Resistant weeds, fitness

In practical terms, the Ser264 to Gly mutation causing triazine resistance reduces plant productivity and yield. This has two agronomic implications first, triazine-resistant weeds carrying this mutation are less competitive (often referred in the literature as reduced fitness) on a per plant basis as compared to their susceptible counterparts, and second, triazine-resistant rapeseed cultivars with Hie mutant psbA gene are less productive than near isogenic, susceptible cultivars (Forcella, 1987 Beversdorf et al, 1988 Hart and Stemler, 1990 Hall et al, 1996). 

Triazine-resistant weeds have an impaired electron transport system. Reduced electron transport, in turn, reduces photosynthetic activity and fitness. Under controlled conditions, most triazine-resistant biotypes exhibit impaired photosynthesis. Significant fitness costs from resistance (10-50%) have been reported in most studies (Warwick, 1991). This substantial fitness cost or handicap has been important in the management of triazine-resistant weeds (Radosevich et al., 1991 Bergelson and Purrington, 1996). Anderson et al. (1996b) found that the competitive advantage of triazine-susceptible waterhemp over triazine-resistant waterhemp isolated from one field in Nebraska was equal to or less than that for other species or isolates. This indicates that additional factors contributed to the slow and limited distribution of resistance for this waterhemp biotype. 

This characteristic, however, is not universally found in all triazine-resistant weeds. Gray et al. (1995a, b) found that velvetleaf resistance to atrazine in Wisconsin was not associated with a reduction in fitness, productivity, or intraspecific competitive ability. This triazine-resistant species found in Maryland and Wisconsin does not have D1 level resistance in the chloroplasts, but instead has a more rapid metabolic detoxification of triazines in these biotypes. The extent of the rapid metabolic resistance in other velvetleaf-resistant biotypes is unknown. 

There is generally a lack of fitness or ability in the triazine-resistant biotypes to compete with the crop or with other nontriazine-resistant weeds as a result of the altered triazine binding site at the D1 protein in PS II. 

Radosevich, S.R., B.D. Maxwell, and M.L. Roush (1991). Managing herbicide resistance through fitness and gene flow. In J.C. Caseley, G.W. Cussans, and R.K. Atkin, eds., Herbicide Resistance in Weeds and Crops. Oxford, UK Butterworth-Heinemann Ltd, pp. 129-143. 

The rate of evolution of resistant weeds is based on several factors, including characteristics of the weed and herbicide, gene frequency, size and viability of the soil seedbank, weed fitness, herbicide potency, frequency and rate of application, and persistence in soil. Various attempts have been made to use modeling to determine the relative importance of these factors and to predict the probability of resistance, as well as to evaluate how to avoid, delay, or solve the problem (Gressel and Segel, 1990). 

Table VIII shows some interesting trends in the first occurrences of herbicide resistant biotypes. Not only are herbicide resistant weeds appearing after fewer repeat annual applications of some of the newer herbicides (e.g., 4 to 5 years of treatment with sulfonylures herbicides), but there seem to be more species that have potential for resistance, as shown by the 26 new cases in 1988. In addition, the resistant biotypes are more fit and competitive than most biotypes resistant to triazine herbicides.

The lower relative fitness in most triazine resistant weeds is a very important reason why they have been fairly easily controlled, and why more problems of cross-resistance or multiple resistance have not occurred where both a triazine and another type of herbicide have been used together repeatedly. However, some cases of such cross-resistance are now beginning to appear, consistent with the predictions by Gressel and Segel (12). 

In the field, natural selection acts to optimize the adaptations of a plant so as to maximize individual fitness. In triazine resistant weeds, coevolution of the less productive chloroplast with the nuclear genome could have resulted in compensatory mechanisms not present in susceptible plants. These mechanisms could optimize productivity and maximize the fitness of those individuals, within the constraints imposed by impaired PSII. Even slight differences in the chloroplast genome between susceptible and resistant biotypes could result in different responses to the same selection pressures in the environment, perhaps in the direction of overcoming limitations caused by the resistance mutation. Thus, after several generations of selection, many nuclear-genome controlled traits are likely to appear that could mask intrinsic differences between biotypes due to the chloroplast mutation. It is also possible that the alteration in PSII in resistant plants triggers developmental events that compensate in some way. Effects of the resistance mutation may be compensated for by other aspects of plant performance such as carbon allocation or rate of development. Resistant plants may not necessarily be less productive than susceptible ones when traits not directly linked with triazine resistance are considered. 

Herbicide resistant populations have evolved only in monoculture and/or mono-herbicide conditions at the rates we have previously predicted. Contrary to our original model, no populations of atrazine-resistant weeds have appeared in corn where rotations of crops and herbicides or herbicide mixtures were used. This is due to the previous lack of information about the greatly reduced fitness of the resistant individuals, which could be expressed only during rotational cycles, and also to the greater sensitivity of resistant individuals to other herbicides, pests and control practices. 

