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Evolution of target and non-target based multiple herbicide resistance in a single Palmer amaranth (Amaranthus palmeri) population from Kansas

Published online by Cambridge University Press:  29 June 2020

Sushila Chaudhari
Affiliation:
Assistant Professor, Department of Horticulture, Michigan State University, East Lansing, MI, USA
Vijay K. Varanasi
Affiliation:
Senior Biologist, Bayer Crop Science, Chesterfield, MO, USA
Sridevi Nakka
Affiliation:
Scientist, Heartland Plant Innovations, Manhattan, KS, USA
Prasanta C. Bhowmik
Affiliation:
Professor, Weed Science, Stockbridge School of Agriculture, University of Massachusetts, Amherst, MA, USA
Curtis R. Thompson
Affiliation:
Extension Specialist and Professor Emeritus, Department of Agronomy, Kansas State University, Manhattan, KS, USA
Dallas E. Peterson
Affiliation:
Professor, Department of Agronomy, Kansas State University, Manhattan, KS, USA
Randall S. Currie
Affiliation:
Associate Professor, Kansas State University, Southwest Research–Extension Center, Garden City, KS, USA
Mithila Jugulam*
Affiliation:
Associate Professor and Weed Scientist, Department of Agronomy, Kansas State University, Manhattan, KS, USA
*
Author for correspondence: Mithila Jugulam, Department of Agronomy, 2004 Throckmorton PSC, 1712 Claflin Road, Kansas State University, Manhattan, KS66506-0110. Email: [email protected]

Abstract

The evolution of resistance to multiple herbicides in Palmer amaranth is a major challenge for its management. In this study, a Palmer amaranth population from Hutchinson, Kansas (HMR), was characterized for resistance to inhibitors of photosystem II (PSII) (e.g., atrazine), acetolactate synthase (ALS) (e.g., chlorsulfuron), and EPSP synthase (EPSPS) (e.g., glyphosate), and this resistance was investigated. About 100 HMR plants were treated with field-recommended doses (1×) of atrazine, chlorsulfuron, and glyphosate, separately along with Hutchinson multiple-herbicide (atrazine, chlorsulfuron, and glyphosate)–susceptible (HMS) Palmer amaranth as control. The mechanism of resistance to these herbicides was investigated by sequencing or amplifying the psbA, ALS, and EPSPS genes, the molecular targets of atrazine, chlorsulfuron, and glyphosate, respectively. Fifty-two percent of plants survived a 1× (2,240 g ai ha−1) atrazine application with no known psbA gene mutation, indicating the predominance of a non–target site resistance mechanism to this herbicide. Forty-two percent of plants survived a 1× (18 g ai ha−1) dose of chlorsulfuron with proline197serine, proline197threonine, proline197alanine, and proline197asparagine, or tryptophan574leucine mutations in the ALS gene. About 40% of the plants survived a 1× (840 g ae ha−1) dose of glyphosate with no known mutations in the EPSPS gene. Quantitative PCR results revealed increased EPSPS copy number (50 to 140) as the mechanism of glyphosate resistance in the survivors. The most important finding of this study was the evolution of resistance to at least two sites of action (SOAs) (~50% of plants) and to all three herbicides due to target site as well as non–target site mechanisms. The high incidence of individual plants with resistance to multiple SOAs poses a challenge for effective management of this weed.

