Genetic control of a cytochrome P450 metabolism-based herbicide resistance mechanism in Lolium rigidum (original) (raw)
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New Phytologist, 2005
• Costs of resistance are predicted to reduce plant productivity in herbicide-resistant weeds.• Lolium rigidum herbicide-susceptible individuals (S), individuals possessing cytochrome P450-based herbicide metabolism (P450) and multiple resistant individuals possessing a resistant ACCase and enhanced cytochrome P450 metabolism (ACCase/P450) were grown in the absence of mutual plant interaction to estimate plant growth traits.• Both P450 and ACCase/P450 resistant phenotypes produced less above-ground biomass than the S phenotype during the vegetative stage. Reduced biomass production in the resistant phenotypes corresponded to a reduced relative growth rate and a lower net assimilation rate and rate of carbon fixation. There were no significant differences between the two resistant phenotypes, suggesting that costs of resistance are associated with P450 metabolism-based resistance. There were no differences in reproductive output among the three phenotypes, indicating that the cost of P450 resistance during vegetative growth is compensated during the production of reproductive structures.• The P450-based herbicide metabolism is shown to be associated with physiological resistance costs, which may be manipulated by agronomic management to reduce the evolution of herbicide resistance.Costs of resistance are predicted to reduce plant productivity in herbicide-resistant weeds.Lolium rigidum herbicide-susceptible individuals (S), individuals possessing cytochrome P450-based herbicide metabolism (P450) and multiple resistant individuals possessing a resistant ACCase and enhanced cytochrome P450 metabolism (ACCase/P450) were grown in the absence of mutual plant interaction to estimate plant growth traits.Both P450 and ACCase/P450 resistant phenotypes produced less above-ground biomass than the S phenotype during the vegetative stage. Reduced biomass production in the resistant phenotypes corresponded to a reduced relative growth rate and a lower net assimilation rate and rate of carbon fixation. There were no significant differences between the two resistant phenotypes, suggesting that costs of resistance are associated with P450 metabolism-based resistance. There were no differences in reproductive output among the three phenotypes, indicating that the cost of P450 resistance during vegetative growth is compensated during the production of reproductive structures.The P450-based herbicide metabolism is shown to be associated with physiological resistance costs, which may be manipulated by agronomic management to reduce the evolution of herbicide resistance.
Enhanced rates of herbicide metabolism in low herbicide-dose selected resistant Lolium rigidum
Plant, Cell & Environment, 2013
Lolium rigidum is an obligately cross-pollinated, genetically diverse species and an economically important herbicide resistance-prone weed. Our previous work has demonstrated that recurrent selection of initially susceptible L. rigidum populations with low herbicide rates results in rapid herbicide resistance evolution. Here we report on the mechanisms endowing low-dose-selected diclofop-methyl resistance in L. rigidum. Results showed that resistance was not due to target-site ACCase mutations or overproduction, or differential herbicide leaf uptake and translocation. The in vivo de-esterification of diclofop-methyl into phytotoxic diclofop acid was rapid and similar in resistant versus susceptible populations. However, further metabolism of diclofop acid into non-toxic metabolites was always faster in resistant plants than susceptible plants, resulting in up to 2.6-fold lower level of diclofop acid in resistant plants. This corresponded well with up to twofold higher level of diclofop acid metabolites in resistant plants. The major polar metabolites of diclofop acid chromatographically resembled those of wheat, a naturally tolerant species. Clearly, recurrent selection at reduced herbicide rates selected for non-target-sitebased enhanced rates of herbicide metabolism, likely involving cytochrome P450 monooxygenases.
Evolutionary Applications, 2013
The interaction between environment and genetic traits under selection is the basis of evolution. In this study, we have investigated the genetic basis of herbicide resistance in a highly characterized initially herbicide-susceptible Lolium rigidum population recurrently selected with low (below recommended label) doses of the herbicide diclofop-methyl. We report the variability in herbicide resistance levels observed in F 1 families and the segregation of resistance observed in F 2 and back-cross (BC) families. The selected herbicide resistance phenotypic trait(s) appear to be under complex polygenic control. The estimation of the effective minimum number of genes (N E ), depending on the herbicide dose used, reveals at least three resistance genes had been enriched. A joint scaling test indicates that an additive-dominance model best explains gene interactions in parental, F 1 , F 2 and BC families. The Mendelian study of six F 2 and two BC segregating families confirmed involvement of more than one resistance gene. Cross-pollinated L. rigidum under selection at low herbicide dose can rapidly evolve polygenic broad-spectrum herbicide resistance by quantitative accumulation of additive genes of small effect. This can be minimized by using herbicides at the recommended dose which causes high mortality acting outside the normal range of phenotypic variation for herbicide susceptibility.
