Skip to main content
SpringerLink
Log in

No fitness cost of glyphosate resistance endowed by massive EPSPS gene amplification in Amaranthus palmeri

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Amplification of the EPSPS gene has been previously identified as the glyphosate resistance mechanism in many populations of Amaranthus palmeri, a major weed pest in US agriculture. Here, we evaluate the effects of EPSPS gene amplification on both the level of glyphosate resistance and fitness cost of resistance. A. palmeri individuals resistant to glyphosate by expressing a wide range of EPSPS gene copy numbers were evaluated under competitive conditions in the presence or absence of glyphosate. Survival rates to glyphosate and fitness traits of plants under intra-specific competition were assessed. Plants with higher amplification of the EPSPS gene (53-fold) showed high levels of glyphosate resistance, whereas less amplification of the EPSPS gene (21-fold) endowed a lower level of glyphosate resistance. Without glyphosate but under competitive conditions, plants exhibiting up to 76-fold EPSPS gene amplification exhibited similar height, and biomass allocation to vegetative and reproductive organs, compared to glyphosate susceptible A. palmeri plants with no amplification of the EPSPS gene. Both the additive effects of EPSPS gene amplification on the level of glyphosate resistance and the lack of associated fitness costs are key factors contributing to EPSPS gene amplification as a widespread and important glyphosate resistance mechanism likely to become much more evident in weed plant species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

ALS:

Acetolactate synthase

DAT:

Days after treatment

EPSPS:

5-Enolpyruvylshikimate-3-phosphate synthase

LD50 :

Lethal dose fifty

PCR:

Polymerasa chain reaction

R:

Glyposate resistant

S:

Glyphosate susceptible

References

  • Ashigh J, Tardif F (2007) An Ala205Val substitution in acetohydroxyacid synthase of Eastern black nightshade (Solanum ptychanthum) reduces sensitivity to herbicides and feedback inhibition. Weed Sci 55:558–565

    Article  CAS  Google Scholar 

  • Ashigh J, Tardif FJ (2009) An amino acid substitution at position 205 of acetohydroxyacid synthase reduces fitness under optimal light in resistant populations of Solanum ptychanthum. Weed Res 49:479–489

    Article  CAS  Google Scholar 

  • Ashigh J, Tardif FJ (2011) Water and temperature stress impact fitness of acetohydroxyacid synthase-inhibiting herbicide-resistant populations of eastern black nightshade (Solanum ptychanthum). Weed Sci 59:341–348

    Article  CAS  Google Scholar 

  • Baerson SR, Rodriguez DJ, Tran M, Feng YM, Biest NA, Dill GM (2002) Glyphosate-resistant goosegrass. Identification of a mutation in the target enzyme 5-enolpyruvylshikimate-3-phosphate synthase. Plant Physiol 129:1265–1275

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bekaert M, Edger PP, Hudson CM, Pires JC, Conant GC (2012) Metabolic and evolutionary costs of herbivory defense: systems biology of glucosinolate synthesis. New Phytol 196:596–605

    Article  CAS  PubMed  Google Scholar 

  • Bergelson J, Purrington CB (1996) Surveying patterns in the cost of resistance in plants. Am Nat 148:536–558

    Article  Google Scholar 

  • Cohan FM, King EC, Zawadzki P (1994) Amelioration of the deleterious pleiotropic effects of an adaptive mutation in Bacillus subtilis. Evolution 48:81–95

    Article  Google Scholar 

  • Culpepper AS, Grey TL, Vencill WK, Kichler JM, Webster TM, Brown SM, York AC, Davis JW, Hanna WW (2006) Glyphosate-resistant Palmer amaranth (Amaranthus palmeri) confirmed in Georgia. Weed Sci 54:620–626

    Article  CAS  Google Scholar 

  • Field LM, Foster SP (2002) Amplified esterase genes and their relationship with other insecticide resistance mechanisms in English field populations of the aphid, Myzus persicae (Sulzer). Pest Manag Sci 58:889–894

    Article  CAS  PubMed  Google Scholar 

  • Fisher RA (1928) The possible modification of the response of the wild type to recurrent mutations. Am Nat 62:115–126

    Article  Google Scholar 

  • Fisher RA (1958) The genetical theory of natural selection. Dover Publications, New York

    Google Scholar 

  • Gaines TA, Zhang W, Wang D, Bukun B, Chisholm ST, Shaner DL, Nissen SJ, Patzoldt WL, Tranel PJ, Culpepper AS, Grey TL, Webster TM, Vencill WK, Sammons RD, Jiang J, Preston C, Leach JE, Westra P (2010) Gene amplification confers glyphosate resistance in Amaranthus palmeri. Proc Natl Acad Sci USA 107:1029–1034

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gaines TA, Shaner DL, Ward SM, Leach JE, Preston C, Westra P (2011) Mechanism of resistance of evolved glyphosate-resistant Palmer amaranth (Amaranthus palmeri). J Agric Food Chem 59:5886–5889

