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Nontarget site resistance in Palmer amaranth [Amaranthus palmeri (S.) Wats.] confers cross-resistance to protoporphyrinogen oxidase-inhibiting herbicides

  • Vijay K. Varanasi (a1), Chad Brabham (a1), Nicholas E. Korres (a1) and Jason K. Norsworthy (a2)


Palmer amaranth is one of the most problematic weeds in cropping systems of North America, especially in midsouthern United States, because of its competitive ability and propensity to evolve resistance to several herbicide sites of action. Previously, we confirmed and characterized the first case of nontarget site resistance (NTSR) to fomesafen in a Palmer amaranth accession from Randolph County, AR (RCA). The primary basis of the present study was to evaluate the cross- and multiple-resistance profile of the RCA accession. The fomesafen dose-response assay in the presence of malathion revealed a lower level of RCA resistance when compared with fomesafen alone. The resistance index of the RCA accession, based on 50% biomass reduction, ranged from 63-fold (fomesafen alone) to 22-fold (malathion plus fomesafen), when compared with a 2007 susceptible, and 476-fold and 167-fold, respectively, relative to a 1986 susceptible check. The RCA accession was resistant to other protoporphyrinogen oxidase (PPO) inhibitors (i.e., flumioxazin, acifluorfen, saflufenacil) as well as the 4-hydroxyphenylpyruvate dioxygenase (HPPD) inhibitor tembotrione and acetolactate synthase (ALS) inhibitor pyrithiobac sodium. Sequencing of the ALS gene revealed no point mutations, indicating that a target-site mechanism is not involved in conferring ALS-inhibitor resistance in the RCA accession. Of the three PPO-inhibiting herbicides tested in combination with the malathion, saflufenacil resulted in the greatest biomass reduction (80%; P < 0.05) and lowest survival rate (23%; P < 0.05) relative to nontreated plants. The application of cytochrome P450 or glutathione S-transferase inhibitors with fomesafen did not lead to any adverse effects on soybean, suggesting a possible role for these compounds for management of NTSR under field conditions. These results shed light on the relative unpredictability of NTSR in conferring herbicide cross- and multiple resistance in Palmer amaranth.


Corresponding author

Author for correspondence: Vijay K. Varanasi, Altheimer Laboratory, 1366 West Altheimer Dr., Fayetteville, AR 72704 Email:


