Hostname: page-component-745bb68f8f-v2bm5 Total loading time: 0 Render date: 2025-01-11T06:58:01.392Z Has data issue: false hasContentIssue false
  • English
  • Français

Association between metabolic resistances to atrazine and mesotrione in a multiple-resistant waterhemp (Amaranthus tuberculatus) population

Published online by Cambridge University Press:  28 April 2020

Kip E Jacobs Jr ,
Carrie J. Butts-Wilmsmeyer ,
Rong Ma ,
Sarah R. O’Brien  and
Dean E. Riechers Open the ORCID record for Dean E. Riechers [Opens in a new window]
Kip E Jacobs Jr
Affiliation:
Graduate Research Assistant, Department of Crop Sciences, University of Illinois, Urbana, IL, USA
Carrie J. Butts-Wilmsmeyer
Affiliation:
Research Assistant Professor, Department of Crop Sciences, University of Illinois, Urbana, IL, USA; current: Associate Professor, Department of Biological Sciences, Southern Illinois University at Edwardsville, Edwardsville, IL, USA
Rong Ma
Affiliation:
Postdoctoral Research Associate, Department of Crop Sciences, University of Illinois, Urbana, IL, USA; current: Agrochemical Discovery Lead, Bayer U.S.–Crop Science, Chesterfield, MO, USA
Sarah R. O’Brien
Affiliation:
Graduate Research Assistant, Department of Crop Sciences, University of Illinois, Urbana, IL, USA
Dean E. Riechers*
Affiliation:
Professor, Department of Crop Sciences, University of Illinois, Urbana, IL, USA
*
Author for correspondence: Dean E. Riechers, Department of Crop Sciences, University of Illinois, 1102 S. Goodwin Avenue, Urbana, IL61801. Email: riechers@illinois.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Metabolic resistances to atrazine (atz-R) and mesotrione (meso-R) occur in several waterhemp [Amaranthus tuberculatus (Moq.) Sauer] populations in the United States. Interestingly, although metabolic atz-R but mesotrione-sensitive A. tuberculatus populations have been reported, an Amaranthus population has not been confirmed as meso-R but atrazine-sensitive, implying an association between these traits. Experiments were designed to investigate whether the single gene conferring metabolic atz-R plays a role in meso-R. An F2 population was generated from a multiple herbicide–resistant A. tuberculatus population from McLean County, IL (MCR). A cross was made between a known meso-R male clone (MCR-6) and a herbicide-sensitive female clone from Wayne County, IL (WCS-2) to develop an F1 population. Survival of MCR-6 plants following atrazine POST treatment (14.4 kg ha−1) indicated the male parent was homozygous atz-R. F1 plants were intermated to obtain a segregating pseudo-F2 population. Dose–response and metabolic studies conducted with mesotrione using F1 plants indicated intermediate biomass reductions and metabolic rates compared with MCR-6 and WCS. F2 plants were initially treated with either mesotrione (260 g ha−1) or atrazine (2 kg ha−1) POST, and after 21 d of recovery, vegetative clones from surviving resistant plants were subsequently treated with the other herbicide. When mesotrione was applied first, the meso-R frequency was 8.2%, and when atrazine was applied first, the atz-R frequency was 75%. However, the meso-R frequency increased to 16.5% following preselection for atz-R, and 100% of surviving meso-R plants were atz-R. Our findings indicate that the gene conferring metabolic atz-R is also involved with the meso-R trait within the population tested.

Keywords

4-hydroxyphenylpyruvate dioxygenasecytochrome P450detoxificationglutathione S-transferaseoxidative metabolismweed resistancesymmetrical triazines
Type
Research Article
Information
Weed Science , Volume 68 , Issue 4 , July 2020 , pp. 358 - 366
Copyright
© Weed Science Society of America, 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

