Skip to main content

Advertisement

Log in

Transgene escape and persistence in an agroecosystem: the case of glyphosate-resistant Brassica rapa L. in central Argentina

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Brassica rapa L. is an annual Brassicaceae species cultivated for oil and food production, whose wild form is a weed of crops worldwide. In temperate regions of South America and especially in the Argentine Pampas region, this species is widely distributed. During 2014, wild B. rapa populations that escaped control with glyphosate applications by farmers were found in this area. These plants were characterized by morphology and seed acidic profile, and all the characters agreed with B. rapa description. The dose-response assays showed that the biotypes were highly resistant to glyphosate. It was also shown that they had multiple resistance to AHAS-inhibiting herbicides. The transgenic origin of the glyphosate resistance in B. rapa biotypes was verified by an immunological test which confirmed the presence of the CP4 EPSPS protein and by an event-specific GT73 molecular marker. The persistence of the transgene in nature was confirmed for at least 4 years, in ruderal and agrestal habitats. This finding suggests that glyphosate resistance might come from GM oilseed rape crops illegally cultivated in the country or as a seed contaminant, and it implies gene flow and introgression between feral populations of GM B. napus and wild B. rapa. The persistence and spread of the resistance in agricultural environments was promoted by the high selection pressure imposed by intensive herbicide usage in the prevalent no-till farming systems.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Agnihotri A, Prem D, Gupta K (2007) The chronicles of oil and meal quality improvement in oilseed rape. In: Gupta S (ed) Advances in botanical research, Volume 45: Rapeseed breeding. Academic Press - Elsevier Ltd, San Diego, pp 49–97

    Google Scholar 

  • Allainguillaume J, Alexander M, Bullock JM, Saunders M, Allender CJ, King G, Ford CS, Wilkinson MJ (2006) Fitness of hybrids between rapeseed (Brassica napus) and wild Brassica rapa in natural habitats. Mol Ecol 15:1175–1184. https://doi.org/10.1111/j.1365-294X.2006.02856.x

    Article  CAS  Google Scholar 

  • Allender CJ, King GJ (2010) Origins of the amphiploid species Brassica napus L. investigated by chloroplast and nuclear molecular markers. BMC Plant Biol 10:54. https://doi.org/10.1186/1471-2229-10-54

    Article  Google Scholar 

  • Aono M, Wakiyama S, Nagatsu M, Nakajima N, Tamaoki M, Kubo A, Saji H (2006) Detection of feral transgenic oilseed rape with multiple-herbicide resistance in Japan. Environ Biosaf Res 5:77–87. https://doi.org/10.1051/ebr:2006017

    Article  CAS  Google Scholar 

  • Aono M, Wakiyama S, Nagatsu M, Kaneko Y, Nishizawa T, Nakajima N, Tamaoki M, Kubo A, Saji H (2012) Seeds of a possible natural hybrid between herbicide-resistant Brassica napus and Brassica rapa detected on a riverbank in Japan. GM Crops 2:201–210. https://doi.org/10.4161/gmcr.2.3.18931

    Article  Google Scholar 

  • Busi R, Powles SB (2016) Transgenic glyphosate-resistant canola (Brassica napus) can persist outside agricultural fields in Australia. Agric Ecosyst Environ 220:28–34. https://doi.org/10.1016/j.agee.2015.12.028

    Article  Google Scholar 

  • Christoffoleti PJ, Galli AJB, Carvalho SJP, Moreira MS, Nicolai M, Foloni LL, Martins BAB, Ribeiro DN (2008) Glyphosate sustainability in South American cropping systems. Pest Manag Sci 64:422–427. https://doi.org/10.1002/ps.1560

    Article  CAS  Google Scholar 

  • Clay S, Johnson G (2002) Scouting for weeds. Crop Manag. https://doi.org/10.1094/CM-2002-1206-01-MA

  • Cobb A, Reade J (2010) Herbicides and plant physiology, 2nd edn. Wiley-Blackwell, Oxford

    Book  Google Scholar 

  • Crouch JH, Lewis BG, Lydiate DJ, Mithen R (1995) Genetic diversity of wild, weedy and cultivated forms of Brassica rapa. Heredity 74:491–496. https://doi.org/10.1038/hdy.1995.69

    Article  Google Scholar 

  • Devos Y, De Schrijver A, Reheul D (2008) Quantifying the introgressive hybridisation propensity between transgenic oilseed rape and its wild/weedy relatives. Environ Monit Assess 149:303–322. https://doi.org/10.1007/s10661-008-0204-y

    Article  Google Scholar 

  • Devos Y, Hails RS, Messéan A, Perry JN, Squire GR (2012) Feral genetically modified herbicide tolerant oilseed rape from seed import spills: are concerns scientifically justified? Transgenic Res 21:1–21. https://doi.org/10.1007/s11248-011-9515-9

