Summary 1.Pleiotropic effects associated with genes endowing resistance to herbicides are generally predicted to reduce plant fitness. Quantifying these effects is necessary to develop management strategies against herbicide-resistant weeds. We assessed the pleiotropic effects associated with three mutant alleles of the herbicide target enzyme acetyl-coenzyme A carboxylase (ACCase) on plant growth and seed production in black-grass Alopecurus myosuroides . 2. In each of two field experiments, black-grass populations segregating for Leu-1781 (five populations), Asn-2041 (three populations) or Gly-2078 (two populations) ACCase were produced to obtain several distinct, homogenized genetic backgrounds and to permit reliable comparisons among wild-type, heterozygous and homozygous mutant ACCase plants grown in competition with a wheat crop. 3. No significant differences from wild-type plants in vegetative biomass, height and seed production were observed in Leu-1781 or Asn-2041 ACCase plants. 4. Over both experiments, homozygous Gly-2078 ACCase plants displayed a significant reduction in biomass (42%), height (6%) and seed production (36%). Reduction varied with the segregating population and between field experiments. 5. Synthesis and applications . Our work illustrates the variation in fitness cost depending on the resistance gene, the plant genetic background and the environment. This underlines the necessity to identify the resistance gene(s) present in a weed population before designing resistance-management strategies. Competitive crops should be effective against Gly-2078 ACCase plants. The effect of resistant ACCase alleles on seed survival and germination needs to be studied in order to develop cultural practices creating or maximizing fitness costs in resistant plants. However, the variation of fitness cost with the environment and the weed population, as well as the likely absence of fitness cost associated with resistance genes such as Leu-1781 ACCase, renders the success of specific cultural control practices uncertain. A solution could be a weed control programme maximizing the diversity of cultural practices and including anti-resistance cultural practices to avoid or reduce selection for resistant ACCase alleles.
We investigated the molecular bases for resistance to several classes of herbicides that bind tubulins in green foxtail (Setaria viridis L. Beauv.). We identified two a-and two b-tubulin genes in green foxtail. Sequence comparison between resistant and sensitive plants revealed two mutations, a leucine-to-phenylalanine change at position 136 and a threonine-to-isoleucine change at position 239, in the gene encoding a2-tubulin. Association of mutation at position 239 with herbicide resistance was demonstrated using near-isogenic lines derived from interspecific pairings between green foxtail and foxtail millet (Setaria italica L. Beauv.), and herbicide sensitivity bioassays combined with allele-specific PCR-mediated genotyping. Association of mutation at position 136 with herbicide resistance was demonstrated using herbicide sensitivity bioassays combined with allele-specific PCR-mediated genotyping. Both mutations were associated with recessive cross resistance to dinitroanilines and benzoic acids, no change in sensitivity to benzamides, and hypersensitivity to carbamates. Using three-dimensional modeling, we found that the two mutations are adjacent and located into a region involved in tubulin dimer-dimer contact. Comparison of three-dimensional a-tubulin models for organisms with contrasted sensitivity to tubulin-binding herbicides enabled us to propose that residue 253 and the vicinity of the side chain of residue 251 are critical determinants for the differences in herbicide sensitivity observed between organisms, and that positions 16, 24, 136, 239, 252, and 268 are involved in modulating sensitivity to these herbicides.
The cDNAs encoding chloroplastic acetyl-CoA carboxylase (ACCase, EC 6.4.1.2) from three lines of Setaria viridis (L. Beauv.) resistant or sensitive to sethoxydim, and from one sethoxydim-sensitive line of Setaria italica (L. Beauv.) were cloned and sequenced. Sequence comparison revealed that a single isoleucine-leucine substitution discriminated ACCases from sensitive and resistant lines. Using near-isogenic lines of S. italica derived from interspecific hybridisation, we demonstrated that the transfer of the S. viridis mutant ACCase allele into a sethoxydim-sensitive S. italica line conferred resistance to this herbicide. We confirmed this result using allele-specific polymerase chain reaction and showed that a single copy of the mutant allele is sufficient to confer resistance to sethoxydim. We conclude that a mutant allele of chloroplastic ACCase encoding a leucine residue instead of an isoleucine residue at position 1780 is a major gene of resistance to sethoxydim.
It is often alleged that mutations conferring herbicide resistance have a negative impact on plant fitness. A mutant ACCase1781 allele endowing resistance to the sethoxydim herbicide was introgressed from a resistant green foxtail (Setaria viridis (L.) Beauv) population into foxtail millet (S. italica (L.) Beauv.). (1) Better and earlier growth of resistant plants was observed in a greenhouse cabinet. (2) Resistant plants of the advanced BC7 backcross generation showed more vigorous juvenile growth in the field, earlier flowering, more tillers and higher numbers of grains than susceptible plants did, especially when both genotypes were grown in mixture, but their seeds were lighter than susceptible seeds. (3) Field populations originating from segregating hybrids had the expected allele frequencies under normal growth conditions, but showed a genotype shift toward an excess of homozygous resistant plants within 3 years in stressful conditions. Lower seed size, lower germination rate and perhaps unexplored differences in seed longevity and predation could explain how the resistant plants have the same field fitness over the whole life cycle as the susceptible ones although they produce more seeds. More rapid growth kinetics probably accounted for higher fitness of the resistant plants in adverse conditions. The likelihood of a linkage with a beneficial gene is discussed versus the hypothesis of a pleiotropic effect of the ACCase resistance allele. It is suggested that autogamous species like Setaria could not develop a resistant population without the help of a linkage with a gene producing a higher fitness.
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