Associate Editor: Ian Burke, Washington State University

References

Abendroth, JA, Martin, AR, Roeth, FW (2006) Plant response to combinations of mesotrione and photosystem II inhibitors. Weed Technol 20:267–274CrossRefGoogle Scholar
Beaudegnies, R, Edmunds, AJF, Fraser, TEM, Hall, RG, Hawkes, TR, Mitchell, G, Schaetzer, J, Wendeborn, S, Wibley, J (2009) Herbicidal 4-hydroxyphenylpyruvate dioxygenase inhibitor—a review of triketone chemistry story from a Syngenta perspective. Bioorg Med Chem 17:4134–4152CrossRefGoogle Scholar
Beckie, H, Tardif, FJ (2012) Herbicide cross resistance in weeds. Crop Prot 35:15–28CrossRefGoogle Scholar
Bell, MS, Hager, AG, Tranel, PJ (2013) Multiple resistance to herbicides from four site-of-action groups in waterhemp (Amaranthus tuberculatus). Weed Sci 61:460–468CrossRefGoogle Scholar
Bernardo, R, ed (2010) Breeding for Quantitative Traits in Plants. 2nd ed. Woodbury, MN: Stemma Press. 390 pGoogle Scholar
Buhler, DD, Hartzler, RG (2001) Emergence and persistence of seed of velvetleaf, common waterhemp, woolly cupgrass, and giant foxtail. Weed Sci 49:230–235CrossRefGoogle Scholar
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 18:285–292CrossRefGoogle ScholarPubMed
Cummins, I, Dixon, DP, Freitag-Pohl, S, Skipsey, M, Edwards, R (2011) Multiple roles for plant glutathione transferases in xenobiotic detoxification. Drug Metab Rev 43:266–280CrossRefGoogle ScholarPubMed
Cummins, I, Wortley, DJ, Sabbadin, F, He, Z, Coxon, CR, Straker, HE, Sellars, JD, Knight, K, Edwards, L, Hughes, D, Kaundun, SS, Hutchings, S-J, Steel, PG, Edwards, R (2013) Key role for a glutathione transferase in multiple-herbicide resistance in grass weeds. Proc Natl Acad Sci USA 110:5812–5817CrossRefGoogle ScholarPubMed
Délye, C, Jasieniuk, M, Le Corre, V (2013) Deciphering the evolution of herbicide resistance in weeds. Trends Genet 29:649–658CrossRefGoogle ScholarPubMed
Dyer, WE (2018) Stress-induced evolution of herbicide resistance and related pleiotropic effects. Pest Manag Sci 74:1759–1768CrossRefGoogle ScholarPubMed
Evans, AF Jr, 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 15:1238–1249CrossRefGoogle ScholarPubMed
Evans, JA, Tranel, PJ, Hager, AG, Schutte, B, Wu, C, Chatham, LA, and Davis, AS (2016) Managing the evolution of herbicide resistance. Pest Manag Sci 72:74–80CrossRefGoogle ScholarPubMed
Frenkel, E, Matzrafi, M, Rubin, B, Peleg, Z (2017) Effects of environmental conditions on the fitness penalty in herbicide resistant Brachypodium hybridum. Front Plant Sci 8:94CrossRefGoogle ScholarPubMed
Hager, AG, Wax, LM, Simmons, FW, Stoller, EW (1997) Waterhemp Management in Agronomic Crops. Urbana, IL: University of Illinois Bulletin 855. P 12Google Scholar
Hamad, I, Arda, N, Pekmez, M, Karaer, S, Temizkan, G (2010) Intracellular scavenging activity of Trolox (6-hydroxy-2,5,7,8-tetramethylchromane-2-carboxylic acid) in the fission yeast, Schizosaccharomyces pombe. J Nat Sci Biol Med 1:16–21CrossRefGoogle ScholarPubMed
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 67:258–261CrossRefGoogle Scholar
Hawkes, TR, Holt, DC, Andrews, CJ, Thomas, PJ (2001) Mesotrione: mechanism of herbicidal activity and selectivity in corn. Pages 563–568 in Proceedings of the Brighton Crop Protection Conference. Farnham, U.K.: Brighton Crop Protection CouncilGoogle Scholar
Heap, I (2020) The International Survey of Herbicide Resistant Weeds. http://www.weedscience.org. Accessed: February 26, 2020Google Scholar
Hess, FD (2000) Light-dependent herbicides: an overview. Weed Sci 48:160–170CrossRefGoogle Scholar
Holt, JS, Powles, SB, Holtum, JAH (1993) Mechanisms and agronomic aspects of herbicide resistance. Annu Rev Plant Physiol Plant Mol Biol 44:203–229CrossRefGoogle Scholar
Hu, T, Qv, X, Xiao, G, Huang, X (2009) Enhanced tolerance to herbicide of rice plants by over-expression of a glutathione S-transferase. Mol Breed 24:409–418CrossRefGoogle Scholar
Huberts, DHEW, van der Klei, IJ (2010) Moonlighting proteins: an intriguing mode of multitasking. Biochim Biophys Acta 1803:520–525CrossRefGoogle ScholarPubMed
