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      Herbicide Safeners Decrease Sensitivity to Herbicides Inhibiting Acetolactate-Synthase and Likely Activate Non-Target-Site-Based Resistance Pathways in the Major Grass Weed Lolium sp. (Rye-Grass)

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          Abstract

          Herbicides are currently pivotal to control weeds and sustain food security. Herbicides must efficiently kill weeds while being as harmless as possible for crops, even crops taxonomically close to weeds. To increase their selectivity toward crops, some herbicides are sprayed in association with safeners that are bioactive compounds exacerbating herbicide-degrading pathways reputedly specifically in crops. However, exacerbated herbicide metabolism is also a key mechanism underlying evolved non-target-site-based resistance to herbicides (NTSR) in weeds. This raised the issue of a possible role of safeners on NTSR evolution in weeds. We investigated a possible effect of the respective field rates of the two broadly used safeners cloquintocet-mexyl and mefenpyr-diethyl on the sensitivity of the troublesome global weed Lolium sp. (rye-grass) to the major herbicides inhibiting acetolactate-synthase (ALS) pyroxsulam and iodosulfuron + mesosulfuron, respectively. Three Lolium sp. populations were studied in three series of experiments. The first experiment series compared the frequencies of plants surviving application of each herbicide alone or in association with its safener. Safener co-application caused a net increase ranging from 5.0 to 46.5% in the frequency of plants surviving the field rate of their associated herbicide. In a second series of experiments, safener effect was assessed on individual plant sensitivity using vegetative propagation. A reduction in sensitivity to pyroxsulam and to iodosulfuron + mesosulfuron was observed for 44.4 and 11.1% of the plants in co-treatment with cloquintocet-mexyl and mefenpyr-diethyl, respectively. A third series of experiments investigated safener effect on the expression level of 19 Lolium sp. NTSR marker genes. Safeners showed an enhancing effect on the expression level of 10 genes. Overall, we demonstrated that cloquintocet-mexyl and mefenpyr-diethyl both reduced the sensitivity of Lolium sp. to their associated ALS-inhibiting herbicide and most likely exacerbated herbicide-degrading secondary metabolism pathways. This suggests that genetic variation for safener response is present in Lolium sp. Thus, a possible, uninvestigated way to NTSR evolution could be selection for increased responsiveness to safener action. Delivering safeners exclusively to the crop could mitigate the risk for NTSR evolution in weeds.

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          Most cited references35

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          Deciphering the evolution of herbicide resistance in weeds.

          Resistance to herbicides in arable weeds is increasing rapidly worldwide and threatening global food security. Resistance has now been reported to all major herbicide modes of action despite the development of resistance management strategies in the 1990s. We review here recent advances in understanding the genetic bases and evolutionary drivers of herbicide resistance that highlight the complex nature of selection for this adaptive trait. Whereas early studied cases of resistance were highly herbicide-specific and largely under monogenic control, cases of greatest concern today generally involve resistance to multiple modes of action, are under polygenic control, and are derived from pre-existing stress response pathways. Although 'omics' approaches should enable unraveling the genetic bases of complex resistances, the appearance, selection, and spread of herbicide resistance in weed populations can only be fully elucidated by focusing on evolutionary dynamics and implementing integrative modeling efforts. Copyright © 2013 Elsevier Ltd. All rights reserved.
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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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              Non-target-site herbicide resistance: a family business.

              We have witnessed a dramatic increase in the frequency and diversity of herbicide-resistant weed biotypes over the past two decades, which poses a threat to the sustainability of agriculture at both local and global levels. In addition, non-target-site mechanisms of herbicide resistance seem to be increasingly implicated. Non-target-site herbicide resistance normally involves the biochemical modification of the herbicide and/or the compartmentation of the herbicide (and its metabolites). In contrast to herbicide target site mutations, fewer non-target mechanisms have been elucidated at the molecular level because of the inherently complicated biochemical processes and the limited genomic information available for weedy species. To further understand the mechanisms of non-target-site resistance, we propose an integrated genomics approach to dissect systematically the functional genomics of four gene families in economically important weed species.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                08 August 2017
                2017
                : 8
                : 1310
                Affiliations
                l'Institut National de la Recherche Agronomique (INRA) Agroécologie, Dijon, France
                Author notes

                Edited by: Chengdao Li, Murdoch University, Australia

                Reviewed by: Todd Gaines, Colorado State University, United States; Khawar Jabran, Duzce University, Turkey

                *Correspondence: Christophe Délye christophe.delye@ 123456inra.fr

                This article was submitted to Crop Science and Horticulture, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2017.01310
                5551093
                81e5b46d-6a38-4b08-990e-7d45a5bdc38d
                Copyright © 2017 Duhoux, Pernin, Desserre and Délye.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 17 February 2017
                : 12 July 2017
                Page count
                Figures: 5, Tables: 3, Equations: 0, References: 36, Pages: 14, Words: 9204
                Categories
                Plant Science
                Original Research

                Plant science & Botany
                evolution,herbicide resistance,safener,plant secondary metabolism,transcriptional marker,weed management

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