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Prevalence and Mechanism of Atrazine Resistance in Waterhemp (Amaranthus tuberculatus) from Nebraska

  • Amaranatha Reddy Vennapusa (a1), Felipe Faleco (a2), Bruno Vieira (a3), Spencer Samuelson (a3), Greg R. Kruger (a4), Rodrigo Werle (a5) and Mithila Jugulam (a6)...
Abstract

Resistance to atrazine (a photosystem II [PSII] inhibitor) is prevalent in waterhemp [Amaranthus tuberculatus (Moq.) J. D. Sauer] across the U.S. Midwest. Previous research suggests that target-site mutation or rapid metabolism of atrazine mediated by glutathione S-transferase (GST) conjugation confers resistance in A. tuberculatus from Illinois. The distribution and mechanism of resistance to atrazine in A. tuberculatus populations from Nebraska (NE) are unknown. In this research we (1) evaluated the response and frequency of resistance in NE A. tuberculatus to soil-applied PSII (metribuzin and atrazine) and protoporphyrinogen oxidase (sulfentrazone) inhibitors, as well as POST-applied atrazine; and (2) determined the mechanism of atrazine resistance in NE A. tuberculatus. The chloroplastic psbA gene, coding for a D1 protein (the target site of atrazine) was sequenced in 85 plants representing 27 populations of A. tuberculatus. Furthermore, 24 plants selected randomly from four atrazine-resistant (AR) populations were used to determine the metabolism of atrazine via GST conjugation. Results from the soil-applied herbicide evaluation suggest that metribuzin (0.56 kg ai ha−1) and sulfentrazone (0.28 kg ai ha−1) were effective on A. tuberculatus management. PRE and POST screenings against atrazine in the greenhouse indicate that atrazine (1.345 kg ai ha−1) was not effective on 39% and 73% of the A. tuberculatus populations evaluated (total of 109 and 85 populations, respectively), suggesting the prevalence of atrazine resistance in A. tuberculatus in NE. Sequence analysis of the psbA gene found no known point mutations conferring atrazine resistance. However, the AR plants conjugated atrazine via GST activity faster than the known atrazine-susceptible A. tuberculatus. Overall, the outcome of this study demonstrates the predominance of metabolism-based resistance to atrazine in A. tuberculatus from NE, which may predispose this species to evolve resistance to other herbicides. The use of integrated management strategies for A. tuberculatus is crucial for the control of this troublesome species.

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Corresponding author
*Author for correspondence: Mithila Jugulam, Kansas State University, Manhattan, KS 66506. (Email: mithila@ksu.edu)
References
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Anderson, DD, Roeth, FW Martin, AR (1996) Occurrence and control of triazine-resistant common waterhemp (Amaranthus rudis) in field corn (Zea mays). Weed Technol 10:570575
Anderson, DD, Roeth, FW Martin, AR (1998) Discovery of a primisulfuron-resistant shattercane (Sorghum bicolor) biotype. Weed Technol 12:7477
Anderson, MP Gronwald, JW (1991) Atrazine resistance in a velvetleaf (Abutilon theophrasti) biotype due to enhanced glutathione S-transferase activity. Plant Physiol 96:104109
Bernards, ML, Crespo, RJ, Kruger, GR, Gaussoin, R Tranel, PJ (2012) A waterhemp (Amaranthus tuberculatus) population resistant to 2, 4-D. Weed Sci 60:379384
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
Chi, Y, Cheng, Y, Vanitha, J, Kumar, N, Ramamoorthy, R, Ramachandran, S Jiang, SY (2010) Expansion mechanisms and functional divergence of the glutathione S-transferase family in sorghum and other higher plants. DNA Res 18:116
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
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
Dumont, M, Letarte, J Tardif, FJ (2016) Identification of a psbA mutation (valine219 to isoleucine) in Powell amaranth (Amaranthus powellii) conferring resistance to linuron. Weed Sci 64:611
