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Recurrent selection with reduced herbicide rates results in the rapid evolution of herbicide resistance in Lolium rigidum

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Abstract

There has been much debate regarding the potential for reduced rates of herbicide application to accelerate evolution of herbicide resistance. We report a series of experiments that demonstrate the potential for reduced rates of the acetyl-co enzyme A carboxylase (ACCase)-inhibiting herbicide diclofop-methyl to rapidly select for resistance in a susceptible biotype of Lolium rigidum. Thirty-six percent of individuals from the original VLR1 population survived application of 37.5 g diclofop-methyl ha−1 (10% of the recommended field application rate). These individuals were grown to maturity and bulk-crossed to produce the VLR1 low dose-selected line VLR1 (0.1). Subsequent comparisons of the dose-response characteristics of the original and low dose-selected VLR1 lines demonstrated increased tolerance of diclofop-methyl in the selected line. Two further rounds of selection produced VLR1 lines that were resistant to field-applied rates of diclofop-methyl. The LD50 (diclofop-methyl dose required to cause 50% mortality) of the most resistant line was 56-fold greater than that of the original unselected VLR1 population, indicating very large increases in mean population survival after three cycles of selection. In vitro ACCase inhibition by diclofop acid confirmed that resistance was not due to an insensitive herbicide target-site. Cross-resistance studies showed increases in resistance to four herbicides: fluazifop-P-butyl, haloxyfop-R-methyl, clethodim and imazethapyr. The potential genetic basis of the observed response and implications of reduced herbicide application rates for management of herbicide resistance are discussed.

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References

  • Brown AC, Moss SR, Wilson ZA, Field LN (2002) An isoleucine to leucine substitution in the ACCase of Alopecurus myosuroides (black-grass) is associated with resistance to the herbicide sethoxydim. Pest Biochem Physiol 72:160–168

    Google Scholar 

  • Burnet MWM, Hart Q, Holtum JAM, Powles SB (1994) Resistance to nine herbicide classes in a population of rigid ryegrass (Lolium rigidum). Weed Sci 42:369–377

    Google Scholar 

  • Christopher JT, Powles SB, Holtum JAM, Liljegren DR (1991) Cross resistance to herbicides in annual ryegrass (Lolium rigidum): II chlorsulfuron resistance involves a wheat-like detoxification system. Plant Physiol 95:1036–1043

    Google Scholar 

  • Cocker KM, Moss SR, Coleman JOD (1999) Multiple mechanisms of resistance to fenoxaprop-P-ethyl in United Kingdom and other European populations of herbicide-resistant Alopecurus myosuroides (black-grass). Pest Biochem Physiol 65:169–180

    Google Scholar 

  • Daborn PJ, Yen JL, Bogwitz MR, Le Goff G, Feil E, Jeffers S, Tijet N, Perry T, Heckel D, Batterham P, Feyereisen R, Wilson TG, Ffrench-Constant RH (2002) A single P450 allele associated with insecticide resistance in Drosophila. Science 297:2253–2256

    Google Scholar 

  • Darmency H (1994) Genetics of herbicide resistance in weeds and crops. In: Powles SB, Holtum JAM (eds) Herbicide resistance in plants: biology and biochemistry. CRC, Baton Rouge, pp 263–297

    Google Scholar 

  • DeGennaro FP, Weller SC (1984) Differential susceptibility of field bindweed (Convolvulus arvensis) biotypes to glyphosate. Weed Sci 32:472–476

    Google Scholar 

  • Delye C, Wang TY, Darmency H (2002) An isoleucine-leucine substitution in chloroplastic acetyl-CoA carboxylase from green foxtail (Setaria viridis L. Beauv.) is responsible for resistance to the cyclohexanedione herbicide sethoxydim. Planta 214:421–427

    Google Scholar 

  • Delye C, Zhang X, Chalopin C, Michel S, Powles SB (2003) An isoleucine residue within the carboxyl-transferase domain of multidomain acetyl-coenzyme A carboxylase is a major determinant of sensitivity to aryloxyphenoxypropionate but not to cyclohexanedione inhibitors. Plant Physiol 132:1716–1723

    Google Scholar 

  • Diggle AJ, Neve P (2001) The population dynamics and genetics of herbicide resistance—a modeling approach. In: Powles SB, Shaner DL (eds) Herbicide resistance and world grains. CRC, Baton Rouge, pp 61–99

    Google Scholar 

  • Diggle AD, Neve PB, Smith FP (2003) Herbicides used in combination can reduce the probability of herbicide resistance in finite weed populations. Weed Res 43:371–382