    Article  CAS  PubMed  Google Scholar 

  • Gaines TA, Wright AA, Molin WM, Lorentz L, Riggins CW, Tranel PJ, Beffa R, Westra P, Powles SB (2013) Identification of genetic elements associated with EPSPS gene amplification. Plos One. doi:101371/journalpone0065819 (in press)

    Google Scholar 

  • Gassmann AJ (2005) Resistance to herbicide and susceptibility to herbivores: environmental variation in the magnitude of an ecological trade-off. Oecologia 145:575–585

    Article  PubMed  Google Scholar 

  • Ge X, d’Avignon DA, Ackerman JJH, Sammons RD (2010) Rapid vacuolar sequestration: the horseweed glyphosate resistance mechanism. Pest Manag Sci 66:345–348

    CAS  PubMed Central  PubMed  Google Scholar 

  • Guillemaud T, Raymond M, Tsagkarakou A, Bernard C, Rochard P, Pasteur N (1999) Quantitative variation and selection of esterase gene amplification in Culex pipiens. Heredity 83:87–99

    Article  CAS  PubMed  Google Scholar 

  • Heap I (2013) The international survey of herbicide resistant weeds. Available in www.weedscience.com. Accessed May 2, 2013

  • Herms DA, Mattson WJ (1992) The dilemma of plants––to grow or defend. Q Rev Biol 67:283–335

    Article  Google Scholar 

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

    CAS  Google Scholar 

  • Lenormand T, Guillemaud T, Bourguet D, Raymond M (1998) Appearance and sweep of a gene duplication: adaptive response and potential for new functions in the mosquito Culex pipiens. Evolution 52:1705–1712

    Article  Google Scholar 

  • Li M, Yu Q, Han H, Vila-Aiub MM, Powles SB (2013) ALS herbicide resistance mutations in Raphanus raphanistrum: evaluation of pleiotropic effects on vegetative growth and ALS activity. Pest Manag Sci 69:689–695

    Article  CAS  PubMed  Google Scholar 

  • Lorraine-Colwill DF, Powles SB, Hawkes TR, Hollinshead PH, Warner SAJ, Preston C (2003) Investigations into the mechanism of glyphosate resistance in Lolium rigidum. Pestic Biochem Physiol 74:62–72

    Article  Google Scholar 

  • Menchari Y, Chauvel B, Darmency H, Delye C (2008) Fitness costs associated with three mutant acetyl-coenzyme A carboxylase alleles endowing herbicide resistance in black-grass Alopecurus myosuroides. J Appl Ecol 45:939–947

    Article  Google Scholar 

  • Michitte P, De Prado R, Espinoza N, Ruiz-Santaella JP, Gauvrit C (2007) Mechanisms of resistance to glyphosate in a ryegrass (Lolium multiflorum) biotype from Chile. Weed Sci 55:435–440

    Article  CAS  Google Scholar 

  • Nilsson AI, Zorzet A, Kanth A, Dahlström S, Berg OG, Andersson DI (2006) Reducing the fitness cost of antibiotic resistance by amplification of initiator tRNA genes. Proc Natl Acad Sci USA 103:6976–6981

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Paris M, Roux F, Berard A, Reboud X (2008) The effects of the genetic background on herbicide resistance fitness cost and its associated dominance in Arabidopsis thaliana. Heredity 101:499–506

    Article  CAS  PubMed  Google Scholar 

  • Powles SB (2010) Gene amplification delivers glyphosate-resistant weed evolution. Proc Natl Acad Sci USA 107:955–956

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Powles SB, Yu Q (2010) Evolution in action: plants resistant to herbicides. Annu Rev Plant Biol 61:317–347

    Article  CAS  PubMed  Google Scholar 

  • Purrington CB, Bergelson J (1999) Exploring the physiological basis of costs of herbicide resistance in Arabidopsis thaliana. Am Nat 154:S82–S91

    Article  Google Scholar 

  • Raymond M, Poulin E, Boiroux V, Dupont E, Pasteur N (1993) Stability of insecticide resistance due to amplification of esterase genes in Culex pipiens. Heredity 70:301–307

    Article  CAS  Google Scholar 

  • Roux F, Gasquez J, Reboud X (2004) The dominance of the herbicide resistance cost in several Arabidopsis thaliana mutant lines. Genetics 166:449–460

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shaner DL, Nadler-Hassar T, Henry WB, Koger CH (2005) A rapid in vivo shikimate accumulation assay with excised leaf discs. Weed Sci 53:769–774

    Article  CAS  Google Scholar 

  • Steinrücken HC, Amrhein N (1980) The herbicide glyphosate is a potent inhibitor of 5-enolpyruvyl-shikimic acid-3-phosphate synthase. Biochem Biophys Res Commun 94:1207–1212

    Article  PubMed  Google Scholar 

  • Stoebel DM, Dean AM, Dykhuizen DE (2008) The cost of expression of Escherichia coli lac operon proteins is in the process, not in the products. Genetics 178:1653–1660