Huffman, J, Hausman, NE, Hager, AG, Riechers, DE, Tranel, PJ (2015) Genetics and inheritance of nontarget-site resistances to atrazine and mesotrione in a waterhemp (Amaranthus tuberculatus) population from Illinois. Weed Sci 63:799–809CrossRefGoogle Scholar
Jeffery, CJ (2014) An introduction to protein moonlighting. Biochem Soc Trans 42:1679–1683CrossRefGoogle ScholarPubMed
Kaundun, SS, Hutchings, S-J, Dale, RP, Howell, A, Morris, JA, Kramer, VC, Shivrain, VK, Mcindoe, E (2017) Mechanism of resistance to mesotrione in an Amaranthus tuberculatus population from Nebraska, USA. PLoS ONE 12:e0180095CrossRefGoogle Scholar
Ke, Y, Yuan, M, Liu, H, Hui, S, Qin, X, Chen, J, Zhang, Q, Li, X, Xiao, J, Zhang, Q, Wang, S (2020) The versatile functions of OsALDH2B1 provide a genic basis for growth-defense trade-offs in rice. Proc Natl Acad Sci USA 117:3867–3873CrossRefGoogle ScholarPubMed
Knezevic, SZ, Streibig, JC, Ritz, C (2007) Utilizing R software package for dose response studies: the concept and data analysis. Weed Technol 21:840–848CrossRefGoogle Scholar
Kohlhase, DR, Edwards, JW, Owen, MDK (2018) Inheritance of 4-hydroxyphenylpyruvate dioxygenase inhibitor herbicide resistance in an Amaranthus tuberculatus population from Iowa, USA. Plant Sci 274:360–368CrossRefGoogle Scholar
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 32:186–194CrossRefGoogle ScholarPubMed
Lygin, AV, Kaundun, SS, Morris, JA, Mcindoe, E, Hamilton, AR, Riechers, DE (2018) Metabolic pathway of topramezone in multiple-resistant waterhemp (Amaranthus tuberculatus) differs from naturally tolerant maize. Front Plant Sci 9:1644CrossRefGoogle ScholarPubMed
Ma, R, Evans, AF, Riechers, DE (2016) Differential responses to preemergence and postemergence atrazine in two atrazine-resistant waterhemp populations. Agron J 108:1196–1202CrossRefGoogle Scholar
Ma, R, Kaundun, SS, Hawkes, T, Hausman, NE, Tranel, PJ, Hager, AG, Mcindoe, E, Riechers, DE (2013a) Evaluating non-target-site mechanisms of mesotrione resistance in a waterhemp (Amaranthus tuberculatus) population from Illinois. Abstr Weed Sci Soc Am 53:118Google Scholar
Ma, R, Kaundun, SS, Tranel, PJ, Riggins, CW, McGinness, DL, Hager, AG, Hawkes, T, McIndoe, E, Riechers, DE (2013b) Distinct detoxification mechanisms confer resistance to mesotrione and atrazine in a population of waterhemp. Plant Physiol 163:363–377CrossRefGoogle Scholar
Ma, R, Skelton, JJ, Riechers, DE (2015) Measuring rates of herbicide metabolism in dicot weeds with an excised leaf assay. J Visual Expt 103:e53236Google Scholar
Maeda, H, Murata, K, Sakuma, N, Takei, S, Yamazaki, A, Karim, MR, Kawata, M, Hirose, S, Kawagishi-Kobayashi, M, Taniguchi, Y, Suzuki, S, Sekino, K, Ohshima, M, Kato, H, Yoshida, H, Tozawa, Y (2019) A rice gene that confers broad-spectrum resistance to β-triketone herbicides. Science 365:393–396CrossRefGoogle Scholar
Mashiyama, ST, Malabanan, MM, Akiva, E, Bhosle, R, Branch, MC, Hillerich, B, Jagessar, K, Kim, J, Patskovsky, Y, Seidel, RD, Stead, M, Toro, R, Vetting, MW, Almo, SC, Armstrong, RN, Babbitt, PC (2014) Large-scale determination of sequence, structure, and function relationships in cytosolic glutathione transferases across the biosphere. PLoS Biol 12:e1001843CrossRefGoogle ScholarPubMed
Mitchell, G, Bartlett, DW, Fraser, TEM, Hawkes, TR, Holt, DC, Townson, JK, Wichert, RA (2001) Mesotrione: a new selective herbicide for use in maize. Pest Manag Sci 57:120–1283.0.CO;2-E>CrossRefGoogle ScholarPubMed
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 73:2236–2243CrossRefGoogle Scholar
Ndikuryayo, F, Moosavi, B, Yang, W-C, Yang, G-F (2017) 4-Hydroxyphenylpyruvate dioxygenase inhibitors: from chemical biology to agrochemicals. J Agric Food Chem 65:8523–8537CrossRefGoogle ScholarPubMed
Nelson, R, Wiesner-Hanks, T, Wisser, R, Balint-Kurti, P (2018) Navigating complexity to breed disease-resistant crops. Nat Rev Gen 19:21–33CrossRefGoogle ScholarPubMed
