Abstract
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, A. 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 h) 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.
Highlights
Topramezone is a 4-hydroxyphenylpyruvate dioxygenase (HPPD)-inhibiting herbicide primarily used postemergence (POST) in maize (Zea mays L.) for broadleaf and grass weed control (Grossmann and Ehrhardt, 2007; Gitsopoulos et al, 2010)
Mechanistic research investigating topramezone metabolism has not been reported in multiple herbicide-resistant (MHR) Amaranthus populations, yet studying topramezone detoxification in MHR plants is of great interest since topramezone belongs to the pyrazolone subfamily of HPPD inhibitors (Figure 1) (Siddall et al, 2002; Grossmann and Ehrhardt, 2007; Ndikuryayo et al, 2017)
Our findings indicate that MHR waterhemp populations possess multiple genes encoding diverse metabolic enzymes that confer complex, herbicide-dependent, cross- or multiple resistance patterns, which may be influenced significantly by prior fielduse histories
Summary
Topramezone is a 4-hydroxyphenylpyruvate dioxygenase (HPPD)-inhibiting herbicide primarily used postemergence (POST) in maize (Zea mays L.) for broadleaf and grass weed control (Grossmann and Ehrhardt, 2007; Gitsopoulos et al, 2010). Several published reports indicated enhanced oxidative metabolism of either mesotrione (Ma et al, 2013; Kaundun et al, 2017; Nakka et al, 2017) or tembotrione (Küpper et al, 2018) contributes significantly to whole-plant resistance levels relative to HPPD inhibitor-sensitive populations Since these two herbicides belong to the triketone subfamily of HPPDinhibiting herbicides (Figure 1) (Lee et al, 1998; Ndikuryayo et al, 2017), it is not surprising that metabolic resistance in Amaranthus populations proceeds via 4-hydroxylation of the cyclohexanedione ring, which is the same mechanism underlying maize tolerance and selectivity (Hawkes et al, 2001). It remains to be experimentally determined whether populations resistant to HPPD-inhibiting herbicides mimic maize by detoxifying topramezone by N-demethylation (Grossmann and Ehrhardt, 2007) or via ring/alkyl hydroxylation at a liable position, as is the case for mesotrione (Hawkes et al, 2001; Ma et al, 2013)
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