    Google Scholar 

  • Ellis M, Kay QON (1975) Genetic variation in herbicide resistance in scentless mayweed (Tripleurospermum inodorum (L.) Schulz Bip.) III. Selection for increased resistance to ioxynil, MCPA and simazine. Weed Res 15:327–333

    Google Scholar 

  • Faulkner JS (1974) Heritability of paraquat tolerance in Lolium perenne L. Euphytica 23:281–288

    Google Scholar 

  • Ffrench-Constant RH, Daborn PJ, Le Goff G (2004) The genetics and genomics of insecticide resistance. Trends Genet 20:163–170

    Google Scholar 

  • Georghiou GP, Taylor CE (1986) Factors influencing the evolution of resistance. In: Metcalf RL, Luckmann WH (eds) Pesticide resistance: strategies and tactics or management. National Academy Press, Washington D.C., pp 157–169

  • Gressel J (1995) Catch 22—mutually exclusive strategies for delaying/preventing quantitatively vs. monogenically inherited resistances. In: Ragsdale NN, Kearney PC, Plimmer JR (eds) Options 2000. American Chemical Society, Washington, D.C., pp 330–345

    Google Scholar 

  • Gressel J (2002) Molecular biology of weed control. Taylor & Francis, London

    Google Scholar 

  • Gressel J, Segel LA (1978) The paucity of plants evolving genetic resistance to herbicides: possible reasons and implications. J Theor Biol 75:349–371

    Google Scholar 

  • Groeters FR, Tabashnik BE (2000) Roles of selection intensity, major genes and minor genes in evolution of insecticide resistance. J Econ Entomol 93:1580–1587

    Google Scholar 

  • Hall LM, Moss SR, Powles SR (1997) Mechanisms of resistance to aryloxyphenoxypropionate herbicides in two resistant biotypes of Alopecurus myosuroides (blackgrass): herbicide metabolism as a cross-resistance mechanism. Pest Biochem Physiol 57:87–98

    Google Scholar 

  • Holliday RJ, Putwain PD (1980) Evolution of herbicide resistance in Senecio vulgaris: variation in susceptibility to simazine between and within populations. J Appl Ecol 17:779–791

    Google Scholar 

  • Jasieniuk M, Brule-Babel AL, Morrison IA (1996) The evolution and genetics of herbicide resistance. Weed Sci 44:176–193

    CAS  Google Scholar 

  • Jia MH, Larossa RA, Lee JM, Rafalski A, Derose A, Gonye G, Xue Z (2000) Global expression profiling of yeast treated with an inhibitor of amino acid biosynthesis, sulfometuron-methyl. Physiol Genome 3:83–92

    Google Scholar 

  • Lande R (1983) The response to selection on major and minor mutations affecting a metrical trait. Heredity 50:47–65

    Google Scholar 

  • Letouze A, Gasquez J (2003) Enhanced activity of several herbicide-degrading enzymes: a suggested mechanism responsible for multiple resistance in blackgrass (Alopecurus myosuroides Huds.). Agronomie 23:601–608

    Google Scholar 

  • Lipsitch M, Levin BR (1997) The population dynamics of antimicrobial chemotherapy. Antimicrob Agents Chemother 41:363–373

    Google Scholar 

  • Llewellyn RS, Powles SB (2001) High levels of herbicide resistance in rigid ryegrass (Lolium rigidum) in the wheat belt of Western Australia. Weed Technol 15:242–248

    Google Scholar 

  • Macnair MR (1991) Why the evolution of resistance to anthropogenic toxins normally involves major gene changes: the limits to natural selection. Genetica 84:213–219

    Google Scholar 

  • Maxwell BD, Mortimer AM (1994) Selection for herbicide resistance. In: Powles SB, Holtum JAM (eds) Herbicide resistance in plants: biology and biochemistry. CRC, Baton Rouge, pp 1–27

    Google Scholar 

  • Maxwell BD, Roush ML, Radosevich SR (1990) Predicting the evolution and dynamics of herbicide resistance in weed populations. Weed Technol 4:2–13

    Google Scholar 

  • McKenzie JA (2000) The character or the variation: the genetic analysis of the insecticide-resistance phenotype. Bull Entomol Res 90:3–7

    Google Scholar 

  • McKenzie JA, Batterham P (1994) The genetic, molecular and phenotypic consequences of selection for insecticide resistance. Trends Ecol Evol 9:166–169

    Google Scholar 

  • Neve P, Diggle AJ, Smith FP, Powles SB (2003) Simulating evolution of glyphosate resistance in Lolium rigidum I: population biology of a rare resistance trait. Weed Res 43:404–417

    Google Scholar 

  • Oleksiak MF, Churchill GA, Crawford DL (2002) Variation in gene expression within and among populations. Nat Genet 32:261–266