Type
Symposium
Copyright
© Weed Science Society of America, 2020

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References

Bandeen, J, McLaren, R (1976) Resistance of Chenopodium album to triazine herbicides. Can J Plant Sci 56:411412CrossRefGoogle Scholar
Chatham, LA, Wu, C, Riggins, CW, Hager, AG, Young, BG, Roskamp, GK, Tranel, PJ (2015) EPSPS gene amplification is present in the majority of glyphosate-resistant Illinois waterhemp (Amaranthus tuberculatus) populations. Weed Technol 29:485510.1614/WT-D-14-00064.1CrossRefGoogle Scholar
Corpet, F (1988) Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res 16:108811089010.1093/nar/16.22.10881CrossRefGoogle ScholarPubMed
Devine, MD, Eberlein, CV (1997) Physiological, biochemical and molecular aspects of herbicide resistance based on altered target sites. Pages 159185in Roe, RM, Burton, JD, Kuhr, RJ, eds, Herbicide Activity: Toxicology, Biochemistry and Molecular Biology. Amsterdam: IOS PressGoogle Scholar
Dillon, AJ, Varanasi, VK, Danilova, T, Koo, D-H, Nakka, S, Peterson, D, Tranel, P, Friebe, B, Gill, BS, Jugulam, M (2017) Physical mapping of amplified 5-enolpyruvylshikimate-3-phosphate synthase gene copies in glyphosate-resistant Amaranthus tuberculatus. Plant Physiol 173:1226123410.1104/pp.16.01427CrossRefGoogle ScholarPubMed
Friesen, LS, Powles, SB (2007) Physiological and molecular characterization of atrazine resistance in a wild radish (Raphanus raphanistrum) population. Weed Technol 21:91091410.1614/WT-07-008.1CrossRefGoogle Scholar
Gaines, TA, Zhang, W, Wang, D, Bukun, B, Chisholm, ST, Shaner, DL, Nissen, SJ, Patzoldt, WL, Tranel, PJ, Culpepper, AS, Grey, TL (2010) Gene amplification confers glyphosate resistance in Amaranthus palmeri. PNAS 107:1029103410.1073/pnas.0906649107CrossRefGoogle ScholarPubMed
Godar, AS, Varanasi, VK, Nakka, S, Prasad, PV, Thompson, CR, Mithila, J (2015) Physiological and molecular mechanisms of differential sensitivity of Palmer amaranth (Amaranthus palmeri) to mesotrione at varying growth temperatures. PloS one 10(5):e0126731CrossRefGoogle ScholarPubMed
Heap, I (2019) International Survey of Herbicide Resistant Weeds. http://www.weedscience.org. Accessed: May 29, 2019Google Scholar
Hess, FD (2000) Light-dependent herbicides: an overview. Weed Sci 48:16017010.1614/0043-1745(2000)048[0160:LDHAO]2.0.CO;2CrossRefGoogle Scholar
Horak, MJ, Peterson, DE (1995) Biotypes of Palmer amaranth (Amaranthus palmeri) and common waterhemp (Amaranthus rudis) are resistant to imazethapyr and thifensulfuron. Weed Technol 19219510.1017/S0890037X00023174CrossRefGoogle Scholar
Jachetta, J, Radosevich, S (1981) Enhanced degradation of atrazine by corn (Zea mays). Weed Sci 29:374410.1017/S0043174500025807CrossRefGoogle Scholar
Jugulam, M, Gill, BS (2017) Molecular cytogenetics to unravel mechanisms of gene duplication in pesticide resistance. Pest Manag Sci 74:222910.1002/ps.4665CrossRefGoogle Scholar
Kaundun, SS, Zelaya, IA, Dale, RP, Lycett, AJ, Carter, P, Sharples, KR, McIndoe, E (2008) Importance of the P106S target-site mutation in conferring resistance to glyphosate in a goosegrass (Eleusine indica) population from the Philippines. Weed Sci 56:637646CrossRefGoogle Scholar
Keeley, PE, Carter, CH, Thullen, RJ (1987) Influence of planting date on growth of Palmer amaranth. Weed Sci 35:19920410.1017/S0043174500079054CrossRefGoogle Scholar
