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Cross-resistance to acetyl-CoA carboxylase–inhibiting herbicides conferred by a target-site mutation in perennial ryegrass (Lolium perenne) from Argentina

Published online by Cambridge University Press:  13 January 2020

Marcos Yanniccari*
Affiliation:
Researcher, Consejo Nacional de Investigaciones Científicas y Técnicas, Laboratory of Biotechnology and Plant Genetics, Chacra Experimental Integrada Barrow (MAA-INTA), Tres Arroyos, Argentina
Ramón Gigón
Affiliation:
Private Consultant in Weed Control, Tres Arroyos, Argentina
*
Author for correspondence: Marcos Yanniccari, Consejo Nacional de Investigaciones Científicas y Técnicas, Chacra Experimental Integrada Barrow (MAA-INTA), RN 3 km 487, Tres Arroyos (7500), Argentina. (Email: marcosyanniccari@conicet.gov.ar)

Abstract

In Argentina, Lolium spp. occur in 40% of winter cereal crops from the Pampas. Several years ago, cases of glyphosate-resistant perennial ryegrass (Lolium perenne L.) were detected, and the use of acetyl-CoA carboxylase (ACCase)-inhibiting herbicides to eradicate these plants has been considered. The aim of this study was to evaluate the sensitivity of a putative pinoxaden-resistant L. perenne population to ACCase-inhibiting herbicides. Around 80% of plants from the putative resistant population survived at a recommended dose of pinoxaden, and they produced viable seeds. The resistance indices (RIs) to pinoxaden were 5.1 and 2.8 for plant survival and seed production, respectively. A single point mutation that conferred a Asp-2078-Gly substitution in ACCase was the source of the resistance. To match the plant control achieved in the susceptible population, the resistant population required 5.4- and 10.4-fold greater doses of clethodim and quizalofop, respectively. RIs for viable seed production when treated with clethodim and quizalofop were 3.3 and 6.6, respectively. The Asp-2078-Gly mutation endowed significant levels of resistance to pinoxaden, clethodim, and quizalofop. For three herbicides, the level of resistance of a pinoxaden-resistant L. perenne population to ACCase inhibitors was evaluated, based on an evaluation of dose response for plant survival and seed production. The RIs were higher for plant survival than for seed production. In Argentina, the selection pressure associated with clethodim and haloxifop preplant application and pinoxaden use on wheat (Triticum aestivum L.) and barley (Hordeum vulgare L.) crops, would have favored the propagation of the Asp-2078-Gly mutation with its associated resistance.

