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Rapid necrosis: a novel plant resistance mechanism to 2,4-D

Published online by Cambridge University Press:  05 November 2019

Andrew R. S. de Queiroz
Affiliation:
Graduate Student, Department of Crop Science, Federal University of Rio Grande do Sul–UFRGS, Porto Alegre, RS, Brazil
Carla A. Delatorre
Affiliation:
Professor, Department of Crop Science, Federal University of Rio Grande do Sul–UFRGS, Porto Alegre, RS, Brazil
Felipe R. Lucio
Affiliation:
Integrated Field Science, Dow AgroSciences Industrial LTDA, São Paulo, Brazil
Caio V. S. Rossi
Affiliation:
Integrated Field Science, Dow AgroSciences Industrial LTDA, São Paulo, Brazil
Luiz H. S. Zobiole
Affiliation:
Integrated Field Science, Dow AgroSciences Industrial LTDA, São Paulo, Brazil
Aldo Merotto Jr*
Affiliation:
Professor, Department of Crop Science, Federal University of Rio Grande do Sul–UFRGS, Porto Alegre, RS, Brazil
*
Author for correspondence: Aldo Merotto Jr, Department of Crop Science, Federal University of Rio Grande do Sul–UFRGS, 7712 Bento Goncalves Avenue, Porto Alegre, RS, Brazil91501-970. (Email: merotto@ufrgs.br)

Abstract

Plants of Sumatran fleabane [Conyza sumatrensis (Retz.) E. Walker] were identified in a field with an unusual rapid leaf-injury herbicide symptoms after application of 2,4-D in mixture with glyphosate. The objectives of this study were to confirm the occurrence of resistance to 2,4-D herbicide and to characterize the occurrence of rapid necrosis as the mechanism associated with the herbicide resistance in C. sumatrensis. The studies performed were an initial screening, effect of 2,4-D alone and associated with glyphosate, cross- and multiple-resistance evaluation, effect of commercial formulation and analytical product, and rate of H2O2 evolution. The Marpr9-rn accession was identified with rapid necrosis symptoms and survival to 804 g ae ha−1 of 2,4-D. The resistance factor to the herbicide 2,4-D was 18.6 at 49 d after spraying. The analytical product 2,4-D and the commercial formulation resulted in similar symptoms of rapid necrosis. This symptom did not occur for the six other auxinic herbicides (dicamba, florpyrauxifen-benzyl, fluroxypyr, halauxifen-methyl, picloram, and triclopyr), indicating absence of cross-resistance. Multiple resistance to the herbicides paraquat, saflufenacil, and ammonium glufosinate was not identified in the Marpr9-rn population. However, survival following treatment with the herbicides glyphosate and chlorimuron-ethyl occurred. The evolution of H2O2 began at 15 min after application and was less pronounced in low light. These results indicate the first case of resistance to 2,4-D and occurrence of rapid necrosis in C. sumatrensis.