Enayati, AA, Ranson, H Hemingway, J (2005) Insect glutathione transferases and insecticide resistance. Insect Mol Biol 14:38
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
Falk, JS, Shoup, DE, Al-Khatib, K Peterson, DE (2006) Protox-resistant common waterhemp (Amaranthus rudis) response to herbicides applied at different growth stages. Weed Sci 54:793799
Foes, MJ, Tranel, PJ, Wax, LM Stoller, EW (1998) A biotype of common waterhemp (Amaranthus rudis) resistant to triazine and ALS herbicides. Weed Sci 56:514520
Friesen, LS Powles, SB (2007) Physiological and molecular characterization of atrazine resistance in a wild radish (Raphanus raphanistrum) population. Weed Technol 21:910914
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
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
Hager, AG, Wax, LM, Bollero, GA Simmons, FW (2002a) Common waterhemp (Amaranthus rudis Sauer) management with soil-applied herbicides in soybean (Glycine max (L.) Merr.). Crop Protect 21:277283
Hager, AG, Wax, LM, Bollero, GA Stoller, EW (2003) Influence of diphenylether herbicide application rate and timing on common waterhemp (Amaranthus rudis) control in soybean (Glycine max). Weed Technol 17:1420
Hager, AG, Wax, LM, Stoller, EW Bollero, GA (2002b) Common waterhemp (Amaranthus rudis) interference in soybean. Weed Sci 50:607610
Hartzler, RG, Buhler, DD Stoltenberg, DE (1999) Emergence characteristics of four annual weed species. Weed Sci 47:578584
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
Heap, I (2018) The International Survey of Herbicide Resistant Weeds. www.weedscience.org. Accessed: March 25, 2018
Holt, DC, Lay, VJ, Clarke, ED, Dinsmore, A, Jepson, I, Bright, SW Greenland, AJ (1995) Characterization of the safener-induced glutathione S-transferase isoform II from maize. Planta 196:295302
Irzyk, GP Fuerst, EP (1993) Purification and characterization of a glutathione S-transferase from benoxacor-treated maize (Zea mays). Plant Physiol 102:803810
Jachetta, J Radosevich, S (1981) Enhanced degradation of atrazine by corn (Zea mays). Weed Sci 29:3744
Jepson, I, Lay, VJ, Holt, DC, Bright, SW Greenland, AJ (1994) Cloning and characterization of maize herbicide safener-induced cDNAs encoding subunits of glutathione S-transferase isoforms I, II and IV. Plant Mol Biol 26:18551866
Johnson, WG, Kendig, A Null, DE (1996) Waterhemp Management in Missouri. Columbia: University of Missouri Extension Guide G4871. 4 p
Krausz, RF Young, BG (2003) Sulfentrazone enhances weed control of glyphosate in glyphosate-resistant soybean (Glycine max). Weed Technol 17:249255
Kreuz, K, Tommasini, R Martinoia, E (1996) Old enzymes for a new job (herbicide detoxification in plants). Plant Physiol 111:349353
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
LeBaron, HM (2008) Distribution and management of triazine-resistant weeds. Pages 119132 in LeBaron HM, McFarland JE, Burnside OC, eds. The Triazine Herbicides: 50 Years Revolutionizing Agriculture. San Diego, CA: Elsevier
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 mechanisms confer resistance to mesotrione and atrazine in a population of waterhemp. Plant Physiol 163:363377
Masabni, JG Zandstra, BH (1999) A serine-to-threonine mutation in linuron-resistant Portulaca oleracea . Weed Sci 47:393400
Mengistu, LW, Christoffers, MJ Lym, RG (2005) A psbA mutation in Kochia scoparia (L) Schrad from railroad rights‐of‐way with resistance to diuron, tebuthiuron and metribuzin. Pest Manag Sci 61:10351042
Nakka, S, Godar, AS, Thompson, CR, Peterson, DE Jugulam, M (2017) Rapid detoxification via glutathione S‐transferase (GST)‐conjugation confers high level of atrazine resistance in Palmer amaranth (Amaranthus palmeri). Pest Manag Sci 73:22362243
