Fitness of herbicide-resistant weeds: Current knowledge and implications for management

Herbicide resistance is the ultimate evidence of the extraordinary capacity of weeds to evolve under stressful conditions. Despite the extraordinary plant fitness advantage endowed by herbicide resistance mutations in agroecosystems under herbicide selection, resistance mutations are predicted to exhibit an adaptation cost (i.e., fitness cost), relative to the susceptible wild-type, in herbicide untreated conditions. Fitness costs associated with herbicide resistance mutations are not universal and their expression depends on the particular mutation, genetic background, dominance of the fitness cost, and environmental conditions. The detrimental effects of herbicide resistance mutations on plant fitness may arise as a direct impact on fitness-related traits and/or coevolution with changes in other life history traits that ultimately may lead to fitness costs under particular ecological conditions. This brings the idea that a “lower adaptive value” of herbicide resistance mutations represents an opportunity for the design of resistance management practices that could minimize the evolution of herbicide resistance. It is evident that the challenge for weed management practices aiming to control, minimize, or even reverse the frequency of resistance mutations in the agricultural landscape is to “create” those agroecological conditions that could expose, exploit, and exacerbate those life history and/or fitness traits affecting the evolution of herbicide resistance mutations. Ideally, resistance management should implement a wide range of cultural practices leading to environmentally mediated fitness costs associated with herbicide resistance mutations.Fil: Vila Aiub, Martin Miguel. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; Argentina. University of Western Australia; Australi

Evidence for an ecological cost of enhanced herbicide metabolism in Lolium rigidum

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-resistant gene traits. Such fitness costs impact in the ecology and evolutionary trajectory of resistant populations. 2. Neighbourhood experiments were performed to quantify competitive effects and responses between herbicide-susceptible (S) and resistant (R) Lolium rigidum individuals in which resistance is due to enhanced herbicide metabolism mediated by cytochrome P450. 3. In two-way competitive interactions between the S and R phenotypes, individuals of the S phenotype were the stronger effect competitors on both a per capita and per unit-size basis. The S phenotype also exhibited a stronger competitive response to wheat plants than did the R phenotype, displaying significantly greater (30%) above-ground biomass at the vegetative stage. When subjected to competition from wheat, R individuals produced significantly fewer reproductive tillers and allocated fewer resources to reproductive traits than individuals of the S phenotype. 4. The role of potential mechanisms underlying this resistance cost driven by traits such as plant size and tolerance to low resource availability, as well as the evolutionary implications of the results are discussed. 5. Synthesis. Evolved herbicide resistance due to enhanced-herbicide metabolism mediated by cytochrome-P450 in L. rigidum has been shown to be accompanied with an impaired ability to compete for resources. These results are consistent with the resource-based theory that predicts a negative trade-off between growth and plant defence

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

Effect of herbicide resistance endowing Ile-1781-Leu and Asp-2078-Gly ACCase gene mutations on ACCase kinetics and growth traits in Lolium rigidum

4711-4718The rate of herbicide resistance evolution in plants depends on fitness traits endowed by alleles in both the presence and absence (resistance cost) of herbicide selection. The effect of two Lolium rigidum spontaneous homozygous target-site resistance-endowing mutations (Ile-1781-Leu, Asp-2078-Gly) on both ACCase activity and various plant growth traits have been investigated here. Relative growth rate (RGR) and components (net assimilation rate, leaf area ratio), resource allocation to different organs, and growth responses in competition with a wheat crop were assessed. Unlike plants carrying the Ile-1781-Leu resistance mutation, plants homozygous for the Asp-2078-Gly mutation exhibited a significantly lower RGR (30 per cent), which translated into lower allocation of biomass to roots, shoots, and leaves, and poor responses to plant competition. Both the negligible and significant growth reductions associated, respectively, with the Ile-1781-Leu and Asp-2078-Gly resistance mutations correlated with their impact on ACCase activity. Whereas the Ile-1781-Leu mutation showed no pleiotropic effects on ACCase kinetics, the Asp-2078-Gly mutation led to a significant reduction in ACCase activity. The impaired growth traits are discussed in the context of resistance costs and the effects of each resistance allele on ACCase activity. Similar effects of these two particular ACCase mutations on the ACCase activity of Alopecurus myosuroides were also confirmed

Evidence for an ecological cost of enhanced herbicide metabolism in Lolium rigidum

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-resistant gene traits. Such fitness costs impact in the ecology and evolutionary trajectory of resistant populations. 2. Neighbourhood experiments were performed to quantify competitive effects and responses between herbicide-susceptible (S) and resistant (R) Lolium rigidum individuals in which resistance is due to enhanced herbicide metabolism mediated by cytochrome P450. 3. In two-way competitive interactions between the S and R phenotypes, individuals of the S phenotype were the stronger effect competitors on both a per capita and per unit-size basis. The S phenotype also exhibited a stronger competitive response to wheat plants than did the R phenotype, displaying significantly greater (30%) above-ground biomass at the vegetative stage. When subjected to competition from wheat, R individuals produced significantly fewer reproductive tillers and allocated fewer resources to reproductive traits than individuals of the S phenotype. 4. The role of potential mechanisms underlying this resistance cost driven by traits such as plant size and tolerance to low resource availability, as well as the evolutionary implications of the results are discussed. 5. Synthesis. Evolved herbicide resistance due to enhanced-herbicide metabolism mediated by cytochrome-P450 in L. rigidum has been shown to be accompanied with an impaired ability to compete for resources. These results are consistent with the resource-based theory that predicts a negative trade-off between growth and plant defence

Editorial: Multiple herbicide-resistant weeds and non-target site resistance mechanisms : a global challenge for food production