Type
Research Article
Copyright
© Weed Science Society of America, 2020

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Footnotes

Associate Editor: Franck E. Dayan, Colorado State University

References

Alarcón-Reverte, R, Shanley, S, Kaundun, S, Karp, A, Moss, S (2013) A SNaPshot assay for the rapid and simple detection of known point mutations conferring resistance to ACCase-inhibiting herbicides in Lolium spp. Weed Res 53:1220CrossRefGoogle Scholar
Bararpour, T, Korres, NE, Burgos, NR, Hale, RR, Tseng, TP (2018) Performance of pinoxaden on the control of diclofop-resistant Italian ryegrass (Lolium perenne L. ssp. multiflorum) in winter wheat. Agriculture 8:114CrossRefGoogle Scholar
Baucom, RS (2019) Evolutionary and ecological insights from herbicide-resistant weeds: what have we learned about plant adaptation, and what is left to uncover? New Phytol 223:6882CrossRefGoogle ScholarPubMed
Beckie, H, Warwick, S, Sauder, C (2012) Basis of resistance in Canadian populations of wild oat (Avena fatua). Weed Sci 60:1018CrossRefGoogle Scholar
Beckie, HJ, Reboud, X (2009) Selecting for weed resistance: herbicide rotation and mixture. Weed Technol 23:363370CrossRefGoogle Scholar
Busi, R (2018) Herbicide resistance management: a 10-year case study and a look into the future. Pages 2426in Proceedings of the II Congreso Argentino de Malezas. Rosario, Argentina: Asociación Argentina de Ciencia de las MalezasGoogle Scholar
Cob, AH, Reade, JPH (2010) Inhibitors of lipid biosynthesis. Pages 157175in Cob, AH, Reade, JPH, eds. Herbicide and Plant Physiology. Chichester, UK: Wiley-BlackwellCrossRefGoogle Scholar
Cruz-Hipolito, H, Fernandez, P, Alcantara, P, Gherekhloo, J, Osuna, MD, De Prado, R (2015) Ile-1781-Leu and Asp-2078-Gly mutations in ACCase gene, endow cross-resistance to APP, CHD, and PPZ in Phalaris minor from Mexico. Int J Mol Sci 16:2136321377CrossRefGoogle ScholarPubMed
Cruz-Hipolito, H, Osuna, MD, Domínguez-Valenzuela, JA, Espinoza, N, De Prado, R (2011) Mechanism of resistance to ACCase-inhibiting herbicides in wild oat (Avena fatua) from Latin America. J Agric Food Chem 59:72617267CrossRefGoogle ScholarPubMed
Délye, C (2005) Weed resistance to acetyl coenzyme A carboxylase inhibitors: an update. Weed Sci 53:728746CrossRefGoogle Scholar
De Prado, JL, Osuna, MD, Heredia, A, De Prado, R (2005) Lolium rigidum, a pool of resistance mechanisms to ACCase inhibitor herbicides. J Agric Food Chem 53:21852191CrossRefGoogle ScholarPubMed
Diggle, AJ, Neve, PB, Smith, FP (2003) Herbicides used in combination can reduce the probability of herbicide resistance in finite weed populations. Weed Res 43:371382CrossRefGoogle Scholar
Doyle, J, Doyle, L (1990) Isolation of plant DNA from fresh tissue. Focus 12:1315Google Scholar
Evans, JA, Tranel, PJ, Hager, AG, Schutte, B, Wu, C, Chatham, LA, Davis, AS (2016) Managing the evolution of herbicide resistance. Pest Manag Sci 72:7480CrossRefGoogle ScholarPubMed
Gherekhloo, J, Osuna, MD, De Prado, R (2012) Biochemical and molecular basis of resistance to ACCase-inhibiting herbicides in Iranian Phalaris minor populations. Weed Res 52:367372CrossRefGoogle Scholar
Ghosh, S, Sen-Mandi, S (2018) Methylation status of ACCase promoter affects seed vigor-viability trait in Oryza sativa L. Trop Plant Res 5:17CrossRefGoogle Scholar
Gigón, R, Yanniccari, M (2018) Evaluación de sensibilidad a diferentes herbicidas en poblaciones de Lolium spp. del centro sur de la provincia de Buenos Aires. Page 69 in Proceedings of II Congreso Argentino de Malezas. Rosario, Argentina: ASACIMGoogle Scholar
Heap, I (2019) The International Survey of Herbicide Resistant Weeds. http://www.weedscience.org. Accessed: February 7, 2019Google Scholar
Heap, IM, Knight, R (1982) A population of ryegrass tolerant to the herbicide diclofop-methyl. J Aust Inst Agric Sci 48:156157Google Scholar