Nordby, JN, Williams, MM, Pataky, JK, Riechers, DE, Lutz, JD (2008) A common genetic basis in sweet corn inbred Cr1 for cross sensitivity to multiple cytochrome P450-metabolized herbicides. Weed Sci 56:376–382CrossRefGoogle Scholar
O’Brien, SR, Davis, AS, Riechers, DE (2018) Quantifying resistance to isoxaflutole and mesotrione and investigating their interactions with metribuzin postemergence in Amaranthus tuberculatus. Weed Sci 66:586–594CrossRefGoogle Scholar
Oliveira, MC, Gaines, TA, Jhala, AJ, Knezevic, SZ (2018) Inheritance of mesotrione resistance in an Amaranthus tuberculatus (var. rudis) population from Nebraska, USA. Front Plant Sci 9:60CrossRefGoogle Scholar
Ott, R, Longnecker, M (2010) Conditional probability and independence. Pages 149–152in Taylor, M, ed. An Introduction to Statistical Methods and Data Analysis. 6th ed. Belmont, CA: Brooks/Cole, Cengage LearningGoogle Scholar
Patzoldt, WL, Tranel, PJ, Hager, AG (2005) A waterhemp (Amaranthus tuberculatus) biotype with multiple resistances across three herbicide sites of action. Weed Sci 53:30–36CrossRefGoogle Scholar
Perperopoulou, F, Pouliou, F, Labrou, NE (2018) Recent advances in protein engineering and biotechnological applications of glutathione transferases. Crit Rev Biotechnol 38:511–528CrossRefGoogle ScholarPubMed
Preston, C (2004) Herbicide resistance in weeds endowed by enhanced detoxification: complications for management. Weed Sci 52:448–453CrossRefGoogle Scholar
Refsell, DE, Hartzler, RG (2009) Effect of tillage on common waterhemp (Amaranthus rudis) emergence and vertical distribution of seed in the soil. Weed Technol 23:129–133CrossRefGoogle Scholar
Riechers, DE, Kreuz, K, Zhang, Q (2010) Detoxification without intoxication: herbicide safeners activate plant defense gene expression. Plant Physiol 153:3–13CrossRefGoogle ScholarPubMed
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 7:44913CrossRefGoogle ScholarPubMed
Shergill, LS, Barlow, BR, Bish, MD, Bradley, KW (2018) Investigations of 2,4-D and multiple herbicide resistance in a Missouri waterhemp (Amaranthus tuberculatus) population. Weed Sci 66:386–394CrossRefGoogle Scholar
Steckel, LE (2007) The dioecious Amaranthus spp.: here to stay. Weed Technol 21:567–570CrossRefGoogle Scholar
Steckel, LE, Sprague, CL, Hager, AG, Simmons, FW, Bollero, GA (2003) Effects of shading on common waterhemp (Amaranthus rudis) growth and development. Weed Sci 51:898–903CrossRefGoogle Scholar
Steckel, LE, Sprague, CL, Stoller, EW, Wax, LM, Simmons, FW (2007) Tillage, cropping system, and soil depth effects on common waterhemp (Amaranthus rudis) seed-bank persistence. Weed Sci 55:235–239CrossRefGoogle Scholar
Strom, SA, Davis, AS, Gonzini, L, Mitsdarfer, C, Riechers, DE, Hager, AG (2019) Characterization of multiple herbicide-resistant waterhemp (Amaranthus tuberculatus) populations from Illinois to VLCFA-inhibiting herbicides. Weed Sci 67:369–379CrossRefGoogle Scholar
Tranel, PJ, Riggins, CW, Bell, MS, Hager, AG (2011) Herbicide resistance in Amaranthus tuberculatus: a call for new options. J Agric Food Chem 59:5808–5812CrossRefGoogle Scholar
Tranel, PJ, Wu, C, Sadeque, A (2017) Target-site resistances to ALS and PPO inhibitors are linked in waterhemp (Amaranthus tuberculatus). Weed Sci 65:4–8CrossRefGoogle Scholar
Vennapusa, AR, Faleco, F, Vieira, B, Samuelson, S, Kruger, GR, Werle, R, Jugulam, M (2018) Prevalence and mechanism of atrazine resistance in waterhemp (Amaranthus tuberculatus) from Nebraska. Weed Sci 66:595–602CrossRefGoogle Scholar
Vila-Aiub, MM, Neve, P, Powles, SB (2009) Fitness costs associated with evolved herbicide resistance alleles in plants. New Phytol 184:751–767CrossRefGoogle ScholarPubMed
Williams, MM II, Pataky, JK (2010) Factors affecting differential sensitivity of sweet corn to HPPD-inhibiting herbicides. Weed Sci 58:289–294CrossRefGoogle Scholar
Woodyard, AJ, Bollero, GA, Riechers, DE (2009) Broadleaf weed management in corn utilizing synergistic postemergence herbicide combinations. Weed Technol 23:513–518CrossRefGoogle Scholar
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 166:1106–1118CrossRefGoogle ScholarPubMed