    Article  CAS  Google Scholar 

  • Di Rienzo JA, Casanoves F, Balzarini MG, Gonzalez L, Tablada M, Robledo CW (2016) Infostat versión 2016. Grupo InfoStat, FCA-Universidad Nacional de Córdoba, Córdoba

    Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15. https://doi.org/10.2307/4119796

    Google Scholar 

  • Evans JA, Tranel PJ, Hager AG, Schutte B, Wu C, Chatman LA, Davis AS (2016) Managing the evolution of herbicide resistance. Pest Manag Sci 72:74–80. https://doi.org/10.1002/ps.4009

    Article  CAS  Google Scholar 

  • FAOSTAT (2016) Food and agriculture Organization of the United Nations. http://www.fao.org/faostat/en/. Accessed 19 Dec 2016

  • FitzJohn RG, Armstrong TT, Newstrom-Lloyd LE, Wilton AD, Cochrane M (2007) Hybridisation within Brassica and allied genera: evaluation of potential for transgene escape. Euphytica 158:209–230. https://doi.org/10.1007/s10681-007-9444-0

    Article  Google Scholar 

  • Friesen L, Nelson A, Van Acker R (2003) Evidence of contamination of pedigree canola (Brassica napus) seedlots in western Canada from genetically engineered herbicide resistance traits. Agron J 95:1342–1347

    Article  Google Scholar 

  • Gomez-Campo C, Prakash S (1999) Origin and domestication. In: Gomez-Campo C (ed) Biology of Brassica coenospecies. Elsevier Science, Madrid, pp 33–58

    Chapter  Google Scholar 

  • Gulden RH, Warwick SI, Thomas AG (2008) The biology of Canadian weeds. 137. Brassica napus L. and B. rapa L. Can J Plant Sci 88:951–996. https://doi.org/10.4141/CJPS07203

    Article  Google Scholar 

  • Gupta S, Pratap A (2007) History, origin, and evolution. In: Gupta S (ed) Advances in botanical research, Rapeseed breeding, first edit., vol 45. Academic Press - Elsevier Ltd., San Diego, pp 1–20

    Google Scholar 

  • Hall L, Topinka K, Huffman J, Davis L, Good A (2000) Pollen flow between herbicide-resistant Brassica napus is the cause of multiple-resistant B. napus volunteers. Weed Sci 48:688–694. https://doi.org/10.1614/0043-1745(2000)048[0688:PFBHRB]2.0.CO;2

    Article  CAS  Google Scholar 

  • Hecht M, Oehen B, Schulze J, Brodmann P, Bagutti C (2014) Detection of feral GT73 transgenic oilseed rape (Brassica napus) along railway lines on entry routes to oilseed factories in Switzerland. Environ Sci Pollut Res Int 21:1455–1465. https://doi.org/10.1007/s11356-013-1881-9

    Article  CAS  Google Scholar 

  • Ibarra FE (1937) Malezas más comunes del trigo y del lino. In: Almanaque del Ministerio de Agricultura, Buenos Aires, pp 405–410

  • IBPGR (International Board for Plant Genetic Resources) (1990) Descriptors for Brassica and Raphanus. Rome

  • INASE (Instituto Nacional de Semillas) (2007) Resolución 305/2007: Prohíbe la importación de colza portadora de eventos transgénicos no autorizados para su producción y comercialización en la República Argentina. http://wwwinasegovar/indexphp?option=com_remository&Itemid=102&func=fileinfo&id=547. Accessed 20 Mar 2017

  • INASE (Instituto Nacional de Semillas) (2016) Catálogo Nacional de Cultivares http://www.inase.gov.ar. Accessed 12 Dec 2016

  • Iniguez-Luy F, Federico M (2011) The genetics of Brassica napus. In: Schmidt R, Bancroft I (eds) Genetics and genomics of the Brassicaceae. Springer, Berlin, pp 33–66

    Google Scholar 

  • Iriarte L (2015) Cultivo de colza: comportamiento varietal y manejo, XXIII Congreso AAPRESID http://2015congresoaapresidorgar/wp-content/uploads/Iriarte-Liliana-Actapdf. Accessed 06 Mar 2016

  • Iriarte L, Valetti O (2008) Cultivo de Colza. Chacra Experimental Integrada Barrow, Convenio MAAyP-INTA, Tres Arroyos

    Google Scholar 

  • ISAAA (International Service for the Acquisition of Agri-Biotech Applications) (2016) Global status of commercialized biotech/GM crops: 2016. ISAAA brief no. 52. ISAAA, Ithaca