Hochberg, O, Sibony, M, Rubin, B (2009) The response of ACCase-resistant Phalaris paradoxa populations involves two different target site mutations. Weed Res 49:3746CrossRefGoogle Scholar
Istilart, C, Yanniccari, M (2012) Análisis de la evolución de malezas en cereales de invierno durante 27 años en la zona sur de la pampa húmeda argentina. Revista Técnica Aapresid 2012(Malezas problema):4750Google Scholar
Jabran, K, Chauhan, BS (2018) Overview and significance of non-chemical weed control. Pages 18in Jabran, K, Chauhan, BS, eds. Non-chemical Weed Control. London: ElsevierGoogle Scholar
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 197:11101116CrossRefGoogle ScholarPubMed
Kaundun, SS (2014) Resistance to acetyl-CoA carboxylase-inhibiting herbicides. Pest Manag Sci 70:14051417CrossRefGoogle ScholarPubMed
Kaundun, SS, Bailly, GC, Dale, RP, Hutchings, S-J, McIndoe, E (2013a) A novel W1999S mutation and non-target site resistance impact on acetyl-CoA carboxylase inhibiting herbicides to varying degrees in a UK Lolium multiflorum population. PLoS ONE 8:e58012CrossRefGoogle Scholar
Kaundun, SS, Hutchings, S, Dale, RP, McIndoe, E (2013b) Role of a novel I1781T mutation and other mechanisms in conferring resistance to acetyl-CoA carboxylase inhibiting herbicides in a black grass population. PLoS ONE 8:e69568CrossRefGoogle Scholar
Keith, BK, Lehnhoff, EA, Burns, EE, Menalled, FD, Dyer, WE (2015) Characterisation of Avena fatua populations with resistance to multiple herbicides. Weed Res 55:621630CrossRefGoogle Scholar
Keshtkar, E, Abdolshahi, R, Sasanfar, H, Zand, E, Beffa, R, Dayan, FE, Kudsk, P (2019) Assessing fitness costs from a herbicide-resistance management perspective: a review and insight. Weed Sci 67:137148CrossRefGoogle Scholar
Kukorelli, G, Reisinger, P, Pinke, G (2013) ACCase inhibitor herbicide—selectivity, weed resistance and fitness cost: a review. Int J Pest Manag 59:165173CrossRefGoogle Scholar
Lemerle, D, Verbeek, B, Combes, NE (1995) Losses in grain yield of winter crops from Lolium rigidum competition depend on crop species, cultivar and season. Weed Res 35:503509CrossRefGoogle Scholar
Liu, W, Harrison, DK, Chalupska, D, Gornicki, P, O’Donnell, CC, Adkins, SW, Haselkorn, R, Williams, RR (2007) Single-site mutations in the carboxyltransferase domain of plastid acetyl-CoA carboxylase confer resistance to grass-specific herbicides. Proc Natl Acad Sci USA 104:36273632CrossRefGoogle ScholarPubMed
Lukatkin, AS, Gar’kova, AN, Bochkarjova, AS, Nushtaeva, OV, Teixeira da Silva, JA (2013) Treatment with the herbicide TOPIK induces oxidative stress in cereal leaves. Pest Biochem Physiol 105:4449CrossRefGoogle ScholarPubMed
Mahmood, K, Mathiassen, SK, Kristensen, M, Kudsk, P (2016) Multiple herbicide resistance in Lolium multiflorum and Identification of conserved regulatory elements of herbicide resistance genes. Front Plant Sci 7:1160CrossRefGoogle ScholarPubMed
Matzrafi, M, Gadri, Y, Frenkel, E, Rubin, B, Peleg, Z (2014) Evolution of herbicide resistance mechanisms in grass weeds. Plant Sci 229:4352CrossRefGoogle ScholarPubMed
Menchari, Y, Chauvel, B, Darmency, H, Délye, C (2008) Fitness costs associated with three mutant acetyl-coenzyme A carboxylase alleles endowing herbicide resistance in black-grass Alopecurus myosuroides. J Appl Ecol 45:939947CrossRefGoogle Scholar
Mithila, J, Godar, AS (2013) Understanding genetics of herbicide resistance in weeds: implications for weed management. Adv Crop Sci Tech 1:14CrossRefGoogle Scholar
Murray, BG, Friesen, LF, Beaulieu, KJ, Morrison, IN (1996) A seed bioassay to identify acetyl-CoA carboxylase inhibitor resistant wild oat (Avena fatua) populations. Weed Tech 10:8589CrossRefGoogle Scholar
Osuna, MD, Goulart, ICGR, Vidal, RA, Kalsing, A, Ruiz Santaella, JP, De Prado, R (2012) Resistance to ACCase inhibitors in Eleusine indica from Brazil involves a target site mutation. Planta Daninha 30:675681CrossRefGoogle Scholar
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 66:168177Google ScholarPubMed
