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Front. Plant Sci. | doi: 10.3389/fpls.2018.01644

Metabolic Pathway of Topramezone in Multiple-Resistant Waterhemp (Amaranthus tuberculatus) Differs from Naturally Tolerant Maize

Anatoli V. Lygin1,  Shiv S. Kaundun2, James A. Morris2, Eddie McIndoe2,  Andrea R. Hamilton3 and  Dean E. Riechers1*
  • 1University of Illinois at Urbana-Champaign, United States
  • 2Syngenta (United Kingdom), United Kingdom
  • 3Truman State University, United States

Waterhemp [Amaranthus tuberculatus (Moq.) Sauer] is a problematic dicot weed in maize, soybean, and cotton production in the United States. Waterhemp has evolved resistance to several commercial herbicides that inhibit the 4-hydroxyphenylpyruvate-dioxygenase (HPPD) enzyme in sensitive dicots, and research to date has shown that HPPD-inhibitor resistance is conferred by rapid oxidative metabolism of the parent compound in resistant populations. Mesotrione and tembotrione (both triketones) have been used exclusively to study HPPD-inhibitor resistance mechanisms in waterhemp and a related species, Amaranthus palmeri (S. Wats.), but the commercial HPPD inhibitor topramezone (a pyrazolone) has not been investigated from a mechanistic standpoint despite numerous reports of cross resistance in the field and greenhouse. The first objective of our research was to determine if two multiple herbicide-resistant (MHR) waterhemp populations (named NEB and SIR) metabolize topramezone more rapidly than two HPPD inhibitor-sensitive waterhemp populations (named SEN and ACR). Our second objective was to determine if initial topramezone metabolite(s) detected in MHR waterhemp are qualitatively different than those formed in maize. An excised leaf assay and whole-plant study investigated initial rates of topramezone metabolism (< 24 hr) and identified topramezone metabolites at 48 hours after treatment (HAT), respectively, in the four waterhemp populations and maize. Results indicated both MHR waterhemp populations metabolized more topramezone than the sensitive (SEN) population at 6 HAT, while only the SIR population metabolized more topramezone than SEN at 24 HAT. Maize metabolized more topramezone than any waterhemp population at each time point examined. LC-MS analysis of topramezone metabolites at 48 HAT showed maize primarily formed desmethyl and benzoic acid metabolites, as expected based on published reports, whereas SIR formed two putative hydroxylated metabolites. Subsequent LC-MS/MS analyses identified both hydroxytopramezone metabolites in SIR as different hydroxylation products of the isoxazole ring, which were also present in maize 48 HAT but at very low levels. These results indicate that SIR initially metabolizes and detoxifies topramezone in a different manner than tolerant maize.

Keywords: Herbicide metabolism in plant, detoxification, Triketone herbicides, Pyrazolone, cytochrome P450, oxidative metabolism, Herbicide Resistance, HPPD inhibitors

Received: 29 Aug 2018; Accepted: 23 Oct 2018.

Edited by:

Fumiya Kurosaki, University of Toyama, Toyama, Japan

Reviewed by:

Tahira Fatima, Purdue University, United States
Rafael De Prado, Universidad de Córdoba, Spain  

Copyright: © 2018 Lygin, Kaundun, Morris, McIndoe, Hamilton and Riechers. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Dr. Dean E. Riechers, University of Illinois at Urbana-Champaign, Champaign, 61820, Illinois, United States, riechers@illinois.edu