    Google Scholar 

  • Jorgensen R, Andersen B (1994) Spontaneous hybridization between oilseed rape (Brassica napus) and weedy B. campestris (Brassicaceae): a risk of growing genetically modified oilseed rape. Am J Bot 81:1620–1626

    Article  Google Scholar 

  • Knispel AL, McLachlan SM, Van Acker RC, Friesen LF (2008) Gene flow and multiple herbicide resistance in escaped canola populations. Weed Sci 56:72–80. https://doi.org/10.1614/WS-07-097.1

    Article  CAS  Google Scholar 

  • Kumar A, Salisbury PA, Gurung AM, Barbetti MJ (2015) Importance and origin. In: Kumar A, Banga SS, Meena PD, Kumar PR (eds) Brassica oilseeds: breeding and management. CABI International, Oxfordshire, pp 1–10

    Chapter  Google Scholar 

  • Linnaeus C (1753) Species plantarum, vol 2, p 666 http://wwwbiodiversitylibraryorg/item/13830#page/108/mode/1up. Accessed 20 Mar 2017

  • Martinez-Laborde JB (1999) Brassicaceae. In: Zuloaga FO, Morrone O (eds) Catálogo de las Plantas Vasculares de la Argentina. Dycotyledoneae Monogr Syst Bot Missouri Bot Gard 74:1–1246

    Google Scholar 

  • Marzocca A, Marisco O, Del Puerto O (1976) Manual de Malezas, 3rd edn. Hemisferio Sur, Buenos Aires

    Google Scholar 

  • Mazzara M, Grazioli E, Savini C, Van den Eede G (2007) Event specific method for the quantitation of oilseed rape line RT73 using real-time PCR. Italy

  • MinAgro (Ministerio de Agroindustria) (2016) Datos Abiertos Agroindustria. https://datos.magyp.gob.ar/. Accessed 12 Dec 2016

  • Monsanto Biotechnology Regulatory Sciences (2004) A recommended procedure for real-time quantitative TaqMan PCR for Roundup Ready® canola RT73

  • Mueller-Dombois D, Ellemberg H (1974) Aims and methods of vegetation ecology, 1st edn. Wiley, New York 547 p

    Google Scholar 

  • Mulligan G (1995) Key to the Brassicaceae (cruciferae) of Canada and Alaska. Agriculture Canada, Ottawa

    Google Scholar 

  • Nagaharu U (1935) Genome-analysis in Brassica with special reference to the experimental formation of B. napus and peculiar mode of fertilization. Japanese J Bot 7:389–452

    Google Scholar 

  • Pandolfo CE, Presotto A, Carbonell FT, Ureta S, Poverene M, Cantamutto M (2016) Transgenic glyphosate-resistant oilseed rape (Brassica napus) as an invasive weed in Argentina: detection, characterization, and control alternatives. Environ Sci Pollut Res. https://doi.org/10.1007/s11356-016-7670-5

  • Pascale N (1976) Colza. Su cultivo, mejoramiento y usos. In: Kugler W (ed), Enciclopedia Argentina de Agricultura y Jardineria – Tomo II. Editorial Acme (2da edicion), Buenos Aires

  • Patiño VM (1963) Plantas cultivadas y animales domésticos en América Equinoccial IV: Plantas introducidas. Editorial Imprenta Departamental, Cali

    Google Scholar 

  • Prakash S, Wu X, Bhat SR (2012) History, evolution, and domestication of Brassica crops. In: Plant breeding reviews. Wiley, Hoboken, pp 19–84

    Google Scholar 

  • R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna www.R-project.org

    Google Scholar 

  • Ritz C (2010) Toward a unified approach to dose-response modeling in ecotoxicology. Environ Toxicol Chem 29:220–229. https://doi.org/10.1002/etc.7/abstract

    Article  CAS  Google Scholar 

  • SAGPyA (Secretaría de Agricultura, Ganadería, Pesca y Alimentación) (1997) Solicitud de ensayo a campo de canola tolerante al herbicida glifosato. Resolución N° 228

  • Saji H, Nakajima N, Aono M, Tamaoki M, Kubo A, Wakiyama S, Hatase Y, Nagatsu M (2005) Monitoring the escape of transgenic oilseed rape around Japanese ports and roadsides. Environ Biosaf Res 4:217–222. https://doi.org/10.1051/ebr:2006003

    Article  CAS  Google Scholar 

  • Schafer MG, Ross AA, Londo JP, Burdick CA, Lee EH, Travers SE, Van de Water PK, Sagers CL (2011) The establishment of genetically engineered canola populations in the U.S. PLoS One 6:e25736. https://doi.org/10.1371/journal.pone.0025736

    Article  CAS  Google Scholar 

  • Schoenenberger N, D’Andrea L (2012) Surveying the occurrence of subspontaneous glyphosate-tolerant genetically engineered Brassica napus L. (Brassicaceae) along Swiss railways. Environ Sci Eur 24:23. https://doi.org/10.1186/2190-4715-24-23