Koger, CH, Reddy, KN (2005) Role of absorption and translocation in the mechanism of glyphosate resistance in horseweed (Conyza canadensis). Weed Sci 53:848910.1614/WS-04-102RCrossRefGoogle Scholar
Koo, DH, Molin, WT, Saski, CA, Jiang, J, Putta, K, Jugulam, M, Friebe, B, Gill, BS (2018) Extra-chromosomal circular DNA (eccDNA) based amplification and transmission of herbicide resistance in crop weed Amaranthus palmeri. PNAS 115:3332333710.1073/pnas.1719354115CrossRefGoogle Scholar
Krysiak, M, Gawroński, SW, Adamczewski, K, Kierzek, R (2011) ALS gene mutations in Apera spica-venti confer broad-range resistance to herbicides. J Plant Prot Res 51:26126710.2478/v10045-011-0043-7CrossRefGoogle Scholar
Lamego, FP, Charlson, D, Delatorre, CA, Burgos, NR, Vidal, RA (2009) Molecular basis of resistance to ALS-inhibitor herbicides in greater beggarticks. Weed Sci 57:47448110.1614/WS-09-056.1CrossRefGoogle Scholar
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 163:36337710.1104/pp.113.223156CrossRefGoogle Scholar
Malone, JM, Morran, S, Shirley, N, Boutsalis, P, Preston, C (2016) EPSPS gene amplification in glyphosate-resistant Bromus diandrus. Pest Manage Sci 72:818810.1002/ps.4019CrossRefGoogle ScholarPubMed
Nakka, S, Godar, AS, Thompson, CR, Peterson, DE, Jugulam, M (2017a) Rapid detoxification via glutathione-S-transferase (GST) conjugation confers a high level of atrazine resistance in Palmer amaranth (Amaranthus palmeri). Pest Manag Sci 73:22362243CrossRefGoogle Scholar
Nakka, S, Thompson, CR, Peterson, DE, Jugulam, M (2017b) Target-site and non-target-site based resistance to ALS-inhibitors in Palmer amaranth (Amaranthus palmeri). Weed Sci 65:68168910.1017/wsc.2017.43CrossRefGoogle Scholar
Nandula, VK, Ray, JD, Ribeiro, DN, Pan, Z, Reddy, KN (2013) Glyphosate resistance in tall waterhemp (Amaranthus tuberculatus) from Mississippi is due to both altered target-site and nontarget-site mechanisms. Weed Sci 61:37438310.1614/WS-D-12-00155.1CrossRefGoogle Scholar
Park, KW, Kolkman, JM, Mallory-Smith, CA (2012) Point mutation in acetolactate synthase confers sulfonylurea and imidazolinone herbicide resistance in spiny annual sow-thistle [Sonchus asper (L.) Hill]. Can J Plant Sci 92:30330910.4141/cjps2011-159CrossRefGoogle Scholar
Park, KW, Mallory-Smith, CA (2004) Physiological and molecular basis for ALS inhibitor resistance in Bromous tectorum biotypes. Weed Res 44:717710.1111/j.1365-3180.2003.00374.xCrossRefGoogle Scholar
Patzoldt, WL, Tranel, PJ (2007) Multiple ALS mutations confer herbicide resistance in waterhemp (Amaranthus tuberculatus). Weed Sci 55:421428CrossRefGoogle Scholar
Powles, SB, Yu, Q (2010) Evolution in action: plants resistant to herbicides. Annu Rev Plant Biol 61:31734710.1146/annurev-arplant-042809-112119CrossRefGoogle ScholarPubMed
Ryan, G (1970) Resistance of common groundsel to simazine and atrazine. Weed Sci 18:61461610.1017/S0043174500034330CrossRefGoogle Scholar
Salas, RA, Dayan, FE, Pan, Z, Watson, SB, Dickson, JW, Scott, RC, Burgos, NR (2012) EPSPS gene amplification in glyphosate-resistant Italian ryegrass (Lolium perenne ssp. multiflorum) from Arkansas. Pest Manage Sci 68:1223123010.1002/ps.3342CrossRefGoogle ScholarPubMed
Salas, RA, Scott, RC, Dayan, FE, Burgos, NR (2015) EPSPS gene amplification in glyphosate-resistant Italian ryegrass (Lolium perenne ssp. multiflorum) populations from Arkansas (United States). J Agricultural Food Chem 63:5885589310.1021/acs.jafc.5b00018CrossRefGoogle Scholar
