Stephen B. Powles

Evolution in action: plants resistant to herbicides.

Modern herbicides make major contributions to global food production by easily removing weeds and substituting for destructive soil cultivation. However, persistent herbicide selection of huge weed numbers across vast areas can result in the rapid evolution of herbicide resistance. Herbicides target specific enzymes, and mutations are selected that confer resistance-endowing amino acid substitutions, decreasing herbicide binding. Where herbicides bind within an enzyme catalytic site very few mutations give resistance while conserving enzyme functionality. Where herbicides bind away from a catalytic site many resistance-endowing mutations may evolve. Increasingly, resistance evolves due to mechanisms limiting herbicide reaching target sites. Especially threatening are herbicide-degrading cytochrome P450 enzymes able to detoxify existing, new, and even herbicides yet to be discovered. Global weed species are accumulating resistance mechanisms, displaying multiple resistance across many herbicides and posing a great challenge to herbicide sustainability in world agriculture. Fascinating genetic issues associated with resistance evolution remain to be investigated, especially the possibility of herbicide stress unleashing epigenetic gene expression. Understanding resistance and building sustainable solutions to herbicide resistance evolution are necessary and worthy challenges.

Glyphosate: a once-in-a-century herbicide.

Since its commercial introduction in 1974, glyphosate [N-(phosphonomethyl)glycine] has become the dominant herbicide worldwide. There are several reasons for its success. Glyphosate is a highly effective broad-spectrum herbicide, yet it is very toxicologically and environmentally safe. Glyphosate translocates well, and its action is slow enough to take advantage of this. Glyphosate is the only herbicide that targets 5-enolpyruvyl-shikimate-3-phosphate synthase (EPSPS), so there are no competing herbicide analogs or classes. Since glyphosate became a generic compound, its cost has dropped dramatically. Perhaps the most important aspect of the success of glyphosate has been the introduction of transgenic, glyphosate-resistant crops in 1996. Almost 90% of all transgenic crops grown worldwide are glyphosate resistant, and the adoption of these crops is increasing at a steady pace. Glyphosate/glyphosate-resistant crop weed management offers significant environmental and other benefits over the technologies that it replaces. The use of this virtually ideal herbicide is now being threatened by the evolution of glyphosate-resistant weeds. Adoption of resistance management practices will be required to maintain the benefits of glyphosate technologies for future generations.

Reducing the Risks of Herbicide Resistance: Best Management Practices and Recommendations

Herbicides are the foundation of weed control in commercial crop-production systems. However, herbicide-resistant (HR) weed populations are evolving rapidly as a natural response to selection pressure imposed by modern agricultural management activities. Mitigating the evolution of herbicide resistance depends on reducing selection through diversification of weed control techniques, minimizing the spread of resistance genes and genotypes via pollen or propagule dispersal, and eliminating additions of weed seed to the soil seedbank. Effective deployment of such a multifaceted approach will require shifting from the current concept of basing weed management on single-year economic thresholds.

Evolved glyphosate-resistant weeds around the world: lessons to be learnt.

Glyphosate is the worlds most important herbicide, with many uses that deliver effective and sustained control of a wide spectrum of unwanted (weedy) plant species. Until recently there were relatively few reports of weedy plant species evolving resistance to glyphosate. Since 1996, the advent and subsequent high adoption of transgenic glyphosate-resistant crops in the Americas has meant unprecedented and often exclusive use of glyphosate for weed control over very large areas. Consequently, in regions of the USA where transgenic glyphosate-resistant crops dominate, there are now evolved glyphosate-resistant populations of the economically damaging weed species Ambrosia artemissifolia L., Ambrosia trifida L., Amaranthus palmeri S Watson, Amaranthus rudis JD Sauer, Amaranthus tuberculatus (Moq) JD Sauer and various Conyza and Lolium spp. Likewise, in areas of transgenic glyphosate-resistant crops in Argentina and Brazil, there are now evolved glyphosate-resistant populations of Sorghum halepense (L.) Pers and Euphorbia heterophylla L. respectively. As transgenic glyphosate-resistant crops will remain very popular with producers, it is anticipated that glyphosate-resistant biotypes of other prominent weed species will evolve over the next few years. Therefore, evolved glyphosate-resistant weeds are a major risk for the continued success of glyphosate and transgenic glyphosate-resistant crops. However, glyphosate-resistant weeds are not yet a problem in many parts of the world, and lessons can be learnt and actions taken to achieve glyphosate sustainability. A major lesson is that maintenance of diversity in weed management systems is crucial for glyphosate to be sustainable. Glyphosate is essential for present and future world food production, and action to secure its sustainability for future generations is a global imperative.

