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    Stress-induced evolution of herbicide resistance and related pleiotropic effects
    (2018-08) Dyer, William E.
    Herbicide-resistant weeds, especially those with resistance to multiple herbicides, represent a growing worldwide threat to agriculture and food security. Natural selection for resistant genotypes may act on standing genetic variation, or on a genetic and physiological background that is fundamentally altered because of stress responses to sublethal herbicide exposure. Stress-induced changes include DNA mutations, epigenetic alterations, transcriptional remodeling, and protein modifications, all of which can lead to herbicide resistance and a wide range of pleiotropic effects. Resistance selected in this manner is termed systemic acquired herbicide resistance, and the associated pleiotropic effects are manifested as a suite of constitutive transcriptional and post-translational changes related to biotic and abiotic stress adaptation, representing the evolutionary signature of selection. This phenotype is being investigated in two multiple herbicide-resistant populations of the hexaploid, self-pollinating weedy monocot Avena fatua that display such changes as well as constitutive reductions in certain heat shock proteins and their transcripts, which are well known as global regulators of diverse stress adaptation pathways. Herbicide-resistant populations of most weedy plant species exhibit pleiotropic effects, and their association with resistance genes presents a fertile area of investigation. This review proposes that more detailed studies of resistant A. fatua and other species through the lens of plant evolution under stress will inform improved resistant weed prevention and management strategies.
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    Non-target site resistance to flucarbazone, imazamethabenz and pinoxaden is controlled by three linked genes in Avena fatua
    (2018-02) Burns, Erin E.; Keith, Barbara K.; Talbert, Luther E.; Dyer, William E.
    Extensive herbicide usage has led to the evolution of resistant weed populations that cause substantial crop yield losses and increase production costs. The multiple herbicide-resistant (MHR) Avena fatua populations utilised in this study are resistant to members of all selective herbicide families, across five modes of action, available for A. fatua control in US small grain production, and thus pose significant agronomic and economic threats. Resistance to acetolactate synthase and acetyl-CoA carboxylase inhibitors is not conferred by known target site mutations, indicating that non-target site resistance (NTSR) mechanisms are involved. Understanding the inheritance of NTS MHR is of upmost importance for continued agricultural productivity in the face of the rapid increase in resistant weed populations worldwide. As few studies have examined the inheritance of NTSR in autogamous weeds, we investigated the inheritance and genetic control of NTSR in the highly autogamous, allohexaploid species A. fatua. We found that NTSR in MHRA. fatua is controlled by three separate, closely-linked nuclear genes for flucarbazone-sodium, imazamethabenz-methyl and pinoxaden. The single-gene NTSR inheritance patterns reported here contrast with other examples in allogamous species and illustrate the diversity of evolutionary responses to strong selection.
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    Constitutive redox and phosphoproteome changes in multiple herbicide resistant Avena fatua L. are similar to those of systemic acquired resistance and systemic acquired acclimation
    (2018-01) Burns, Erin E.; Keith, Barbara K.; Mohammed, Refai Y.; Bothner, Brian; Dyer, William E.
    Plants are routinely confronted with numerous biotic and abiotic stressors, and in response have evolved highly effective strategies of systemic acquired resistance (SAR) and systemic acquired acclimation (SAA), respectively. A much more evolutionarily recent abiotic stress is the application of herbicides to control weedy plants, and their intensive use has selected for resistant weed populations that cause substantial crop yield losses and increase production costs. Non-target site resistance (NTSR) to herbicides is rapidly increasing worldwide and is associated with alterations in generalized stress defense networks. This work investigated protein post-translational modifications associated with NTSR in multiple herbicide resistant (MHR) Avena fatua, and their commonalities with those of SAR and SAA. We used proteomic, biochemical, and immunological approaches to compare constitutive protein profiles in MHR and herbicide susceptible (HS) A. fatua populations. Phosphoproteome and redox proteome surveys showed that post-translational modifications of proteins with functions in core cellular processes were reduced in MHR plants, while those involved in xenobiotic and stress response, reactive oxygen species detoxification and redox maintenance, heat shock response, and intracellular signaling were elevated in MHR as compared to HS plants. More specifically, MHR plants contained constitutively elevated levels of three protein kinases including the lectin S-receptor-like serine/threonine-protein kinase LecRK2, a well-characterized component of SAR. Analyses of superoxide dismutase enzyme activity and protein levels did not reveal constitutive differences between MHR and HS plants. The overall results support the idea that herbicide stress is perceived similarly to other abiotic stresses, and that A. fatua NTSR shares analogous features with SAR and SAA. We speculate that MHR A. fatua's previous exposure to sublethal herbicide doses, as well as earlier evolution under a diversity of abiotic and biotic stressors, has led to a heightened state of stress preparedness that includes NTSR to a number of unrelated herbicides.