Type
Research Article
Copyright
© Weed Science Society of America, 2019

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Footnotes

Associate Editor: William Vencill, University of Georgia

References

Bestwick, CS, Brown, IR, Mansfield, JW (1998) Localized changes in peroxidase activity accompany hydrogen peroxide generation during the development of a nonhost hypersensitive reaction in lettuce. Plant Physiol 118:10671078CrossRefGoogle ScholarPubMed
Brabham, CB, Gerber, CK, Johnson, WG (2011) Fate of glyphosate-resistant giant ragweed (Ambrosia trifida) in the presence and absence of glyphosate. Weed Sci 59:506511CrossRefGoogle Scholar
Burke, IC, Yenish, JP, Pittmann, D, Gallagher, RS (2009) Resistance of a prickly lettuce (Lactuca serriola) biotype to 2,4-D. Weed Technol 23:586591CrossRefGoogle Scholar
Byker, HP, Soltani, N, Robinson, DE, Tardif, J, Lawton, MB, Sikkema, PH (2013) Occurrence of glyphosate and cloransulam resistant Canada fleabane (Conyza canadensis L. Cronq.) in Ontario. Can J Plant Sci 93:851855CrossRefGoogle Scholar
Cho, M, Cho, HT (2013) The function of ABCB transporters in auxin transport. Plant Signal Behav 8:e22990CrossRefGoogle ScholarPubMed
Dahlke, RI, Luethen, H, Steffens, B (2010) ABP1: an auxin receptor for fast responses at the plasma membrane. Plant Signal Behav 5:13CrossRefGoogle ScholarPubMed
Dang, HT, Malone, JM, Boutsalis, P, Krishnan, M, Gill, G, Preston, C (2018) Reduced translocation in 2,4-D-resistant oriental mustard populations (Sisymbrium orientale L.) from Australia. Pest Manag Sci 74:1524–32CrossRefGoogle ScholarPubMed
Doorn, WG van, Beers, EP, Dangl, JL, Franklin-Tong, VE, Gallois, P, Hara-Nishimura, I, Jones, AM, Kawai-Yamada, M, Lam, E, Mundy, J, Mur, LAJ, Petersen, M, Smertenko, A, Taliansky, M, Van Breusegem, F, et al. (2011) Morphological classification of plant cell deaths. Cell Death Differ 18:12411246CrossRefGoogle ScholarPubMed
Figueiredo, MRA, 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 74:23562362CrossRefGoogle Scholar
Flessner, ML, McElroy, JS, Mccurdy, JD, Toombs, JM, Wehtje, GR, Burmester, CH, Price, AJ, Ducar, JT (2015) Glyphosate-resistant horseweed (Conyza canadensis) control with dicamba in Alabama. Weed Technol 29:633640CrossRefGoogle Scholar
Fuerst, EP, Nakatani, HY, Dodge, AD, Arntzen, Penner D (1985) Paraquat resistance in Conyza. Plant Physiol 77:984989CrossRefGoogle ScholarPubMed
Fuerst, EP, Sterling, TM, Norman, MA, Prather, TS, Irzyk, GP, Wu, Y, Lownds, NK, Callihan, RH (1996) Physiological characterization of picloram resistance in yellow starthistle. Pestic Biochem Physiol 56:149161CrossRefGoogle Scholar
Ghanizadeh, H, Harrington, KC (2017) Non-target site mechanisms of resistance to herbicides. Crit Rev Plant Sci 36:2434CrossRefGoogle Scholar
Goggin, DE, Cawthray, GR, Powles, SB (2016) 2,4-D resistance in wild radish: reduced herbicide translocation via inhibition of cellular transport. J Exp Bot 67:32233235CrossRefGoogle ScholarPubMed
Grones, P, Friml, J (2015) Auxin transporters and binding proteins at a glance. J Cell Sci 128:17CrossRefGoogle ScholarPubMed
Grossmann, K (2010) Auxin herbicides: current status of mechanism and mode of action. Pest Manag Sci 66:113120Google ScholarPubMed
Hall, JC, Alam, SMM, Murr, DP (1993) Ethylene biosynthesis following foliar application of picloram to biotypes of wild mustard (Sinapis arvensis L.) susceptible or resistant to auxinic herbicides. Pestic Biochem and Physiol 47:3643CrossRefGoogle Scholar