Herbicide Resistance in Plants: Biology and Biochemistry

The late 1980s saw an explosion in the amount and diversity of herbicide resistance, posing a threat to crop production in many countries. The rapid escalation in herbicide resistance worldwide has meant that the understanding of resistance at the population, biochemical and molecular level has also been developed. Leading researchers from North America, Australia and Western Europe present reviews which consider the population dynamics and genetics, biochemistry and argo-ecology of resistance. This text should be a useful reference for those interested in evolution and the ability of species to overcome severe environmental stress.

Evolved Glyphosate Resistance in Plants: Biochemical and Genetic Basis of Resistance'

Resistance to the herbicide glyphosate is currently known in at least eight weed species from many countries. Some populations of goosegrass from Malaysia, rigid ryegrass from Australia, and Italian ryegrass from Chile exhibit target site–based resistance to glyphosate through changes at amino acid 106 of the 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS) gene. Mutations change amino acid 106 from proline to either serine or threonine, conferring an EPSPS weakly resistant to glyphosate. The moderate level of resistance is sufficient for commercial failure of the herbicide to control these plants in the field. Conversely, a nontarget site resistance mechanism has been documented in glyphosate-resistant populations of horseweed and rigid ryegrass from the United States and Australia, respectively. In these resistant plants, there is reduced translocation of glyphosate to meristematic tissues. Both of these mechanisms are inherited as a single, nuclear gene trait. Although at present only two glyphosate-resistance mechanisms are known, it is likely that other mechanisms will become evident. The already very large and still increasing reliance on glyphosate in many parts of the world will inevitably result in more glyphosate-resistant weeds, placing the sustainability of this precious herbicide resource at risk. Nomenclature: Glyphosate; goosegrass, Eleusine indica (L.) Gaertn. #3 ELEIN; horseweed, Conyza canadensis (L.) Cronq. # ERICA; rigid ryegrass, Lolium rigidum Gaud. # LOLRI; Italian ryegrass, Lolium multiflorum Lam. # LOLMU. Additional index words: EPSPS, herbicide resistance, herbicide translocation. Abbreviations: ACCase, acetyl-coenzyme A carboxylase; ALS, acetolactate synthase; ESPS, 5-enolpyruvylshikimate-3-phosphate synthase.

Herbicide Resistance: Impact and Management

Publisher Summary This chapter focuses on the threat to the productivity of world agriculture imposed by the evolution of herbicide-resistant weed populations. Implicit in this chapter is that herbicides should and will continue to be a major tool for weed control. It is believed that modern herbicides are a cost-effective, efficient, and environmentally benign means for obtaining weed control. Proponents rightly identify the benefits of herbicides in achieving weed control as well as positive environmental influences in substituting for soil cultivation in weed management. Reliance on herbicides for weed control is expected to continue because there is no attractive superior technology available. However, for sustainable weed management to be achieved, changes to current herbicide use patterns are required. Multiple-resistant populations of weeds, such as L. rigidum and A . myosuroides, are current indicators of potential worst-case weed problems of the future. Resistance will continue to increase if present herbicide use patterns are not altered.

Investigations into the mechanism of glyphosate resistance in Lolium rigidum

Glyphosate is a widely used non-selective herbicide to which so far only three weed species have evolved resistance. Here, we report on the mechanism of glyphosate resistance in one resistant population of Lolium rigidum (Gaud.). Experiments demonstrate that glyphosate resistance in this population is directly correlated with increased transport of the herbicide to leaf tips. No significant differences in the level of expression of the herbicide target site, EPSP synthase, between resistant and susceptible plants were found and the enzyme is equally sensitive to inhibition by glyphosate in both populations. Similarly, plant metabolism of glyphosate does not contribute to resistance. Resistant and susceptible plants are equally capable of absorbing the applied herbicide. The most notable difference between resistant and susceptible populations is found in the translocation of glyphosate. Following treatment, an accumulation of glyphosate in the roots of susceptible plants is observed, whereas glyphosate accumulates in the leaf tips of resistant plants. Taken together, it seems likely that an alteration to the cellular transport of glyphosate confers resistance.

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.

Resistance to glyphosate in Lolium rigidum

Annual ryegrass (Lolium rigidum) is a widespread and important weed of Australia and populations of this weed have developed resistance to most major herbicides, including glyphosate. The possible mechanisms of resistance have been examined in one glyphosate-resistant Lolium population. No major differences were observed between resistant and susceptible biotypes in respect of (i) the target enzyme (EPSP synthase), (ii) DAHP synthase, the first enzyme of the target (shikimate) pathway, (iii) absorption of glyphosate, or (iv) translocation. Following treatment with glyphosate, there was greater accumulation of shikimate (derived from shikimate-3-Pi) in susceptible than in resistant plants. In addition, the resistant population exhibited cross-resistance to 2-hydroxy-3-(1,2,4-triazol-1-yl)propyl phosphonate, a herbicide which, although structurally similar to glyphosate, acts at an unrelated target site. On the basis of these observations we speculate that movement of glyphosate to its site of action in the plastid is involved in the resistance mechanism. © 1999 Society of Chemical Industry