Park, K Mallory-Smith, C (2006a) psbA mutation in Amaranthus retroflexus confers resistance to several PSII-inhibiting herbicides. GenBank accession no. DQ887374
Park, KW Mallory‐Smith, CA (2006b) psbA mutation (Asn266 to Thr) in Senecio vulgaris L. confers resistance to several PS II‐inhibiting herbicides. Pest Manag Sci 62:880885
Patzoldt, WL, Dixon, BS Tranel, PJ (2003) Triazine resistance in Amaranthus tuberculatus (Moq) Sauer that is not site‐of‐action mediated. Pest Manag Sci 59:11341142
Patzoldt, WL, Tranel, PJ Hager, AG (2005) A waterhemp (Amaranthus tuberculatus) biotype with multiple resistance across three herbicide sites of action. Weed Sci 53:3036
Pratt, DB Clark, LG (2001) Amaranthus rudis and A. tuberculatus, one species or two? J Torrey Bot Soc 128:282296
Preston, C Stewart, C (2009) Herbicide resistance: target site mutations. Genomics of Weedy and Invasive Plants. Ames, IA: Blackwell Scientific. Pp 127148
Riechers, DE, Fuerst, EP Miller, KD (1996) Initial metabolism of dimethenamid in safened and unsafened wheat shoots. J Agric Food Chem 44:15581564
Riechers, DE, Kreuz, K Zhang, Q (2010) Detoxification without intoxication: herbicide safeners activate plant defense gene expression. Plant Physiol 153:313
Riveron, JM, Yunta, C, Ibrahim, SS, Djouaka, R, Irving, H, Menze, BD, Ismail, HM, Hemingway, J, Ranson, H Albert, A (2014) A single mutation in the GSTe2 gene allows tracking of metabolically based insecticide resistance in a major malaria vector. Genome Bio 15:R27
Sarangi, D Jhala, AJ (2017) Biologically effective rates of a new premix (atrazine, bicyclopyrone, mesotrione, and S-metolachlor) for preemergence or postemergence control of common waterhemp [Amaranthus tuberculatus (Moq.) Sauer var. rudis] in corn. Can J Plant Sci 97:10751089
Sarangi, D, Tyre, AJ, Patterson, EL, Gaines, TA, Irmak, S, Knezevic, SZ, Lindquist, JL Jhala, AJ (2017) Pollen-mediated gene flow from glyphosate-resistant common waterhemp (Amaranthus rudis Sauer): consequences for the dispersal of resistance genes. Sci Rep 7:44913
Schultz, JL, Chatham, LA, Riggins, CW, Tranel, PJ Bradley, KW (2015) Distribution of herbicide resistances and molecular mechanisms conferring resistance in Missouri waterhemp (Amaranthus rudis Sauer) populations. Weed Sci 63:336345
Steckel, LE (2007) The dioecious Amaranthus spp.: here to stay. Weed Technol 21:567570
Steckel, LE Sprague, CL (2004) Common waterhemp (Amaranthus rudis) interference in corn. Weed Sci 52:359364
Thiel, H Varrelmann, M (2014) Identification of a new PSII target site psbA mutation leading to D1 amino acid leu218val exchange in the Chenopodium album D1 protein and comparison to cross‐resistance profiles of known modifications at positions 251 and 264. Pest Manag Sci 70:278285
Timmerman, KP (1989) Molecular characterization of corn glutathione S‐transferase isozymes involved in herbicide detoxication. Physiol Plant 77:465471
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
Vieira, BC, Samuelson, SL, Alves, GS, Gaines, TA, Werle, R Kruger, GR (2017) Distribution of glyphosate‐resistant Amaranthus spp. in Nebraska. Pest Manag Sci, doi:10.1002/ps.4781
Vyn, J, Swanton, C, Weaver, S Sikkema, P (2007) Control of herbicide-resistant common waterhemp (Amaranthus tuberculatus var. rudis) with pre-and post-emergence herbicides in soybean. Can J Plant Sci 87:175182
Waselkov, KE Olsen, KM (2014) Population genetics and origin of the native North American agricultural weed waterhemp (Amaranthus tuberculatus; Amaranthaceae). Am J Bot 101:17261736
Werle, R, Jhala, A, Yerka, MK, Dille, JA Lindquist, JL (2016) Distribution of herbicide-resistant shattercane and johnsongrass populations in sorghum production areas of Nebraska and northern Kansas. Agron J 108:321328
Werle, R, Sandell, LD, Buhler, DD, Hartzler, RG Lindquist, JL (2014) Predicting emergence of 23 summer annual weed species. Weed Sci 62:267279
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