Sammons, RD, Gaines, TA (2014) Glyphosate resistance: state of knowledge. Pest Manage Sci 70:13671377CrossRefGoogle ScholarPubMed
Sauer, JD (1972) The dioecious amaranths: a new species name and major range extensions. Madroño 21:426434Google Scholar
Schönbrunn, E, Eschenburg, S, Shuttleworth, WA, Schloss, JV, Amrhein, N, Evans, JN, Kabsch, W (2001) Interaction of the herbicide glyphosate with its target enzyme 5-enolpyruvylshikimate 3-phosphate synthase in atomic detail. PNAS USA 98:1376138010.1073/pnas.98.4.1376CrossRefGoogle ScholarPubMed
Sosnoskie, LM, Kichler, JM, Wallace, RD, Culpepper, AS (2011) Multiple resistance in Palmer amaranth to glyphosate and pyrithiobac confirmed in Georgia. Weed Sci 59:32132510.1614/WS-D-10-00132.1CrossRefGoogle Scholar
Spaunhorst, DJ, Nie, H, Todd, JR, Young, JM, Young, BG, Johnson, WG (2019) Confirmation of herbicide resistance mutations Trp574Leu, ΔG210, and EPSPS gene amplification and control of multiple herbicide-resistant Palmer amaranth (Amaranthus palmeri) with chlorimuron-ethyl, fomesafen, and glyphosate. PLoS ONE 14 (3):e021445810.1371/journal.pone.0214458CrossRefGoogle ScholarPubMed
Steckel, E (2007) The dioecious Amaranthus spp.: here to stay. Weed Technol 21:56757010.1614/WT-06-045.1CrossRefGoogle Scholar
Tal, A, Rubin, B (2004) Occurrence of resistant Chrysanthemum coronarium to ALS inhibiting herbicides in Israel. Resist Pest Manage Newsl 13:3133Google Scholar
Timmerman, KP (1989) Molecular characterization of corn glutathione S-transferase isozymes involved in herbicide detoxication. Physiol Plant 77: 46547110.1111/j.1399-3054.1989.tb05668.xCrossRefGoogle Scholar
Tranel, PJ, Wright, TR (2002) Resistance of weeds to ALS-inhibiting herbicides: what have we learned? Weed Sci 50:70071210.1614/0043-1745(2002)050[0700:RROWTA]2.0.CO;2CrossRefGoogle Scholar
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 71:12071212CrossRefGoogle Scholar
Vennapusa, AR, Faleco, F, Vieira, B, Samuelson, S, Kruger, GR, Werle, R, Jugulam, M (2018) Prevalence and mechanism of atrazine resistance in common waterhemp from Nebraska. Weed Sci 66:595602CrossRefGoogle Scholar
Whaley, CM, Wilson, HP, Westwood, JH (2006) ALS resistance in several smooth pigweed (Amaranthus hybridus) biotypes. Weed Sci 54:828832CrossRefGoogle Scholar
Whaley, CM, Wilson, HP, Westwood, JH (2007) A new mutation in plant ALS confers resistance to five classes of ALS-inhibiting herbicides. Weed Sci 55:839010.1614/WS-06-082.1CrossRefGoogle Scholar
Wiersma, AT, Gaines, TA, Preston, C, Hamilton, JP, Giacomini, D, Buell, CR, Leach, JE, Westra, P (2015) Gene amplification of 5-enol-pyruvylshikimate-3-phosphate synthase in glyphosate-resistant Kochia scoparia. Planta 241:463474CrossRefGoogle ScholarPubMed
Yu, Q, Powles, SB (2014) Resistance to AHAS inhibitor herbicides: current understanding. Pest Manag Sci 70:1340–130CrossRefGoogle ScholarPubMed
Yu, Q, Jalaludin, A, Han, H, Chen, M, Sammons, RD, Powles, SB (2015) Evolution of a double amino acid substitution in the 5-enolpyruvylshikimate-3-phosphate synthase in Eleusine indica conferring high-level glyphosate resistance. Plant Physiol 167:1440144710.1104/pp.15.00146CrossRefGoogle ScholarPubMed
Yuan, JS, Tranel, PJ, Stewart, CN (2007) Non-target-site herbicide resistance: a family business. Trends Plant Sci 12:613CrossRefGoogle ScholarPubMed