Heap, I (2019) The International Survey of Herbicide Resistant Weeds. http://www.weedscience.org. Accessed: May 13, 2019Google Scholar
Hilton, HW (1957) Herbicide Tolerant Strains of Weeds. Hawaiian Sugar Planters Association Annual Report. Honolulu, HI: University of Hawaii, Manoa Library. Pp 6972Google Scholar
Jeffery, T (2014) Investigation into the Molecular and Biochemical Mechanisms of Resistance in Two Biotypes of Glyphosate Resistant Giant Ragweed. MS dissertation. Guelph, Ontario: University of Guelph. 77 pGoogle Scholar
Jugulam, M, Dimeo, N, Veldhuis, LJ, Walsh, M, Hall, JC (2013) Investigation of MCPA (4-chloro-2-ethylphenoxyacetate) resistance in wild radish (Raphanus raphanistrum L.). J Agric Food Chem 61:1251612521CrossRefGoogle Scholar
Kohler, EA, Throssell, CS, Reicher, ZJ (2004) 2,4-D rate response, absorption, and translocation of two ground ivy (Glechoma hederacea) populations. Weed Technol 18:917923CrossRefGoogle Scholar
Kruger, GR, Davis, VM, Weller, SC, Johnson, WG (2008) Response and survival of rosette-stage horseweed (Conyza canadensis) after exposure to 2,4-D. Weed Sci 56:748752CrossRefGoogle Scholar
Kruger, GR, Davis, VM, Weller, SC, Johnson, WG (2010) Growth and seed production of horseweed (Conyza canadensis) populations after exposure to postemergence 2,4-D. Weed Sci 58:413419CrossRefGoogle Scholar
Kruger, GR, Davis, VM, Weller, SC, Stachler, JM, Loux, MM, Johnson, WG (2009) Frequency, distribution, and characterization of horseweed (Conyza canadensis) biotypes with resistance to glyphosate and ALS-inhibiting herbicides. Weed Sci 57:652659CrossRefGoogle Scholar
Kubes, M, Yang, H, Richter, GL, Cheng, Y, Młodzińska, E, Wang, X, Blakeslee, JJ, Carraro, N, Petrášek, J, Zažímalová, E, Hoyerová, K, Peer, WA, Murphy, AS (2012) The Arabidopsis concentration-dependent influx/efflux transporter ABCB4 regulates cellular auxin levels in the root epidermis. Plant Journal 69:640654CrossRefGoogle ScholarPubMed
LeClere, S, Wu, C, Westra, P, Sammons, RD (2018) Cross-resistance to dicamba, 2,4-D, and fluroxypyr in Kochia scoparia is endowed by a mutation in an AUX/IAA gene. Proc Natl Acad Sci USA 115:E2911E2920CrossRefGoogle Scholar
Lehoczki, E, Laskay, G, Polos, E, Mikulás, J (1984) Resistance to triazine herbicides in horseweed (Conyza canadensis). Weed Sci 32:669674CrossRefGoogle Scholar
Lespérance, M (2015) Programmed Cell Death and Altered Translocation Cause Glyphosate Resistance in Giant Ragweed (Ambrosia trifida L.). MS dissertation. Guelph, Ontário: University of Guelph. 95 pGoogle Scholar
Mangano, S, Denita-Juarez, SP, Choi, H-S, Marzol, E, Hwang, Y, Ranocha, P, Velasquez, SM, Borassi, C, Barberini, ML, Aptekmann, AA, Muschietti, JP, Nadra, AD, Dunand, C, Cho, H-T, Estevez, JM (2017) Molecular link between auxin and ROS-mediated polar growth. Proc Natl Acad Sci USA 114:52895294CrossRefGoogle ScholarPubMed
McCarthy-Suárez, I (2017) Role of reactive oxygen species in auxin herbicide phytotoxicity: current information and hormonal implications—are gibberellins, cytokinins, and polyamines involved? Botany 95:369385CrossRefGoogle Scholar
Mithila, J, Hall, JC (2005) Comparison of ABP1 over-expressing Arabidopsis and under-expressing tobacco with an auxinic herbicide-resistant wild mustard (Brassica kaber) biotype. Plant Sci 169:2128CrossRefGoogle Scholar