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Corpet, F (1988) Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res 16:1088110890
Cummins, I, Wortley, DJ, Sabbadin, F, He, Z, Coxon, CR, Straker, HE, Sellars, JD, Knight, K, Edwards, L, Hughes, D, Kaundun, SS, Hutching, SJ, Steel, PG, Edwards, R (2013) Key role for a glutathione transferase in multiple-herbicide resistance in grass weeds. Proc Natl Acad Sci U S A 110:58125817
Dayan, FE, Daga, PR, Duke, SO, Lee, RM, Tranel, PJ, Doerksen, RJ (2010) Biochemical and structural consequences of a glucine deletion in the α-8 helix of protoporphyrinogen oxidase. Biochim Biophys Acta 1804:15481556
Délye, C, 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 51:433437
Délye, C, Jasieniuk, M, Le Corre, V (2013) Deciphering the evolution of herbicide resistance in weeds. Trends Genet 29:649658
Doyle, JJ, Doyle, JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:1115
Gaines, TA, Zhang, WL, Wang, D, Bukun, B, Chisholm, ST, Shaner, DL, Nissen, SJ, Patzoldt, WL, Tranel, PJ, Culpepper, AS, Grey, TL, Webster, TM, Vencill, WK, Sammons, RD, Jiang, JM, Preston, C, Leach, JE, Westra, P (2010) Gene amplification confers glyphosate resistance in Amaranthus palmeri. Proc Natl Acad Sci U S A 107:10291034
Giacomini, DA, Umphres-Lopez, AM, Nie, H, Mueller, TC, Steckel, LE, Young, BG, Tranel, PJ (2017) Two new PPX2 mutations associated with resistance to PPO-inhibitor herbicides in Amaranthus palmeri. Pest Manag Sci 73:15591563
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
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
Heap, I (2018) The International Survey of Herbicide Resistant Weeds. Accessed: July 10, 2018
Kaundun, SS, Hutchings, S-J, Dale, RP, Howell, A, Morris, JA, Kramer, VC, Shivrain, VK, Mcindoe, E (2017) Mechanisms of resistance to mesotrione in an Amaranthus tuberculatus population from Nebraska, USA. PLoS One 12:e0180095
Korres, NE, Norsworthy, JK (2017) Palmer amaranth (Amaranthus palmeri) demographic and biological characteristics in wide-row soybean. Weed Sci 65:491503
Lee, RM, Hager, AG, Tranel, PJ (2008) Prevalence of a novel resistance mechanism to PPO-inhibiting herbicides in waterhemp (Amaranthus tuberculatus). Weed Sci 56:371375
Ma, R, Evans, AF, Riechers, DE (2016) Differential responses to preemergence and postemergence atrazine in two atrazine-resistant waterhemp populations. Agron J 108:11961202
Ma, R, Kaundun, SS, Tranel, PJ, Riggins, CW, McGinness, DL, Hager, AG, Hawkes, T, McIndoe, E, Riechers, DE (2013) Distinct detoxification mechanism confer resistance to mesotrione and atrazine in a population of waterhemp. Plant Physiol 163:363377
Nakka, S, Godar, AS, Thompson, CR, Peterson, DE, Jugulam, M (2017) Rapid detoxification via glutathione S-transferase (GST) conjugation confers a high level of atrazine resistance in Palmer amaranth (Amaranthus palmeri). Pest Manag Sci 73:22362243
Norsworthy, JK (2014) Repeated sublethal rates of glyphosate lead to decreased sensitivity in Palmer amaranth. Crop Manag 11:1
Obenland, OA, Ma, R, O’Brien, S, Lygin, AV, Riechers, DE (2017) Resistance to carfentrazone-ethyl in tall waterhemp. Pages 3031 in Proceedings of the 72nd Annual Meeting of the North Central Weed Science Society. St. Louis, MO: North Central Weed Science Society of America
Oliveira, MC, Gaines, TA, Dayan, FE, Patterson, EL, Jhala, AJ, Knezevic, SZ (2018) Reversing resistance to tembotrione in an Amaranthus tuberculatus (var. rudis) population from Nebraska, USA with cytochrome P450 inhibitors. Pest Manag Sci 74(10):22962305
Owczarzy, R, Tataurov, AV, Wu, Y, Manthey, JA, McQuisten, KA, Almabrazi, HG, Pedersen, KF, Lin, Y, Garretson, J, McEntaggart, NO, Sailor, CA, Dawson, RB, Peek, AS (2008) IDT SciTools: a suite for analysis and design of nucleic acid oligomers. Nucleic Acids Res 36:W163169
Owen, MDK, Zelaya, IA (2005) Herbicide-resistant crops and weed resistance to herbicides. Pest Manag Sci 61:301311
Pan, G, Si, P, Yu, Q, Tu, J, Powles, S (2012) Non-target site mechanism of metribuzin tolerance in induced tolerant mutants of narrow-leafed lupin (Lupinus angustifolius L.). Crop Pasture Sci 63:452458
