Epistatic Interactions among Herbicide Resistances in Arabidopsis Thaliana: The Fitness Cost of Multiresistance

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ABSTRACT

The type of interactions among deleterious mutations is considered to be crucial in numerous areas of evolutionary biology, including the evolution of sex and recombination, the evolution of ploidy, the evolution of selfing, and the conservation of small populations. Because the herbicide resistance genes could be viewed as slightly deleterious mutations in the absence of the pesticide selection pressure, the epistatic interactions among three herbicide resistance genes (acetolactate synthase CSR, cellulose synthase IXR1, and auxin-induced AXR1 target genes) were estimated in both the homozygous and the heterozygous states, giving 27 genotype combinations in the model plant Arabidopsis thaliana. By analyzing eight quantitative traits in a segregating population for the three herbicide resistances in the absence of herbicide, we found that most interactions in both the homozygous and the heterozygous states were best explained by multiplicative effects (each additional resistance gene causes a comparable reduction in fitness) rather than by synergistic effects (each additional resistance gene causes a disproportionate fitness reduction). Dominance coefficients of the herbicide resistance cost ranged from partial dominance to underdominance, with a mean dominance coefficient of 0.07. It was suggested that the csr1-1, ixr1-2, and axr1-3 resistance alleles are nearly fully recessive for the fitness cost. More interestingly, the dominance of a specific resistance gene in the absence of herbicide varied according to, first, the presence of the other resistance genes and, second, the quantitative trait analyzed. These results and their implications for multiresistance evolution are discussed in relation to the maintenance of polymorphism at resistance loci in a heterogeneous environment.

THE type of interactions among deleterious mutations is considered to be crucial in numerous areas of evolutionary biology, including the evolution of sex and recombination (KONDRASHOV 1988; BARTON and CHARLESWORTH 1998; PECK and WAXMAN 2000; OTTO and LENORMAND 2002), the evolution of ploidy (PERROT et al. 1991), the evolution of selfing (CHARLESWORTH and CHARLESWORTH 1998), and the conservation of small populations (LANDE 1994). All these issues relate to the mutation load of a population due to the accumulation of deleterious mutations (KIMURA and MARUYAMA 1966). Sex and recombination can provide an advantage by reducing this load (KONDRASHOV 1982). The mutational deterministic (MD) hypothesis states that the elimination of deleterious mutations provides an advantage to sex if the interactions among mutations are synergistic, that is, when each additional deleterious mutation leads to a greater decrease in fitness than the previous one (RIVERO et al. 2003).

Empirical evidence for synergistic epistasis is rather sparse, however (e.g., DE VISSER et al. 1997). ELENA and LENSKI (1997) generated 225 genotypes of Escherichia coli carrying one, two, or three successive mutations and measured their fitness relative to an unmutated competitor. Several combinations of mutations exhibited significant interactions for fitness, but they displayed synergistic epistasis as often as they displayed antagonistic epistasis. Similar results were found in Aspergillus niger (DE VISSER et al. 1997). Recently, using five chromosomal regions containing visible recessive mutations in Drosophila melanogaster, WHITLOCK and BOURGUET (2000) found that the productivity showed a pattern of strong synergistic epistasis. This pattern was not observed, though, for male mating success. In the same manner, using chemically induced deleterious mutations, RIVERO et al. (2003) found that synergistic epistasis occurred for longevity, but not for egg production in the parasitic wasp Nasonia vitripennis. By combing the literature, DE VISSER and HOEKSTRA (1998) studied the distribution of a variety of quantitative characters related to fitness in plants. Fitness-related traits show almost exclusively negative skewness, suggesting the existence of synergistic epistasis among deleterious alleles. …