Mithila, J, Hall, JC, Johnson, WG, Kelley, KB, Riechers, DE (2011) Evolution of resistance to auxinic herbicides: historical perspectives, mechanisms of resistance, and implications for broadleaf weed management in agronomic crops. Weed Science 59:445457CrossRefGoogle Scholar
Mockaitis, K, Estelle, M (2008) Auxin receptors and plant development: a new signaling paradigm. Annu Rev Cell Dev Biol 24:5580CrossRefGoogle ScholarPubMed
Moretti, ML, Van Horn, CR, Robertson, R, Segobye, K, Weller, SC, Young, BG, Johnson, WG, Douglas Sammons, R, Wang, D, Ge, X, d’Avignon, A, Gaines, TA, Westra, P, Green, AC, Jeffery, T, et al. (2017) Glyphosate resistance in Ambrosia trifida. Part 2. Rapid response physiology and non-target-site resistance. Pest Manag Sci 74:10791088CrossRefGoogle ScholarPubMed
Morré, DJ, Brightman, AO, Hidalgo, A, Navas, P (1995) Selective inhibition of auxin-stimulated NADH oxidase activity and elongation growth of soybean hypocotyls by thiol reagents. Plant Physiol 107:12851291CrossRefGoogle ScholarPubMed
Pazmiño, DM, Rodríguez-Serrano, M, Sanz, M, Romero-Puertas, MC, Sandalio, LM (2014) Regulation of epinasty induced by 2,4-dichlorophenoxyacetic acid in pea and Arabidopsis plants. Plant Biol 16:809818CrossRefGoogle ScholarPubMed
Pazmiño, DM, Romero-Puertas, MC, Sandalio, LM (2012) Insights into the toxicity mechanism of and cell response to the herbicide 2,4-D in plants. Plant Signal Behav 7:425427CrossRefGoogle ScholarPubMed
Peer, WA, Cheng, Y, Murphy, AS (2013) Evidence of oxidative attenuation of auxin signalling. J Exp Bot 64:26292639CrossRefGoogle ScholarPubMed
Peterson, MA, McMaster, SA, Riechers, DE, Skelton, J, Stahlman, PW (2016) 2,4-D past, present, and future: a review. Weed Technol 30:303345CrossRefGoogle Scholar
Preston, C, Dolman, FC, Boutsalis, P (2013) Multiple resistance to acetohydroxyacid synthase–inhibiting and auxinic herbicides in a population of oriental mustard (Sisymbrium orientale). Weed Sci 61:185192CrossRefGoogle Scholar
Proskuryakov, SY, Konoplyannikov, AG, Gabai, VL (2003) Necrosis: a specific form of programmed cell death? Exp Cell Res 283:116CrossRefGoogle ScholarPubMed
Riar, DS, Burke, IC, Yenish, JP, Bell, J, Gill, K (2011) Inheritance and physiological basis for 2,4-D resistance in prickly lettuce (Lactuca serriola L.). J Agric Food Chem 59:9417–23CrossRefGoogle Scholar
Roden, LC, Ingle, RA (2009) Lights, rhythms, infection: the role of light and the circadian clock in determining the outcome of plant–pathogen interactions. Plant Cell Online 21:25462552CrossRefGoogle ScholarPubMed
Rodríguez-Serrano, M, Pazmiño, DM, Sparkes, I, Rochetti, A, Hawes, C, Romero-Puertas, MC, Sandalio, LM (2014) 2,4-Dichlorophenoxyacetic acid promotes S-nitrosylation and oxidation of actin affecting cytoskeleton and peroxisomal dynamics. J Exp Bot 65:47834793CrossRefGoogle ScholarPubMed
Romero-Puertas, MC, Mccarthy, I, Gómez, M, Sandalio, LM, Corpas, FJ, Del Río, LA, Palma, JM (2004) Reactive oxygen species-mediated enzymatic systems involved in the oxidative action of 2,4-dichlorophenoxyacetic acid. Plant Cell Environ 27:11351148CrossRefGoogle Scholar
Roux, F, Reboud, X (2005) Is the cost of herbicide resistance expressed in the breakdown of the relationships between characters? A case study using synthetic-auxin-resistant Arabidopsis thaliana mutants. Genet Research 85:101110CrossRefGoogle ScholarPubMed
