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Lack of Glyphosate Resistance Gene Transfer from Roundup Ready

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Lack of Glyphosate Resistance Gene Transfer from Roundup Ready Lack of Glyphosate Resistance Gene Transfer from Roundup Ready® Soybean to Bradyrhizobium japonicum under Field and Laboratory Conditions Laura Arango Isazaa, Katja Opelta, Tobias Wagnera,b, Elke Mattesa, Evi Biebera, Elwood O. Hatleyc, Greg Rothc, Juan Sanjuánd, Hans-Martin Fischere, Heinrich Sandermanna, Anton Hartmannf, and Dieter Ernsta,* a Institute of Biochemical Plant Pathology, Helmholtz Zentrum München – German Research Center for Environmental Health, D-85764 Neuherberg, Germany. Fax: +49 89 3187 3383. E-mail: [email protected] b Present address: Applied Biosystems, Frankfurter Strasse 129B, D-64293 Darmstadt, Germany c The Pennsylvania State University, Department of Crop and Soil Sciences, University Park, PA 16802, USA d Departamento de Microbiologia del Suelo y Sistemas Simbióticos, Estación Experimental del Zaidin, CSIC, Prof. Albareda 1, Granada, Spain e ETH, Institute of Microbiology, Wolfgang-Pauli-Str. 10, Zürich, Switzerland f Department Microbe-Plant Interactions, Helmholtz Zentrum München – German Research Center for Environmental Health, D-85764 Neuherberg, Germany * Author for correspondence and reprint requests Z. Naturforsch. 66 c, 595 – 604 (2011); received March 25/October 14, 2011 This paper is dedicated to the memory of the late Professor Dr. Heinrich Sandermann, former director of the Institute of Biochemical Plant Pathology, Helmholtz Zentrum München A fi eld study was conducted at the Russell E. Larson Agricultural Research Center to de- termine the effect of transgenic glyphosate-resistant soybean in combination with herbicide (Roundup) application on its endosymbiont Bradyrhizobium japonicum. DNA of bacteroids from isolated nodules was analysed for the presence of the transgenic 5-enolpyruvylshiki- mate-3-phosphate synthase (CP4-EPSPS) DNA sequence using polymerase chain reaction (PCR). To further assess the likelihood that the EPSPS gene may be transferred from the Roundup Ready® (RR) soybean to B. japonicum, we have examined the natural transfor- mation effi ciency of B. japonicum strain 110spc4. Analyses of nodules showed the presence of the transgenic EPSPS DNA sequence. In bacteroids that were isolated from nodules of transgenic soybean plants and then cultivated in the presence of glyphosate this sequence could not be detected. This indicates that no stable horizontal gene transfer (HGT) of the EPSPS gene had occurred under fi eld conditions. Under laboratory conditions, no natu- ral transformation was detected in B. japonicum strain 110spc4 in the presence of various amounts of recombinant plasmid DNA. Our results indicate that no natural competence state exists in B. japonicum 110spc4. Results from fi eld and laboratory studies indicate the lack of functional transfer of the CP4-EPSPS gene from glyphosate-tolerant soybean treat- ed with glyphosate to root-associated B. japonicum. Key words: Bradyrhizobium japonicum, Glyphosate, Horizontal Gene Transfer Introduction crops planted worldwide; http://www.fourwinds10. com/siterun_data/science_technology/dna_gmo/ The enormous success of agricultural gene tech- news.php?q=1235154563). However, the increased nology has raised concern about the spread of novel use of transgenic plants in addition to herbicide traits into the environment. In 2010, more than 148 selection pressure on the fi elds may facilitate a million hectares worldwide were planted with crops possible horizontal gene fl ow (Sandermann et al., possessing biotechnologically derived traits (http:// 1997; Wagner et al., 2008) and cause the selection www.transgen.de/anbau/eu_international/). Herbi- of spontaneous herbicide-resistant microorganisms. cide tolerance is the most frequent trait found in Horizontal gene transfer (HGT) requires the genetically modifi ed (GM) plants (80% of all GM bacterial cell to possess the ability to actively take © 2011 Verlag der Zeitschrift für Naturforschung, Tübingen · http://znaturforsch.com 596 L. A. Isaza et al. · Horizontal Gene Transfer from Transgenic Plants to Bacteria up and heritably integrate extracellular DNA into al., 2005). Inhibition of EPSPS prevents the plant its genome, i.e., to have the competence for natu- from synthesizing aromatic amino acids, causes ral transformation (Johnsborg et al., 2007). More shikimate accumulation, and consequently kills than 40 prokaryotic species, including many soil plants. and rhizosphere bacteria, have been described The basis for resistance to glyphosate in RR that undergo natural transformation (Lorenz and soybeans is the insertion of a transgene that origi- Wackernagel, 1994). However, it has been dem- nates from the Agrobacterium strain CP4 (CP4- onstrated that competent bacteria are able to