Powles, S, Yu, Q (2010) Evolution in action: plants resistant to herbicides. Annu Rev Plant Biol 61:317347CrossRefGoogle ScholarPubMed
Preston, C (2004) Herbicide resistance in weeds endowed by enhanced detoxification: complications for management. Weed Sci 52:448453CrossRefGoogle Scholar
Preston, C, Tardif, EJ, Christopher, JT, Powles, SB (1996) Multiple resistance to dissimilar herbicide chemistries in a biotype of Lolium rigidum due to enhanced activity of several herbicide degrading enzymes. Pestic Biochem Physiol 54:123134CrossRefGoogle Scholar
Puntarulo, S, Sánchez, R, Boveris, A (1988) Hydrogen peroxide metabolism in soybean embryonic axes at the onset of germination. Plant Physiol 86:626630CrossRefGoogle ScholarPubMed
Sabet Zangeneh, H, Mohammaddust Chamanabad, HR, Zand, E, Alcántara-de la Cruz, R, Travlos, IS, De Prado, R, Alebrahim, MT (2018) Clodinafop-propargyl resistance genes in Lolium rigidum Guad. populations are associated with fitness costs. Agronomy 8:106CrossRefGoogle Scholar
Sasaki, Y, Nagano, Y (2004) Plant acetyl-CoA carboxylase: structure, biosynthesis, regulation, and gene manipulation for plant breeding. Biosci Biotechnol Biochem 68:11751184CrossRefGoogle ScholarPubMed
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 47:527533CrossRefGoogle Scholar
Scursoni, J, Gigón, R, Martin, A, Vigna, M, Leguizamón, E, Istilart, C, López, R (2014) Changes in weed communities of spring wheat crops of Buenos Aires province of Argentina. Weed Sci 62:5162Google Scholar
Scursoni, JA, Palmano, M, De Notta, A, Delfino, D (2012) Italian ryegrass (Lolium multiflorum Lam.) density and N fertilization on wheat (Triticum aestivum L.) yield in Argentina. Crop Prot 32:3640CrossRefGoogle Scholar
Senseman, S, ed (2007) Herbicide Handbook. 9th ed. Lawrence, MA: Weed Science Society of America. 458 pGoogle Scholar
Siminszky, B (2006) Plant cytochrome P450-mediated herbicide metabolism. Phytochem Rev 5:445458CrossRefGoogle Scholar
Smit, JJ, Smit, HA, de Villiers, BL (1999) Differential efficacy of tralkoxydim and diclofop-methyl on a suspected resistant ryegrass (Lolium rigidum Gaud.) biotype. S Afr J Plant Soil 16:169172CrossRefGoogle Scholar
Vila-Aiub, MM, Neve, P, Powles, SB (2005) Resistance cost of a cytochrome P450 herbicide metabolism mechanism but not an ACCase target site mutation in a multiple resistant Lolium rigidum population. New Phytol 167:787796CrossRefGoogle ScholarPubMed
Vila-Aiub, MM, Yu, Q, Han, H, Powles, SB (2015) Effect of herbicide resistance endowing Ile-1781-Leu and Asp-2078-Gly ACCase gene mutations on ACCase kinetics and growth traits in Lolium rigidum. J Exp Bot 66:47114718CrossRefGoogle ScholarPubMed
Yanniccari, M, Gigón, R, Istilart, C, Castro, AM (2018) Mecanismos de resistencia a múltiples herbicidas en poblaciones de Lolium spp. del sur de la provincia de Buenos Aires. Page 242 in Proceedings of the II Congreso Argentino de Malezas. Rosario, Argentina: Asociación Argentina de Ciencia de las MalezasGoogle Scholar
Yanniccari, M, Istilart, C, Giménez, DO, Castro, AM (2012) Glyphosate resistance in perennial ryegrass (Lolium perenne L.) from Argentina. Crop Prot 32:1216CrossRefGoogle Scholar
Yu, LPC, Kim, YS, Tong, L (2010) Mechanism for the inhibition of the carboxyl-transferase domain of acetyl-coenzyme A carboxylase by pinoxaden. Proc Natl Acad Sci USA 107:2207222077CrossRefGoogle Scholar
Yu, Q, Collavo, A, Zheng, MQ, Owen, M, Sattin, M, Powles, SB (2007) Diversity of acetyl-coenzyme A carboxylase mutations in resistant Lolium populations: evaluation using clethodim. Plant Physiol 145:547548CrossRefGoogle 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 166:11061118CrossRefGoogle ScholarPubMed
Zhang, P, Wu, H, Xu, H, Gao, Y, Zhang, W (2017) Dong L, Mechanism of Fenoxaprop-P-ethyl Resistance in Italian Ryegrass (Lolium perenne ssp. multiflorum) from China. Weed Sci 65:18CrossRefGoogle Scholar