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    Development and Evaluation of an introductory course in sustainable food and bioenergy systems
    (2014-02) Malone, Kate; Harmon, Alison H.; Dyer, William E.; Maxwell, Bruce D.; Perillo, Catherine
    The purpose of this paper is to describe the development, instruction, and evaluation of the undergraduate pilot course, Introduction to Sustainable Food and Bioenergy Systems (SFBS), at Montana State University. Introduction to SFBS is an interdisciplinary, team-taught, experiential education course designed to introduce students to broad array of SFBS-related topics, expose students to career opportunities in these fields, and enable them to establish relationships with food, agriculture, and energy stakeholders. Students completed baseline and follow-up surveys in which they reported information about their backgrounds, values, and knowledge of SFBS-related topics. The surveys also tracked students' learning and allowed them to provide feedback on course methods. According to the follow-up survey, over the course of the semester students demonstrated development of course vocabulary and concepts. Students' experiences in the course prompted changes in their school- and career-related goals. Additionally, the team-teaching approach was highly valued. Students also indicated that teaching should be more solutions-focused. Evaluation of students' backgrounds and learning is an important tool for the future evolution of this course and the development of others like it. The survey tool was in its first iteration; it will require revision as the course evolves. Introduction to SFBS can serve as a model for curricula related to sustainable agriculture, food, and energy. Courses like this can prepare students to become informed, innovative, critical thinkers capable of excelling in a multitude of food, agriculture, and energy-related careers. This course will continue to be monitored and evaluated as the curriculum evolves.
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    Proteomic and biochemical assays of glutathione-related proteins in susceptible and multiple herbicide resistant Avena fatua L.
    (2017-06) Burns, Erin E.; Keith, Barbara K.; Refai, Mohammed Y.; Bothner, Brian; Dyer, William E.
    Extensive herbicide usage has led to the evolution of resistant weed populations that cause substantial crop yield losses and increase production costs. The multiple herbicide resistant (MHR) Avena fatua L. populations utilized in this study are resistant to members of all selective herbicide families, across five modes of action, available for A. fatua control in U.S. small grain production, and thus pose significant agronomic and economic threats. Resistance to ALS and ACCase inhibitors is not conferred by target site mutations, indicating that non-target site resistance mechanisms are involved. To investigate the potential involvement of glutathione-related enzymes in the MHR phenotype, we used a combination of proteomic, biochemical, and immunological approaches to compare their constitutive activities in herbicide susceptible (HS1 and HS2) and MHR (MHR3 and MHR4) A. fatua plants. Proteomic analysis identified three tau and one phi glutathione S-transferases (GSTs) present at higher levels in MHR compared to HS plants, while immunoassays revealed elevated levels of lambda, phi, and tau GSTs. GST specific activity towards 1-chloro-2,4-dinitrobenzene was 1.2-fold higher in MHR4 than in HS1 plants and 1.3- and 1.2-fold higher in MHR3 than in HS1 and HS2 plants, respectively. However, GST specific activities towards fenoxaprop-P-ethyl and imazamethabenz-methyl were not different between untreated MHR and HS plants. Dehydroascorbate reductase specific activity was 1.4-fold higher in MHR than HS plants. Pretreatment with the GST inhibitor NBD-Cl did not affect MHR sensitivity to fenoxaprop-P-ethyl application, while the herbicide safener and GST inducer mefenpyr reduced the efficacy of low doses of fenoxaprop-P-ethyl on MHR4 but not MHR3 plants. Mefenpyr treatment also partially reduced the efficacy of thiencarbazone-methyl or mesosulfuron-methyl on MHR3 or MHR4 plants, respectively. Overall, the GSTs described here are not directly involved in enhanced rates of fenoxaprop-P-ethyl or imazamethabenz-methyl metabolism in MHR A. fatua. Instead, we propose that the constitutively elevated GST proteins and related enzymes in MHR plants are representative of a larger, more global suite of abiotic stress-related changes.
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    Intensive herbicide use has selected for constitutively elevated levels of stress-responsive mRNAs and proteins in multiple herbicide-resistant Avena fatua L.
    (2017-08) Keith, Barbara K.; Burns, Erin E.; Bothner, Brian; Carey, Charles C.; Mazurie, Aurélien J.; Hilmer, Jonathan K.; Biyiklioglu, Sezgi; Budak, Hikmet; Dyer, William E.
