance: a family business. Trends Plant Sci 12:6–13CrossRefPubMedGoogle Scholar
  68. Ziska LH (2000) The impact of elevated CO2 on yield loss from a C3 and C4 weed in field-grown soybean. Global Change Biol 6:899–905CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.The Robert H. Smith Institute of Plant Sciences and Genetics in Agriculture, The Robert H. Smith Faculty of Agriculture, Food and EnvironmentThe Hebrew University of JerusalemRehovotIsrael
  2. 2.Department of Analytical ChemistryHelmholtz-Centre for Environmental Research - UFZLeipzigGermany

Personalised recommendations