Patzoldt, WL, Hager, AG, McCormick, JS, Tranel, PJ (2006) A codon deletion confers resistance to herbicides inhibiting protoporphyrinogen oxidase. Proc Natl Acad Sci U S A 103:1232912334
Petit, C, Duhieu, B, Boucansaud, K, Délye, C (2010) Complex genetic control of non-target-site-based resistance to herbicides inhibiting acetyl-coenzyme A carboxylase and acetolactate-synthase in Alopecurus myosuroides Huds. Plant Sci 178: 501509
Powles, SB, Yu, Q (2010) Evolution in action: plants resistant to herbicides. Annu Rev Plant Biol 61:317347
Preston, C, Wakelin, AM (2008) Resistance to glyphosate from altered herbicide translocation patterns. Pest Manag Sci 64:372376
R Development Core Team (2018) A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Accessed: July 4, 2018
Rangani, G, Salas, R, Aponte, RA, Landes, A, Roma-Burgos, N (2018) A novel amino acid substitution (Gly399Ala) in protoporphyrinogen oxidase 2 confers broad spectrum PPO-inhibitor resistance in Amaranthus palmeri. in Proceedings of the 58th Annual Meeting of the Weed Science Society of America, Arlington, VA: Weed Science Society of America
Rousonelos, SL, Lee, RM, Moreira, MS, VanGessel, MJ, Tranel, PJ (2012) Characterization of a common ragweed (Ambrosia artemisiifolia) population resistant to ALS- and PPO-inhibiting herbicides. Weed Sci 60:335344
Salas, RA, Burgos, NR, Tranel, PJ, Singh, S, Glasgow, L, Scott, RC, Nichols, RL (2016) Resistance to PPO-inhibiting herbicide in Palmer amaranth from Arkansas. Pest Manag Sci 72:864869
Seefeldt, SS, Jensen, JE, Fuerst, EP (1995) Log-logistic analysis of herbicide dose-response relationships. Weed Technol 9:218227
Singh, S, Burgos, N, Singh, V, Alcober, AL, Salas-Perez, R, Shivrain, V (2018) Differential response of Arkansas Palmer amaranth (Amaranthus palmeri) to glyphosate and mesotrione. Weed Technol 34:17
Tehranchian, P, Norsworthy, JK, Powles, S, Bararpour, MT, Bagavathiannan, MV, Barber, T, Scott, RC (2017) Recurrent sublethal-dose selection for reduced susceptibility of Palmer amaranth (Amaranthus palmeri) to dicamba. Weed Sci 65:206212
Tranel, PJ, Wright, TR (2002) Resistance of weeds to ALS-inhibiting herbicides: what have we learned? Weed Sci 50:700712
Van Wychen, L (2016) 2016 Survey of the most common and troublesome weeds in broadleaf crops, fruits and vegetables in the United States and Canada. Weed Science Society of America National Weed Survey Dataset. Accessed: August 10, 2017
Varanasi, VK, Brabham, C, Norsworthy, JK, Nie, H, Young, BG, Houston, M, Barber, T, Scott, RC (2018a) A statewide survey of PPO-inhibitor resistance and the prevalent target-site mechanism in Palmer amaranth (Amaranthus palmeri) accessions from Arkansas. Weed Sci 66:149158
Varanasi, VK, Brabham, C, Norsworthy, JK (2018b) Confirmation and characterization of non-target site resistance to fomesafen in Palmer amaranth (Amaranthus palmeri). Weed Sci 66:702709
Varanasi, VK, Brabham, C, Bagavathiannan, M, Norsworthy, JK (2018c) Repeated low-dose selection results in reduced susceptibility of Palmer amaranth to mesotrione. In Proceedings of the 58th Annual Meeting of the Weed Science Society of America, Arlington, VA: Weed Science Society of America
Vencill, WK, Nichols, RL, Webster, TN, Soteres, JK, Mallory-Smith, C, Burgos, NR, Johnson, WG, McClelland, MR (2012) Herbicide resistance: toward an understanding of resistance development and the impact of herbicide-resistant crops. Weed Sci 60:230
Yuan, JS, Tranel, PJ, Stewart, CN Jr (2007) Non-target-site herbicide resistance: a family business. Trends Plant Sci 12:613
Yu, Q, Powles, SB (2014) Resistance to AHAS inhibitor herbicides: current understanding. Pest Manag Sci 70:13401350
Yu, Q, Abdallah, I, Han, H, Owen, M, Powles, S (2009) Distinct non-target site mechanisms endow resistance to glyphosate, ACCase and ALS-inhibiting herbicides in multiple herbicide-resistant Lolium rigidum. Planta 230:713723



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