    BACKGROUND: Intensive use of herbicides has led to the evolution two multiple herbicide-resistant (MHR) Avena fatua (wild oat) populations in Montana that are resistant to members of all selective herbicide families available for A. fatua control in U.S. small grain crops. We used transcriptome and proteome surveys to compare constitutive changes in MHR and herbicide susceptible (HS) plants associated with non-target site resistance (NTSR). RESULTS: Compared to HS plants, MHR plants contained constitutively elevated levels of differentially expressed genes (DEGs) with functions in xenobiotic catabolism, stress response, redox maintenance, and transcriptional regulation that are similar to abiotic-stress tolerant phenotypes. Proteome comparisons identified similarly elevated proteins including biosynthetic and multifunctional enzymes in MHR plants. Of 25 DEGs validated by RT-qPCR assay, differential regulation of 21 co-segregated with flucarbazone-sodium herbicide resistance in F3 families, and a subset of 10 of these were induced or repressed in herbicide-treated HS plants. CONCLUSIONS: Although the individual and collective contributions of these DEGs and proteins to MHR remain to be determined, our results support the idea that intensive herbicide use has selected for MHR populations with altered, constitutively-regulated patterns of gene expression that are similar to those in abiotic stress-tolerant plants. This article is protected by copyright. All rights reserved.
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    New Curricula for Undergraduate Food-Systems Education: A Sustainable Agriculture Education Perspective
    (2014-12) Jordan, Nicolas; Grossman, J.; Lawrence, Patrick G.; Harmon, Alison H.; Dyer, William E.; Maxwell, Bruce D.; Cadieux, K.V.; Galt, Ryan; Rojas, A.; Byker Shanks, Carmen; Ahmed, Selena; Bass, Thomas; Kebreab, E.; Singh, V.; Michaels, T.; Tzenis, C.
    New undergraduate degree programs that address food systems have appeared at a number of North American universities in the past decade. These programs seek to complement established food- and agriculture-related courses of instruction with additional curricular elements that build students’ capacity to address complex food-systems issues (e.g., food sustainability, security, quality, equity and justice) in the course of their work in food-related professions. Here, we examine these emerging food-systems curricula, building on our collective experiences developing food-systems degree programs at University of British Columbia, Montana State University, University of California-Davis and the University of Minnesota. We present the conceptual framework that underlies our efforts, based on the premise that our degree programs should help students build “systemic” capacities that complement disciplinary training provided by various specialization “tracks.” Thus, we intend for our graduates to have a dual preparation, in both a particular specialization, and in overarching systemic capacities that enhance their ability to address complex food-system issues. We assess our current curricula in light of our framework, and outline high-priority pathways for further development of these curricula.
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    Soil movement and residual aspects of chlorsulfuron and its control of Canada thistle (Cirsium arvense (L.) Scop.)
    (Montana State University - Bozeman, College of Agriculture, 1983) Dyer, William E.
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    Impact of Biotic and Abiotic Stresses on the Competitive Ability of Multiple Herbicide Resistant Wild Oat (Avena fatua)
    (2013-05) Lehnhoff, Erik A.; Keith, Barbara K.; Dyer, William E.; Menalled, Fabian D.
    Ecological theory predicts that fitness costs of herbicide resistance should lead to the reduced relative abundance of resistant populations upon the cessation of herbicide use. This greenhouse research investigated the potential fitness costs of two multiple herbicide resistant (MHR) wild oat (Avena fatua) populations, an economically important weed that affects cereal and pulse crop production in the Northern Great Plains of North America. We compared the competitive ability of two MHR and two herbicide susceptible (HS) A. fatua populations along a gradient of biotic and abiotic stresses The biotic stress was imposed by three levels of wheat (Triticum aestivum) competition (0, 4, and 8 individuals pot−1) and an abiotic stress by three nitrogen (N) fertilization rates (0, 50 and 100 kg N ha−1). Data were analyzed with linear mixed-effects models and results showed that the biomass of all A. fatua populations decreased with increasing T. aestivum competition at all N rates. Similarly, A. fatua relative growth rate (RGR) decreased with increasing T. aestivum competition at the medium and high N rates but there was no response with 0 N. There were no differences between the levels of biomass or RGR of HS and MHR populations in response to T. aestivum competition. Overall, the results indicate that MHR does not confer growth-related fitness costs in these A. fatua populations, and that their relative abundance will not be diminished with respect to HS populations in the absence of herbicide treatment.
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