Enhanced metabolic detoxification is associated with fluroxypyr resistance in Bassia scoparia

Authors: Todd, Olivia; PATTERSON, ERIC - Michigan State University; WESTRA, ERIC - Utah State University; NISSEN, SCOTT - Colorado State University; LUCAS SIMOES ARAUJO, ANDRE - Colorado State University; KRAMER, WILLIAM - Colorado State University; DAYAN, FRANCK - Colorado State University; GAINES, TODD - Colorado State University

Submitted to: Plant Direct
Publication Type: Pre-print Publication
Publication Acceptance Date: 12/6/2023
Publication Date: 1/24/2024
Citation: Todd, O.E., Patterson, E.L., Westra, E.P., Nissen, S.J., Lucas Simoes Araujo, A., Kramer, W., Dayan, F.E., Gaines, T.A. 2024. Enhanced metabolic detoxification is associated with fluroxypyr resistance in Bassia scoparia. Plant Direct. 8(1). Article e560. https://doi.org/10.1002/pld3.560.
DOI: https://doi.org/10.1002/pld3.560

Interpretive Summary: The herbicides fluroxypyr and dicamba are among the most used herbicides in the world. Weed resistance poses a threat in no-till wheat-fallow systems as growers continually rely on these products’ efficacy to control the troublesome weed, kochia. Reports of resistance to dicamba and fluroxypyr in kochia are increasing, which drives the need for understanding the resistance mechanisms so scientists may advise the best and current weed control methods. Scientists at Colorado State University and USDA-ARS in Fort Collins, CO have discovered a resistance mechanism to the herbicide fluroxypyr that helps researchers and farmers understand the issues with herbicide overuse, and how it affects the genetics of the weeds that we apply herbicides to by increasing natural selection of resistant weeds.

Technical Abstract: Auxin-mimic herbicides chemically mimic the phytohormone indole-3-acetic-acid (IAA). Within the auxin-mimic herbicide class, the herbicide fluroxypyr has been extensively used to control an agronomically problematic Great Plains tumbleweed, kochia (Bassia scoparia). A 2014 field survey for herbicide resistance in kochia populations across Colorado identified a putative fluroxypyr resistant population that was assessed for response to five different herbicides representing four different herbicide modes of action. These included fluroxypyr and dicamba (auxin-mimics), atrazine (photosystem II inhibitor), glyphosate (EPSPS inhibitor), and chlorsulfuron (acetolactate synthase inhibitor). The greenhouse screen identified that this kochia population was resistant to fluroxypyr and chlorsulfuron, but sensitive to glyphosate, atrazine, and dicamba. This population was designated Flur-R. Subsequent dose response studies determined that 75% of the Flur-R population survived 628 g ae ha-1 of fluroxypyr (4' the label application rate in wheat fallow, which is 157 g ae ha-1 at 1'). Flur-R was 40 times more resistant to fluroxypyr than a susceptible population (J01-S) collected from the same field survey (LD50 720 and 20 g ae ha-1, respectively). Auxin-responsive gene expression increased following fluroxypyr treatment in both Flur-R, J01-S and dicamba-resistant, fluroxypyr-susceptible line 9425 in an RNA-sequencing experiment. In Flur-R, several transcripts with molecular functions for conjugation and transport were constitutively higher expressed, such as glutathione S-transferases (GSTs), UDP-glucosyl transferase (GT), and ATP binding cassette transporters (ABC transporters). After analyzing metabolic profiles over time, both Flur-R and J01-S rapidly converted [14C]-fluroxypyr ester, the herbicide formulation applied to plants, to [14C]-fluroxypyr acid, the biologically active form of the herbicide, and three unknown metabolites. Formation and flux of these metabolites was faster in Flur-R than J01-S, reducing the concentration of phytotoxic fluroxypyr acid. One unique metabolite was present in Flur-R that was not present in the J01-S metabolic profile. Gene sequence variant analysis specifically for auxin receptor and signaling proteins revealed the absence of non-synonymous mutations affecting auxin signaling and binding in candidate auxin target site genes, further supporting our hypothesis that non-target site metabolic degradation is contributing to fluroxypyr resistance in Flur-R.