EPSPS) and specifi es a glyphosate-insensitive integrate transgenic plant DNA only if homolo- EPSPS variant (Padgette et al., 1995). Molecular gous bacterial DNA sequences are present in the characterization studies determined that the ge- plant genome (de Vries and Wackernagel, 2002). netic insertion in the RR soybean line 40-3-2 con- Laboratory studies have shown that gene trans- tains part of the 35S promoter of the Caulifl ower fer from plants to bacterial strains harbouring the mosaic virus (35S-CaMV), sequences of the Pe- homologous gene, inactivated by a short deletion, tunia hybrida EPSPS chloroplast transit peptide facilitates the selection of recombinant bacterial (CTP), the CP4-EPSPS gene, and an intact 3’ clones (Gebhard and Smalla, 1998; Nielsen et al., non-translated region of the nopaline synthase 2001; de Vries and Wackernagel, 2002; Kay et al., gene (NOS 3’) (Padgette et al., 1995). 2002). Under natural conditions, theoretical cal- The promoter from the 35S-CaMV gene is a culations predicted a very low transformation strong constitutive promoter that is most widely frequency (2 · 10 – 17, 1 transformant per 2 · 1017 used for the expression of transgenes in plants bacteria) (Schlüter et al., 1995); nevertheless, it is (Schnurr and Guerra, 2000). The effi cient ex- presumed that selection pressure can increase the pression of an eukaryotic gene, transferred to a probability for a successful establishment of HGT bacterial organism, requires a prokaryotic pro- (Nielsen et al., 1998). Until now the cultivation moter (Jacob et al., 2004). This implies that plant of GM plants in the fi eld has not revealed any transgenes transferred via HGT from plants to evidence that transgenes have been transferred to bacteria would not be expressed in prokaryotes bacteria (Gebhard and Smalla, 1998; Paget et al., because plant-specifi c regulatory sequences are 1998; Badosa et al., 2004; Demanèche et al., 2008; associated with the transgene. However, the 35S- Wagner et al., 2008), although they were detected CaMV promoter includes prokaryotic promoter- in the soil food web (Hart et al., 2009). like recognition sequences, which allow for direct Roundup Ready® (RR) soybean is currently gene expression in Escherichia coli (Assaad and the most widely used GM crop, which was ge- Signer, 1990) and several other bacteria (Lewin et netically modifi ed to tolerate glyphosate [(N- al., 1998; Jacob et al., 2004). (phosphonomethyl)glycine]-containing herbi- Studies addressing the molecular basis for cides, and was responsible in 2010 for about 70% glyphosate resistance demonstrated that a single of the worldwide soybean production (http:// amino acid exchange in the active site renders www.transgen.de/anbau/eu_international/). Fur- CP4-EPSPS insensitive to glyphosate (Padgette thermore, glyphosate is the most widely used her- et al., 1991; Selvapandiyan et al., 1995). The con- bicide in the world (Yu et al., 2007), largely due to tinued presence of glyphosate is likely to favour the increasing popularity of RR crops. mutations that reduce glyphosate sensitivity while Glyphosate is a foliar-applied, broad-spectrum, still maintaining catalytic effi ciency. Therefore, it non-selective herbicide that is symplastically is not surprising that the gene coding for CP4- translocated to the meristems of growing plants EPSPS was isolated from a bacterium found in an and controls a wide variety of weeds (Rubin et extremely glyphosate-rich environment (Funke al., 1982; Zablotowicz and Reddy, 2004). Glypho- et al., 2006). This suggests that under glyphosate sate blocks the shikimate pathway through the selection pressure, glyphosate tolerance could be inhibition of 5-enolpyruvylshikimate-3-phosphate achieved through spontaneous mutation or via synthase (EPSPS) (Amrhein et al., 1980). Because HGT within bacterial communities. the shikimate pathway is present in plants, bacte- DNA sequence alignments of EPSPS genes ria, and fungi but absent in animals, EPSPS has from the Agrobacterium tumefaciens strain CP4 been an attractive target for effective herbicide and Bradyrhizobium japonicum revealed high development (Coggins et al., 2003; Priestman et homologies in many regions (Wagner et al., 2008). L. A. Isaza et al. · Horizontal Gene Transfer from Transgenic Plants to Bacteria 597 The probability of HGT from RR soybean to DNA isolation bacteria was assessed under natural fi eld condi- DNA was extracted from soybean leaves, nod- tions, choosing the nitrogen-fi xing soybean symbi- ules, and bacteroids according to Chen and Ron- ont B. japonicum as a DNA receptor (Wagner et ald (1999), and the fi nal pellet was dissolved in al., 2008). Because glyphosate inhibits the growth 20 – 50 μl H O. For the isolation of DNA frag- of this symbiotic bacterium by the inhibition 2 ments of the EPSPS construct total genomic of aromatic acid amino biosynthesis
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