Coevolution of resistance to PPO inhibitors in waterhemp (Amaranthus tuberculatus) and Palmer amaranth (Amaranthus palmeri)

Abstract

The first case of evolved protoporphyrinogen oxidase (PPO)-inhibitor resistance was observed in 2001 in common waterhemp [Amaranthus tuberculatus (Moq.) Sauer var. rudis (Sauer) Costea and Tardif]. This resistance in A. tuberculatus is most commonly conferred by deletion of the amino acid glycine at the 210th position (ΔGly-210) of the PPO enzyme (PPO2) encoded by PPX2. In a field in Kentucky in 2015, inadequate control of Amaranthus plants was observed following application of a PPO inhibitor. Morphological observations indicated that survivors included both A. tuberculatus and Palmer amaranth (Amaranthus palmeri S. Watson).Research was conducted to confirm species identities and resistance and then to determine whether resistance evolved independently in the two species or via hybridization. Results from a quantitative PCR assay based on the ribosomal internal transcribed spacer confirmed that both A. tuberculatus and A. palmeri coexisted in the field. The mutation conferring ΔGly-210 in PPO2 was identified in both species; phylogenetic analysis of a region of PPX2, however, indicated that the mutation evolved independently in the two species. Genotyping of greenhousegrown plants that survived lactofen indicated that all A. tuberculatus survivors, but only a third of A. palmeri survivors, contained the ΔGly-210 mutation. Consequently, A. palmeri plants were evaluated for the presence of an arginine to glycine or methionine substitution at position 128 of PPO2 (Arg-128-Gly and Arg-128-Met). The Arg-128-Gly substitution was found to account for resistance that was not accounted for by the ΔGly-210 mutation in plants from the A. palmeri population. Results from this study provide a modern-day example of both parallel and convergent evolution occurring within a single field. https://www.cambridge.org/core/terms. https://doi.

Herbicide drift exposure leads to reduced herbicide sensitivity in Amaranthus spp.

“…Both species had similar mortality when exposed to dicamba drift. Inherent differences in herbicide response between Palmer amaranth and waterhemp were reported in previous studies, with Palmer amaranth being more tolerant to PPO-inhibitors 50 , but more susceptible to glyphosate 17 . Palmer amaranth was very susceptible to glyphosate drift, especially with applications using the flat fan nozzle.…”

“…Both are obligate outcrossing dioecious weed species with a fast growth habitat, extended emergence window, and prolific seed production with high genetic plasticity which pose a challenge to their management 37-44 . Numerous Palmer amaranth and waterhemp populations have evolved resistance to herbicides that target 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS), 4-hydroxyphenylpyruvate dioxygenase (HPPD), photosystem II, protoporphyrinogen oxidase (PPO), auxin receptors, microtubule assembly, and acetolacte synthase (ALS) in the US 15,17,[45][46][47][48][49][50][51][52][53][54] . Moreover, pollen mediated gene flow has been reported as a major contributor to herbicide resistance dissemination in Palmer amaranth and waterhemp in the US Midwest 55,56 .Although controlling weed populations on field margins and ditches is considered a best management practice to delay herbicide resistance evolution, these weed populations are often neglected in agricultural landscapes [15][16][17]29 .…”

Can double PPO mutations exist in a same allele and are such mutants functional?

“…The importance of this residue for protogen binding relates to the salt bridge formed between the positively charged Arg with the negatively charged carboxyl group of ring C of protogen. 1,13,14,22 The continued use of PPO-inhibitors, the dioecious character of some Amaranthus species and their hybridization capacity, has led to an accumulation of mutations at the population-, plant-and allele-levels, 9,11,17,23 although the latter is very rare. Computational data suggested that both combinations ∆G210 + G399A and G399A + R128G would confer high resistance to fomesafen, but the very low frequency of such genotypes, and the absence of double homozygous plants could also indicate that the resultant protein might be inactive.…”

Differences in efficacy, resistance mechanism and target protein interaction between two PPO inhibitors in Palmer amaranth (Amaranthus palmeri)

“…While looking at the spread of resistance at the landscape level, the outcrossing nature of A. palmeri posts another layer of concern, especially surrounding the coevolution of resistance (Lillie et al 2019). Many Amaranthus species are dioecious, and interspecies hybridization among the Amaranthus family is known to facilitate the transfer of herbicide-resistance mechanisms (Franssen et al 2001;Gaines et al 2012;Nandula et al 2014;Trucco et al 2005).…”