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Contrasting plant ecological benefits endowed by naturally occurring EPSPS resistance mutations under glyphosate selection

Concurrent natural evolution of glyphosate resistance single- and double-point EPSPS mutations in weed species provides an opportunity for the estimation of resistance fitness benefits and prediction of equilibrium resistance frequencies in environments under glyphosate selection. Assessment of glyphosate resistance benefit was conducted for the most commonly identified single Pro-106-Ser and less-frequent double TIPS mutations in the EPSPS gene evolved in the global damaging weed Eleusine indica. Under glyphosate selection at the field dose, plants with the single Pro-106-Ser mutation at homozygous state (P106S-rr) showed reduced survival and compromised vegetative growth and fecundity compared with TIPS plants. Whereas both homozygous (TIPS-RR) and compound heterozygous (TIPS-Rr) plants with the double TIPS resistance mutation displayed similar survival rates when exposed to glyphosate, a significantly higher fecundity in the currency of seed number was observed in TIPS-Rr than TIPS-RR plants. The highest plant fitness benefit was associated with the heterozygous TIPS-Rr mutation, whereas plants with the homozygous Pro-106-Ser and TIPS mutations exhibited, respectively, 31% and 39% of the fitness benefit revealed by the TIPS-Rr plants. Populations are predicted to reach stable allelic and genotypic frequencies after 20 years of glyphosate selection at which the WT allele is lost and the stable genotypic polymorphism is comprised by 2% of heterozygous TIPS-Rr, 52% of homozygous TIPS-RR and 46% of homozygous P106S-rr. The high inbreeding nature of E. indica is responsible for the expected frequency decrease in the fittest TIPS-Rr in favour of the homozygous TIPS-RR and P106S-rr. Mutated alleles associated with the glyphosate resistance EPSPS single EPSPS Pro-106-Ser and double TIPS mutations confer contrasting fitness benefits to E. indica under glyphosate treatment and therefore are expected to exhibit contrasting evolution rates in cropping systems under recurrent glyphosate selection.Fil: Vila Aiub, Martin Miguel. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; Argentina. University of Western Australia; AustraliaFil: Han, Heping. University of Western Australia; AustraliaFil: Yu, Qin. University of Western Australia; AustraliaFil: García, Federico. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; ArgentinaFil: Powles, Stephen B.. University of Western Australia; Australi

Glyphosate Resistance in Perennial Ryegrass (Lolium perenne L.) is Associated with a Fitness Penalty

The net selection effect of herbicides on herbicide-resistance traits in weeds is conditioned by the fitness benefits and costs associated with resistance alleles. Fitness costs play an important evolutionary role preventing the fixation of adaptive alleles and contributing to the maintenance of genetic polymorphisms within populations. Glyphosate is widely used in world agriculture, which has led to the evolution of widespread glyphosate resistance in many weed species. The fitness of glyphosate-resistant and -susceptible perennial ryegrass plants selected from within a single population were studied in two field experiments conducted during 2011 and 2012 under different soil water availability. Glyphosate-resistant plants showed a reduction in height of 12 and 16%, leaf blade area of 16 and 33%, shoot biomass of 45 and 55%, seed number of 33 and 53%, and total seed mass of 16 and 5% compared to glyphosate-susceptible plants in 2011 and 2012, respectively. The reduction in seed number per plant resulted in a 40% fitness cost associated with the glyphosate-resistance trait in perennial ryegrass. Fitness costs of glyphosate-resistant plants were expressed under both conditions of water availability. These results could be useful for designing management strategies and exploiting the reduced glyphosate-resistant perennial ryegrass fitness in the absence of glyphosate selection.Facultad de Ciencias Agrarias y Forestale

Physiological Fitness Cost Associated with Glyphosate Resistance in Echinochloa colona: Seed Germination Ecology

The expression of fitness cost associated with herbicide resistance in weeds is not universal and may vary during different life stages. Hence, an analysis of the fitness cost of a glyphosate-resistant Echinochloa colona at the seed stage was conducted. Seed germination ecology of glyphosate-susceptible and - resistant E. colona was studied to examine the physiological fitness cost between the S (susceptible) and R (resistant) phenotypes. The plant material was selected from within one segregating glyphosateresistant E. colona population to minimise allelic interference from other fitness-related loci. Experiments were conducted in a growth incubator at alternating temperatures of 30/20C day/night with a 12-h photoperiod. Seed dormancy and germination were also tested under constant darkness at the same temperature regime. Seeds of both the S and R phenotypes kept at warmer temperatures (after-ripening dry storage at 15 to 35C) or on the ground surface outdoors for 14 days, germinated better (with more than 95% of seeds had germinated) than those seeds (about 20% germination) that were kept at lower temperature (8C) for the same period of storage. Light and longer dry after-ripening times increased the rate of seed dormancy release and germination (almost 100% seed germination) for both the S and R phenotypes. Equal decline in seedling emergence in both the S and R phenotypes was evident with increasing soil burial depth (P > 0.05). Thus, the S and R phenotypes exhibited similar characteristics of seed dormancy release, germination and seedling emergence. As there is lack of physiological fitness cost in the R phenotype of E. colona at the seed and early seedling stage, it remains a challenge to develop specific control measures for the R phenotype. An alternative herbicide with different mode of action should be integrated with other weed management approach such as cultural, mechanical and biological control to reduce sole reliance of glyphosate in controlling the R phenotype of this E. colona population.Fil: Sheng Goh, Sou. The Malaysian Rubber Board; MalasiaFil: Vila Aiub, Martin Miguel. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; ArgentinaFil: Busi, Roberto. University of Western Australia; AustraliaFil: Goggin, Danica. University of Western Australia; AustraliaFil: Powles, Stephen B.. University of Western Australia; Australi