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      DNA Analysis of Herbarium Specimens of the Grass Weed Alopecurus myosuroides Reveals Herbicide Resistance Pre-Dated Herbicides

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      PLoS ONE

      Public Library of Science

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          Abstract

          Acetyl-CoA carboxylase ( ACCase) alleles carrying one point mutation that confers resistance to herbicides have been identified in arable grass weed populations where resistance has evolved under the selective pressure of herbicides. In an effort to determine whether herbicide resistance evolves from newly arisen mutations or from standing genetic variation in weed populations, we used herbarium specimens of the grass weed Alopecurus myosuroides to seek mutant ACCase alleles carrying an isoleucine-to-leucine substitution at codon 1781 that endows herbicide resistance. These specimens had been collected between 1788 and 1975, i.e., prior to the commercial release of herbicides inhibiting ACCase. Among the 734 specimens investigated, 685 yielded DNA suitable for PCR. Genotyping the ACCase locus using the derived Cleaved Amplified Polymorphic Sequence (dCAPS) technique identified one heterozygous mutant specimen that had been collected in 1888. Occurrence of a mutant codon encoding a leucine residue at codon 1781 at the heterozygous state was confirmed in this specimen by sequencing, clearly demonstrating that resistance to herbicides can pre-date herbicides in weeds. We conclude that point mutations endowing resistance to herbicides without having associated deleterious pleiotropic effects can be present in weed populations as part of their standing genetic variation, in frequencies higher than the mutation frequency, thereby facilitating their subsequent selection by herbicide applications.

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          Most cited references 15

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          dCAPS, a simple technique for the genetic analysis of single nucleotide polymorphisms: experimental applications in Arabidopsis thaliana genetics.

          PCR-based detection of single nucleotide polymorphisms is a powerful tool for the plant geneticist. Cleaved amplified polymorphic sequence analysis is the most widely used approach for the detection of single nucleotide polymorphisms. However, this technique is limited to mutations which create or disrupt a restriction enzyme recognition site. This paper presents a modification of this technique where mismatches in a PCR primer are used to create a polymorphism based on the target mutation. This technique is useful for following known mutations in segregating populations and genetic mapping of isolated DNAs used for positional based cloning of new genes. In addition, a computer program has been developed that facilitates the design of these PCR primers.
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            Unravelling the genetic bases of non-target-site-based resistance (NTSR) to herbicides: a major challenge for weed science in the forthcoming decade.

            Non-target-site-based resistance (NTSR) can confer unpredictable cross-resistance to herbicides. However, the genetic determinants of NTSR remain poorly known. The current, urgent challenge for weed scientists is thus to elucidate the bases of NTSR so that detection tools are developed, the evolution of NTSR is understood, the efficacy of the shrinking herbicide portfolio is maintained and integrated weed management strategies, including fully effective herbicide applications, are designed and implemented. In this paper, the importance of NTSR in resistance to herbicides is underlined. The most likely way in which NTSR evolves-by accumulation of different mechanisms within individual plants-is described. The NTSR mechanisms, which can interfere with herbicide penetration, translocation and accumulation at the target site, and/or protect the plant against the consequences of herbicide action, are then reviewed. NTSR is a part of the plant stress response. As such, NTSR is a dynamic process unrolling over time that involves 'protectors' directly interfering with herbicide action, and also regulators controlling 'protector' expression. NTSR is thus a quantitative trait. On this basis, a three-step procedure is proposed, based on the use of the 'omics' (genomics, transcriptomics, proteomics or metabolomics), to unravel the genetic bases of NTSR. Copyright © 2012 Society of Chemical Industry.
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              Fitness costs associated with evolved herbicide resistance alleles in plants.

              Predictions based on evolutionary theory suggest that the adaptive value of evolved herbicide resistance alleles may be compromised by the existence of fitness costs. There have been many studies quantifying the fitness costs associated with novel herbicide resistance alleles, reflecting the importance of fitness costs in determining the evolutionary dynamics of resistance. However, many of these studies have incorrectly defined resistance or used inappropriate plant material and methods to measure fitness. This review has two major objectives. First, to propose a methodological framework that establishes experimental criteria to unequivocally evaluate fitness costs. Second, to present a comprehensive analysis of the literature on fitness costs associated with herbicide resistance alleles. This analysis reveals unquestionable evidence that some herbicide resistance alleles are associated with pleiotropic effects that result in plant fitness costs. Observed costs are evident from herbicide resistance-endowing amino acid substitutions in proteins involved in amino acid, fatty acid, auxin and cellulose biosynthesis, as well as enzymes involved in herbicide metabolism. However, these resistance fitness costs are not universal and their expression depends on particular plant alleles and mutations. The findings of this review are discussed within the context of the plant defence trade-off theory and herbicide resistance evolution.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2013
                16 October 2013
                : 8
                : 10
                Affiliations
                INRA, UMR1347 Agroécologie, Dijon, France
                University of Florence, Italy
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: C. Délye C. Deulvot. Performed the experiments: C. Deulvot. Analyzed the data: C. Délye C. Deulvot BC. Contributed reagents/materials/analysis tools: C. Délye C. Deulvot BC. Wrote the manuscript: C. Délye C. Deulvot BC. Obtained permission for sampling herbarium specimens: BC.

                Article
                PONE-D-13-25703
                10.1371/journal.pone.0075117
                3797703

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                Funding
                The authors are grateful to Bayer CropScience SA (Lyon, France) for supporting this work. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. This does not alter the authors' adherence to all the PLOS ONE policies on sharing data and materials.
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