    Article  CAS  PubMed  Google Scholar 

  • Orr HA, Coyne JA (1992) The genetics of adaptation: a reassessment. Am Nat 140:725–742

    Google Scholar 

  • Patzoldt WL, Tranel PJ, Hager AG (2002) Variable herbicide responses among Illinois waterhemp (Amaranthus rudis and A. tuberculatus) populations. Crop Prot 21:707–712

    Google Scholar 

  • Pedra JHF, McIntyre LM, Scharf ME, Pittendrigh BR (2004) Genome-wide transcription profile of field- and laboratory-selected dichlorodiphenyltrichloroethane (DDT)-resistant Drosophila. Proc Natl Acad Sci USA 101:7034–7039

    Google Scholar 

  • Powles SB, Shaner DL (2001) Herbicide resistance and world grains. CRC, Baton Rouge

    Google Scholar 

  • Preston C, Tardif FJ, Christopher JT, Powles SB (1996) Multiple resistance to dissimilar herbicide chemistries in a biotype of Lolium rigidum due to enhanced activity of several herbicide degrading enzymes. Pest Biochem Physiol 54:123–134

    Google Scholar 

  • Price SC, Hill JE, Allard RW (1983) Genetic variability for herbicide reaction in plant populations. Weed Sci 31:652–657

    Google Scholar 

  • Price SC, Allard RW, Hill JE, Naylor J (1985) Associations between discrete genetic loci and genetic variability for herbicide reaction in plant populations. Weed Sci 33:650–653

    Google Scholar 

  • Roush RT, McKenzie JA (1987) Ecological genetics of insecticide and acaricide resistance. Annu Rev Entomol 32:361–380

    Google Scholar 

  • Schenk PM, Kazan K, Wilson I, Anderson JP, Richmond T, Somerville SC, Manners JM (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc Natl Acad Sci USA 97:11655–11660

    Article  CAS  PubMed  Google Scholar 

  • Seefeldt SS, Fuerst EP, Gealy DR, Shukla A, Irzyk GA, Devine M (1996) Mechanisms of resistance to diclofop of two wild oat (Avena fatua) biotypes from the Willamette Valley of Oregon. Weed Sci 44:776–781

    Google Scholar 

  • Shaw MW (2000) Models of the effects of dose heterogeneity and escape on selection pressure for pesticide resistance. Phytopathology 90:333–339

    Google Scholar 

  • Steva H (1994) Evaluating anti-resistance strategies for control of Uncinula necator. In: Heaney SP, Slawson D, Holloman DW, Smith M, Russell PE, Parry DW (eds) Fungicide resistance. British Crop Protection Council, Farnham, pp 59–66

    Google Scholar 

  • Tabashnik TE, Gould F, Carriere Y (2004) Delaying evolution of insect resistance to transgenic crops by decreasing dominance and heritability. J Evol Biol 17:904–912

    Google Scholar 

  • Tardif FJ, Holtum JAM, Powles SB (1993) Occurrence of a herbicide-resistant acetyl-coenzyme A carboxylase mutant in annual ryegrass (Lolium rigidum) selected by sethoxydim. Planta 190:176–181

    Google Scholar 

  • Uyenoyama MK (1986) Pleiotropy and the evolution of genetic systems conferring resistance to pesticides. In: Metcalf RL, Luckmann WH (eds) Pesticide resistance: strategies and tactics for management. National Academy Press, Washington D.C., pp 207–221

  • Via S (1986) Quantitative genetic models and the evolution of pesticide resistance. In: Metcalf RL, Luckmann WH (eds) Pesticide resistance: strategies and tactics for management. National Academy Press, Washington D.C., pp 222–235

  • Zagnitko O, Jelenska J, Tevzadze G, Haselkorn R, Gornicki P (2001) An isoleucine/leucine residue in the carboxyl transferase domain of acetyl-CoA carboxylase is critical for interaction with aryloxyphenoxypropionate and cyclohexanedione inhibitors. Proc Natl Acad Sci USA 98:6617–6622

    Google Scholar 

Download references

Acknowledgements

The Western Australian Herbicide Resistance Initiative (WAHRI) is funded by the Grains Research and Development Corporation of Australia. The authors are indebted to Mechelle Owen and other WAHRI staff for technical assistance. Valuable comments on an earlier version of this manuscript were provided by J.A. McKenzie and X. Reboud.

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Correspondence to Paul Neve.

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Communicated by H.H. Geiger

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Neve, P., Powles, S. Recurrent selection with reduced herbicide rates results in the rapid evolution of herbicide resistance in Lolium rigidum. Theor Appl Genet 110, 1154–1166 (2005). https://doi.org/10.1007/s00122-005-1947-2

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