Ruifrok, AC, Johnston, DA (2001) Quantification of histochemical staining by color deconvolution. Anal Quant Cytol Histol 23:291299Google ScholarPubMed
Santos, G, Oliveira, JR RS, Constantin, J., Francischini, AC, Osipe, JB (2014) Multiple resistance of Conyza sumatrensis to chlorimuron-ethyl and glyphosate. Planta Daninha 32:409416CrossRefGoogle Scholar
Schopfer, P, Liszkay, A, Bechtold, M, Frahry, G, Wagner, A (2002) Evidence that hydroxyl radicals mediate auxin-induced extension growth. Planta 214:821828CrossRefGoogle ScholarPubMed
Smith, AE (1989) Degradation, fate, and persistence of phenoxyalkanoic acid herbicides in soil. Rev Weed Sci 4:124Google Scholar
Soares, DJ, Oliveira, WS, López-Ovejero, RF, Christoffoleti, P (2012) Control of glyphosate resistant hairy fleabane (Conyza bonariensis) with dicamba and 2,4-D. Planta Daninha 30:401406CrossRefGoogle Scholar
Song, Y (2014) Insight into the mode of action of 2, 4 -dichlorophenoxyacetic acid (2, 4 -D) as an herbicide. J Int Plant Biol 56:106113CrossRefGoogle ScholarPubMed
Switzer, CM (1957) The existence of 2,4-D-resistant strains of wild carrot. Proceedings of the Northeastern Weed Control Conference 11:315318Google Scholar
Titapiwatanakun, B, Murphy, AS (2009) Post-transcriptional regulation of auxin transport proteins: cellular trafficking, protein phosphorylation, protein maturation, ubiquitination, and membrane composition. J Exp Bot 60:10931107CrossRefGoogle ScholarPubMed
Urbano, JM, Borrego, A, Torres, V, Leon, JM, Jimenez, C, Dinelli, G, Barnes, J (2007) Glyphosate-resistant HAIRY FLEABANE (Conyza Bonariensis) in Spain. Weed Technol 21:396401CrossRefGoogle Scholar
Valenzuela-Valenzuela, JM, Lownds, NK, Sterling, TM (2001) Clopyralid uptake, translocation, metabolism, and ethylene induction in picloram-resistant yellow starthistle (Centaurea solstitialis L.). Pestic Biochem Physiol 71:1119CrossRefGoogle Scholar
VanGessel, MJ (2001) Glyphosate-resistant horseweed from Delaware. Weed Sci 49:703705CrossRefGoogle Scholar
Van Horn, CR, Moretti, ML, Robertson, RR, Segobye, K, Weller, SC, Young, BG, Johnson, WG, Schulz, B, Green, AC, Jeffery, T, Lespérance, MA, Tardif, FJ, Sikkema, PH, Hall, JC, McLean, MD, et al. (2017) Glyphosate resistance in Ambrosia trifida: Part 1. Novel rapid cell death response to glyphosate. Pest Manag Sci 74:10711078CrossRefGoogle ScholarPubMed
Vargas, L, Bianchi, M, Rizzardi, M, Agostinetto, D, Dal Magro, T (2007) Conyza bonariensis biotypes resistant to the glyphosate in southern Brazil. Planta Daninha 25:573578CrossRefGoogle Scholar
Walsh, TA, Neal, R, Merlo, AO, Honma, M, Hicks, GR, Wolff, K, Matsumura, W, Davies, JP (2006) Mutations in an auxin receptor homolog AFB5 and in SGT1b confer resistance to synthetic picolinate auxins and not to 2,4-dichlorophenoxyacetic acid or indole-3-acetic acid in Arabidopsis. Plant Physiol 142:542552CrossRefGoogle ScholarPubMed
Wang, Y, Deshpande, S, Hall, JC (2001) Calcium may mediate auxinic herbicide resistance in wild mustard. Weed Sci 49:27CrossRefGoogle Scholar
Weinberg, T, Stephenson, GR, McLean, MD, Hall, JC (2006) MCPA (4-chloro-2-ethylphenoxyacetate) resistance in hemp-nettle (Galeopsis tetrahit L.). J Agric Food Chem 54:91269134CrossRefGoogle Scholar
Yu, J, Wen, CK (2013) Arabidopsis aux1 rcr1 mutation alters AUXIN RESISTANT1 targeting and prevents expression of the auxin reporter DR5:GUS in the root apex. J Exp Bot 64:921933CrossRefGoogle ScholarPubMed
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