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tardif FJ, Rajcan I, Costea M (2006) A mutation in the herbicide target site acetohydroxyacid synthase produces morphological and structural alterations and reduces fitness in Amaranthus powellii. New Phytol 169:251–264

    Article  CAS  PubMed  Google Scholar 

  • Uyenoyama M (1986) Pleiotropy and the evolution of genetic systems conferring resistance to pesticides. In: Glass E (ed) Pesticide resistance strategies and tactics for management. National Academy of Sciences, Washington, pp 207–221

    Google Scholar 

  • Vila-Aiub MM, Neve P, Powles SB (2005) Resistance cost of a cytochrome P450 herbicide metabolism mechanism but not an ACCase target site mutation in a multiple resistant Lolium rigidum population. New Phytol 167:787–796

    Article  CAS  PubMed  Google Scholar 

  • Vila-Aiub MM, Neve P, Powles SB (2009a) Evidence for an ecological cost of enhanced herbicide metabolism in Lolium rigidum. J Ecol 97:772–780

    Article  Google Scholar 

  • Vila-Aiub MM, Neve P, Powles SB (2009b) Fitness costs associated with evolved herbicide resistance alleles in plants. New Phytol 184:751–767

    Article  CAS  PubMed  Google Scholar 

  • Vila-Aiub MM, Neve P, Roux F (2011) A unified approach to the estimation and interpretation of resistance costs in plants. Heredity 107:386–394

    CAS  PubMed Central  PubMed  Google Scholar 

  • Vila-Aiub MM, Balbi MC, Distéfano AJ, Fernandez L, Hopp E, Yu Q, Powles SB (2012) Glyphosate resistance in perennial Sorghum halepense (Johnson grass) endowed by reduced glyphosate translocation and leaf uptake. Pest Manag Sci 68:430–436

    Article  CAS  PubMed  Google Scholar 

  • Wagner A (2005) Energy constraints on the evolution of gene expression. Mol Biol Evol 22:1365–1374

    Article  CAS  PubMed  Google Scholar 

  • Wakelin AM, Preston C (2006) A target-site mutation is present in a glyphosate-resistant Lolium rigidum population. Weed Res 46:432–440

    Article  CAS  Google Scholar 

  • Wang T, Picard JC, Tian X, Darmency H (2010) A herbicide-resistant ACCase 1781 Setaria mutant shows higher fitness than wild type. Heredity 105:394–400

    Article  CAS  PubMed  Google Scholar 

  • Wang W, Xia H, Yang X, Xu T, Si HJ, Cai XX, Wang F, Su J, Snow AA, Lu BR (2013) A novel 5-enolpyruvoylshikimate-3-phosphate (EPSP) synthase transgene for glyphosate resistance stimulates growth and fecundity in weedy rice (Oryza sativa) without herbicide. New Phytol. doi:10.1111/nph.12428

    PubMed Central  Google Scholar 

  • Ward SM, Webster TM, Steckel LE (2013) Palmer amaranth (Amaranthus palmeri): a review. Weed Technol 27:12–27

    Article  Google Scholar 

  • Weiner J (2004) Allocation, plasticity and allometry in plants. Perspect Plant Ecol Evol Syst 6:207–215

    Article  Google Scholar 

  • Weiner J, Campbell LG, Pino J, Echarte L (2009) The allometry of reproduction within plant populations. J Ecol 97:1220–1233

    Article  Google Scholar 

  • Yu Q, Han H, Vila-Aiub MM, Powles SB (2010) AHAS herbicide resistance endowing mutations: effect on AHAS functionality and plant growth. J Exp Bot 61:3925–3934

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Dr. Pedro E. Gundel (IFEVA-CONICET) for his valuable help in the statistical analyses. This work was supported by a grant from the Grains Research and Development Corporation (GRDC), Australia.

Author information

Authors and Affiliations

  1. Australian Herbicide Resistance Initiative (AHRI)-School of Plant Biology, University of Western Australia (UWA), Crawley, WA, Australia

    Martin M. Vila-Aiub, Sou S. Goh, Todd A. Gaines, Heping Han, Roberto Busi, Qin Yu & Stephen B. Powles

  2. Facultad de Agronomía, Departamento de Ecología, IFEVA-CONICET, Universidad de Buenos Aires (UBA), Av. San Martín 4453, 1417, Buenos Aires, Argentina

    Martin M. Vila-Aiub

Authors
  1. Martin M. Vila-Aiub
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sou S. Goh
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Todd A. Gaines
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Heping Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Roberto Busi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Qin Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Stephen B. Powles
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Martin M. Vila-Aiub.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vila-Aiub, M.M., Goh, S.S., Gaines, T.A. et al. No fitness cost of glyphosate resistance endowed by massive EPSPS gene amplification in Amaranthus palmeri . Planta 239, 793–801 (2014). https://doi.org/10.1007/s00425-013-2022-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-013-2022-x

Keywords

Search

Navigation