    Article  Google Scholar 

  • Schulze J, Brodmann P, Oehen B, Bagutti C (2015) Low level impurities in imported wheat are a likely source of feral transgenic oilseed rape (Brassica napus L.) in Switzerland. Environ Sci Pollut Res 22:16936–16942. https://doi.org/10.1007/s11356-015-4903-y

    Article  Google Scholar 

  • Simard M-J, Légère A, Warwick SI (2006) Transgenic Brassica napus fields and Brassica rapa weeds in Quebec: sympatry and weed-crop in situ hybridization. Can J Bot 84:1842–1851. https://doi.org/10.1139/B06-135

    Article  CAS  Google Scholar 

  • Snapp SS, Swinton SM, Labarta R, Mutch D, Black JR, Leep R, Nyiraneza J, O’Neil K (2005) Evaluating cover crops for benefits, costs and performance within cropping system niches. Agron J 97(1):322–332. https://doi.org/10.2134/agronj2005.0322

  • Snow A, Andersen B, Jørgensen R (1999) Costs of transgenic herbicide resistance introgressed from Brassica napus into weedy B. rapa. Mol Ecol 8:605–615

    Article  Google Scholar 

  • Suwabe K, Iketani H, Nunome T, Kage T, Hirai M (2002) Isolation and characterization of microsatellites in Brassica rapa L. Theor Appl Genet 104:1092–1098. https://doi.org/10.1007/s00122-002-0875-7

    Article  CAS  Google Scholar 

  • Tenembaum J (1937) El Nabo. Su cultivo en el país. In: Almanaque del Ministerio de Agricultura, Buenos Aires, pp 329–334

  • Vila-Aiub MM, Vidal RA, Balbi MC, Gundel PE, Trucco F, Ghersa CM (2008) Glyphosate-resistant weeds of South American cropping systems: an overview. Pest Manag Sci 64:366–371. https://doi.org/10.1002/ps.1488

    Article  CAS  Google Scholar 

  • Warwick SI, Simard M-J, Légère A, Beckie HJ, Braun L, Zhu B, Mason P, Séguin-Swartz G, Stewart CN (2003) Hybridization between transgenic Brassica napus L. and its wild relatives: Brassica rapa L., Raphanus raphanistrum L., Sinapis arvensis L., and Erucastrum gallicum (Willd.) O.E. Schulz. Theor Appl Genet 107:528–539. https://doi.org/10.1007/s00122-003-1278-0

    Article  CAS  Google Scholar 

  • Warwick SI, Légère A, Simard M-J, James T (2008) Do escaped transgenes persist in nature? The case of an herbicide resistance transgene in a weedy Brassica rapa population. Mol Ecol 17:1387–1395. https://doi.org/10.1111/j.1365-294X.2007.03567.x

    Article  CAS  Google Scholar 

  • Wu C, Davis AS, Tranel PJ (2017) Limited fitness costs of herbicide-resistance traits in Amaranthus tuberculatus facilitate resistance evolution. Pest Manag Sci. https://doi.org/10.1002/ps.4706

  • Yoshimura Y, Beckie HJ, Matsuo K (2006) Transgenic oilseed rape along transportation routes and port of Vancouver in western Canada. Environ Biosaf Res 5:67–75. https://doi.org/10.1051/ebr:2006019

    Article  Google Scholar 

Download references

Acknowledgments

We thank El Diez, La Isaura, Morales, and La Sarita Co. for letting us conduct our research in their fields and for providing historical records of herbicide applications. We also extend our thanks to Damian Gopar, Agustín Bilbao, and Horacio Repetto for their valuable contributions; to BASF Argentina Co., in particular the assistance of Juan Pablo Migasso and Fabricio Mock; and to Ignacio Barragué and Franco Ruiz for helping in the assays. We also thank Noemí Fritz and Cámara Arbitral de Cereales Bahía Blanca for the analysis of grain oil content and fatty acid composition.

Funding

We gratefully acknowledge the National Research Council of Argentina (CONICET) for a fellowship to CEP. This work was supported by Agencia Nacional de Promoción Científica y Técnica (grant ANPCYT-PICT 2854).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Claudio E. Pandolfo.

Additional information

Responsible editor: Diane Purchase

Electronic supplementary material

ESM 1

(PDF 649 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pandolfo, C.E., Presotto, A., Carbonell, F.T. et al. Transgene escape and persistence in an agroecosystem: the case of glyphosate-resistant Brassica rapa L. in central Argentina. Environ Sci Pollut Res 25, 6251–6264 (2018). https://doi.org/10.1007/s11356-017-0726-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-017-0726-3

Keywords

Navigation