Frontiers in Plant Science, 2016
Herbicide resistance is a ubiquitous challenge to herbicide sustainability and a looming threat to control weeds in crops. Recently four genes were found constituently over-expressed in herbicide resistant individuals of Lolium rigidum, a close relative of Lolium multiflorum. These include two cytochrome P450s, one nitronate monooxygenase and one glycosyl-transferase. Higher expressions of these four herbicide metabolism related (HMR) genes were also observed after herbicides exposure in the gene expression databases, indicating them as reliable markers. In order to get an overview of herbicidal resistance status of L. multiflorum L, 19 field populations were collected. Among these populations, four populations were found to be resistant to acetolactate synthase (ALS) inhibitors while three exhibited resistance to acetyl-CoA carboxylase (ACCase) inhibitors in our initial screening and dose response study. The genotyping showed the presence of mutations Trp-574-Leu and Ile-2041-Asn in ALS and ACCase, respectively, and qPCR experiments revealed the enhanced expression of HMR genes in individuals of certain resistant populations. Moreover, co-expression networks and promoter analyses of HMR genes in O. sativa and A. thaliana resulted in the identification of a cis-regulatory motif and zinc finger transcription factors. The identified transcription factors were highly expressed similar to HMR genes in response to xenobiotics whereas the identified motif is known to play a vital role in coping with environmental stresses and maintaining genome stability. Overall, our findings provide an important step forward toward a better understanding of metabolism-based herbicide resistance that can be utilized to devise novel strategies of weed management.
Pest management science, 2015
Lolium rigidum populations in Australia and globally have demonstrated rapid and widespread evolution of resistance to acetyl coenzyme A carboxylase (ACCase)-inhibiting and acetolactate synthase (ALS)-inhibiting herbicides. Thirty-three resistant L. rigidum populations, randomly collected from crop fields in a most recent resistance survey, were analysed for non-target-site diclofop metabolism and all known target-site ACCase gene resistance-endowing mutations. The HPLC profile of [(14) C]-diclofop-methyl in vivo metabolism revealed that 79% of these resistant L. rigidum populations showed enhanced capacity for diclofop acid metabolism (metabolic resistance). ACCase gene sequencing identified that 91% of the populations contain plants with ACCase resistance mutation(s). Importantly, 70% of the populations exhibit both non-target-site metabolic resistance and target-site ACCase mutations. This work demonstrates that metabolic herbicide resistance is commonly occurring in L. rigidum, ...
Evidence for an ecological cost of enhanced herbicide metabolism in Lolium rigidum
Journal of Ecology, 2009
Article Title: Evidence for an ecological cost of enhanced herbicide metabolism in Lolium rigidum Year of publication: 2009 Link to published version:http://dx.Running title: ecological cost of herbicide resistance Summary 1. In some cases, evaluation of resource competitive interactions between herbicide resistant vs. susceptible weed ecotypes provides evidence for the expression of fitness costs associated with evolved herbicide-resistance gene traits. Such fitness costs impact the ecology and evolutionary trajectory of resistant populations.
Induction and inactivation of a cytochrome P450 confering herbicide resistance in wheat seedlings
European Journal of Drug Metabolism and Pharmacokinetics, 2001
Cytochrome P450-dependent enzymes from wheat catalyze the oxidation of endogenous compounds (lauric and oleic acids) and of several herbicides (diclofop, chlortoluron, bentazon). Treatment of wheat seedlings with the satener, naphthalic anhydride and with phenobarbital increases dramatically several P450-dependent enzyme activities including diclofop and lauric acid hydroxylation. The parallel induction of lauric acid ({J)-1)-hydroxylase and diclofop hydroxylase activities suggests that both compounds proceeds from the same or very similar forms of P450. To test whether either one or multiple P450 forms are involved in these oxidations, we have designed selective irreversible inhibitors of lauric acid ({J)-1)-hydroxylase. Results of in vivo and in vitro experiments with acetylenic analogs of lauric acid (10-and 11-dodecynoic acids) strongly suggest that a single P450 catalyzes both laurate and diclofop hydroxylation. Treatment of wheat seedlings with these acetylenes results in a strong inhibition of the in vivo metabolism of diclofop although oxidation of chlortoluron and bentazon are not affected. Our results suggest that at least three distinct P450 forms are involved in the detoxification process of the three herbicides. Interestingly, we also demonstrate that herbicides themselves are potent inducers of the amount of total P450 and laurate/diclofop hydroxylase activies. This increased capacity of wheat to detoxify the herbicide through the induction of P450 enzymes seems to be for a large extend the mechanism which confers a tolerance on various herbicides.
Agriculture, Ecosystems & Environment, 2011
In two different locations of the Western Australian "wheatbelt", Lolium rigidum (rigid ryegrass) seeds were collected from organic fields (no herbicide use) and neighbouring conventional fields (persistent herbicide use), the latter infested with herbicide-resistant plants, to investigate the occurrence of gene flow among field populations as revealed by herbicide resistance gene transfer. Herbicides targeting acetyl-CoA carboxylase (ACCase) or acetolactate-synthase (ALS) were used to detect herbicide-resistant plants. Overall, the frequency of plants resistant to ACCase-or ALS-inhibiting herbicides was, respectively, 21% and 74% in the conventional fields and 2% and 37% in neighbouring organic fields. Mutant, herbicideresistant ACCase and ALS alleles were detected in 16% and 38% of plants from conventional fields and in 0.53% and 3.7% of plants from organic fields. Identical mutant, herbicide-resistant ALS haplotypes were detected both in conventional and organic fields, supporting the occurrence of gene flow between L. rigidum populations in different fields. Gene flow can thus substantially increase the frequency of herbicide-resistant plants in unselected L. rigidum populations. Although gene flow cannot be prevented, it can be limited or managed. Hygiene tactics such as clean crop seed, weed seed removal at harvest and seed destruction post-harvest should be considered in order to minimize gene transfer among farms.