Various parameters appear in the simple algebraic Eq. 1 for the frequency (proportion) of resistant weeds in a species that is preponderantly sensitive to a given herbicide. N is the very low frequency of resistant individuals in the population before it is exposed to the herbicide. In the absence of herbicide, resistance is sustained in the population by a balance between mutation and depletion of the proportion of resistant individuals by their lesser fitness in the absence of selection, resulting in a resistance fraction somewhat lower than the mutation frequency. If mutants were more fit than the wild type, they would be the wild type. Mutant fitness can be near neutrality, and the mutants would then be found in different proportions at various geographical areas due to drift". 

Many of the characteristics which combine to make ALS an excellent target for engineering beneficial herbicide resistance in crop plants may also lead to the proliferation of herbicide-resistant weeds. These characteristics include the following sulfonylurea herbicide resistance is a semi-dominant trait that is carried on a nuclear gene(s) ALS is the single primary site of action there are multiple positions in ALS that can be mutated to confer herbicide resistance mutant ALS enzymes can possess full catalytic activity. The latter property results in engineered crop plants that are fit, but can equally well result in weed biotypes that are fit. 

The ALS inhibitors are at the highest risk for the selection of resistance in weeds because they have a single target site, are effective against a wide spectrum of weeds, are now used extensively on many crops, and are relatively persistent - often providing season-long control of germinating weed seeds (Brown et al., 1995). Also, the various sites of mutations for resistance are not near the active site of the enzyme. As a result, there is no fitness loss due to a lower affinity for the normal substrates (Christoffoleti et al., 1997). 

Natural selection for a particular trait incurs an initial cost to the organism in terms of fitness, or its ability to survive and reproduce. In weeds selected for herbicide resistance, this generalization holds true for biotypes possessing the maternally inherited trait of triazine resistance. This mutation has a detrimental effect on photosynthesis that results in decreased biomass production and reproductive output. However, compensatory interactions of the chloroplast and nuclear genomes may partially overcome reduced productivity. Expression of reduced productivity also appears to be regulated by environmental conditions. Whether similar trends in relative fitness will be found in weeds resistant to other herbicides remains to be examined. 

It should be possible to assess the potential and the reason for decreased fitness in resistant biotypes in cases where the mechanism of resistance is known (2). Table I lists the herbicides or classes of herbicides to which resistance has been found in field situations and for which the mechanism of resistance is known or suspected. (A complete list of weeds with herbicide resistant biotypes as of December, 1988 is presented in the chapter by LeBaron and McFarland in this book.)... 

Eq. 1 allowed the plotting of rates of enrichment of resistance, with different scenarios of selection pressure, seed bank size, fitness, and initial mutation frequency (Fig. 1A). The values that could be plugged into the equation to generate the scenarios were based on a very limited data-base, mostly from corollary systems, such as heavy-metal tolerance. We knew too little about weed-herbicide interactions at that time to make precise estimates. With the experience of hindsight, we can see where the model was clearly correct, and where it needed modification. 

The very low frequencies of resistant individuals in the field must compete with the crop, with resistant members of other weed species, and (when the herbicide is not present) with susceptible members of the same and other species. If triazine resistance evolved only in populations with plastome mutator genes (see above), there is the strong possibility of multiple mutations in these plastid genomes, including deleterious mutations giving unfit alleles of other genes. These may explain much of the unfitness of resistant plants, as well as the published variabilities of plastid fitness. Deleterious nuclear... 

The previous model kept track of the various influences affecting resistant and susceptible weeds. In particular, a seed bank was presumed to contain fully viable seeds for n years which then died. We neglected the loss of seeds from the seed bank due to germination. In the appendix to our earlier paper (3), an alternative model was developed based on the hypothesis that a constant fraction of seeds in the seed bank perish each year for resistants and for susceptibles). In this alternative model the effects of germination on the seed bank are tallied. The two models agreed and yielded Eq. 1 when the factors / and a of Eq. 1 satisfied fa 1, i.e., when the herbicide selection pressure was sufficiently high. We now know that this will not be met in rotational years with fitness near 0.1 and a < 10. 

Returning to Eq. 9, we show in Fig. 4 the values of a that provide resistance stasis, as a function of the duration of the seedbank, for f0// = 0.2 (Fig. 4A) and for values of f0 that are so small compared to unity (/<,// <. 05) that /off essentially has no effect (Fig. 4B). Three possible rotation strategies are examined. We see that there can be cases where there is no enrichment at all for resistance. If the effective kill of 2,4-D in wheat is only 50-60% due to late weed germination, then under low fitness and a 1 1 enrichment there is no enrichment (Fig. 4). Stasis can even be obtained with selection pressures above 90% if there is a 2 or more year interval between the treatments with the herbicide. Stasis is impossible with very high selection pressure herbicides in usual rotational sequences. Long duration in the seed bank is actually a deterrent to stasis, as resistant seeds act as a buffer for longer periods (Fig. 4). 

In many cases, mutants of weed species with target-site resistance to triazines showed lower growth rate and ecological fitness than the susceptible wild type, when analyzed in absence of a triazine herbicide as selection agent. The quantum yield of CO2 reduction in resistant biotypes was decreased. Furthermore, the electron transfer between the primary and secondary quinones in the PS II reaction center was slowed, which may have been the cause of increased susceptibility to photoinhibition in the resistant biotypes [23, 24]. 

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