Hostname: page-component-8448b6f56d-qsmjn Total loading time: 0 Render date: 2024-04-19T23:43:59.786Z Has data issue: false hasContentIssue false

Effects of rhizodeposition of non-transgenic and transplastomic tobaccos on the soil bacterial community

Published online by Cambridge University Press:  03 April 2008

Lorenzo Brusetti
Affiliation:
Dipartimento di Scienze e Tecnologie Alimentari e Microbiologiche (DISTAM), Università degli Studi di Milano, via Celoria 2, 20133, Milano, Italy
Aurora Rizzi
Affiliation:
Dipartimento di Scienze e Tecnologie Alimentari e Microbiologiche (DISTAM), Università degli Studi di Milano, via Celoria 2, 20133, Milano, Italy
Alessandro Abruzzese
Affiliation:
Dipartimento di Produzione Vegetale (DIPROVE), Università degli Studi di Milano, via Celoria 2, 20133, Milano, Italy
Gian Attilio Sacchi
Affiliation:
Dipartimento di Produzione Vegetale (DIPROVE), Università degli Studi di Milano, via Celoria 2, 20133, Milano, Italy
Enzio Ragg
Affiliation:
Dipartimento di Scienze Molecolari ed Agroalimentari (DISMA), Università degli Studi di Milano, via Celoria 2, 20133, Milano, Italy
Marco Bazzicalupo
Affiliation:
Dipartimento di Biologia Animale e Genetica (DBAG), Università degli Studi di Firenze, via Romana 17, 50125, Firenze, Italy
Claudia Sorlini
Affiliation:
Dipartimento di Biologia Animale e Genetica (DBAG), Università degli Studi di Firenze, via Romana 17, 50125, Firenze, Italy
Daniele Daffonchio
Affiliation:
Dipartimento di Scienze e Tecnologie Alimentari e Microbiologiche (DISTAM), Università degli Studi di Milano, via Celoria 2, 20133, Milano, Italy

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

The effect of root-released compounds of transplastomic tobacco (Nicotiana tabacum) on the soil bacterial community structure, and their potential to support horizontal gene transfer (HGT) to bacteria have been studied. Soil microcosms were exposed to root-released compounds collected from transplastomic and non-transgenic tobacco cultivars. Cluster analysis of automated ribosomal intergenic spacer analysis (ARISA) profiles of the soil bacterial community after 48 h incubation grouped the transgenic cultivar apart from the non-transgenic, indicating that it had a rhizodeposition pattern different from the parental plants. However, these differences were less than between the two non-transgenic tobacco cultivars studied. NMR characterization of the root-released compounds showed some differences in chemical fingerprinting pattern between the transplastomic and the parental cultivar. However, the effect on bacterial community structure was transient, and tended to disappear after 96 h of incubation. The potential of root-released compounds as a source of transforming DNA for bacteria was investigated by using four potential recipient species. No transformants were obtained following exposure of all the recipients to the root-released compounds. Root-released compounds amended to transgene donor DNA decreased the transformation frequency of Acinetobacter baylyi strain ADP1200, while Azospirillum, Agrobacterium, and Sinorhizobium strains failed to develop competence also in the presence of an external added transgene source. Detection of plastid sequences by PCR suggested that a very low amount of fragmented plastid donor DNA was present in the root-released compounds.

Type
Research Article
Copyright
© ISBR, EDP Sciences, 2008

References

Andersen JM, Pedersen WB (1983) Analysis of plant phenolics by High-Performance Liquid Chromatography. J. Chromatogr. 259: 131–139
Baudoin, E, Benizri, E, Guckert, A (2002) Impact of growth stage on the bacterial community structure along maize roots as determined by metabolic and genetic fingerprinting. Appl. Soil Ecol. 19: 135145 CrossRef
Brusetti, L, Francia, P, Bertolini, C, Pagliuca, A, Borin, S, Sorlini, C, Abruzzese, A, Sacchi, G, Viti, C, Giovannetti, L, Giuntini, E, Bazzicalupo, M, Daffonchio, D (2004) Bacterial communities associated with the rhizosphere of transgenic Bt 176 maize (Zea mays) and its non transgenic counterpart. Plant Soil 266: 1121 CrossRef
Brusetti L, Borin S, Mora D, Rizzi A, Raddadi N, Sorlini C, Daffonchio D (2006) Usefulness of length heterogeneity-PCR for monitoring lactic acid bacteria succession during maize ensiling. FEMS Microbiol. Ecol. 56: 154–164
Cardinale, M, Brusetti, L, Quatrini, P, Borin, S, Puglia, AM, Rizzi, A, Zanardini, E, Sorlini, C, Corselli, C, Daffonchio, D (2004) Comparison of different primer sets for the Automated Ribosomal Intergenic Spacer Analysis (ARISA) of complex bacterial communities. Appl. Environ. Microbiol. 70: 61476156 CrossRef
Chiarini, L, Bevivino, A, Dalmastri, C, Nacamulli, C, Tabacchioni, S (1998) Influence of plant development, cultivar and soil type on microbial colonisation of maize roots. Appl. Soil Ecol. 8: 1118 CrossRef
Courtois, J, Courtois, B, Guillaume, J (1988) High-frequency transformation of Rhizobium meliloti. J. Bacteriol. 170: 59255927 CrossRef
Daffonchio, D, Cherif, A, Brusetti, L, Rizzi, A, Mora, D, Boudabous, A, Borin, S (2003) Nature of polymorphisms in 16S-23S rRNA gene intergenic transcribed spacer fingerprinting of Bacillus and related genera. Appl. Environ. Microbiol. 69: 51285137 CrossRef
Daniell H, Datta R, Varma S, Gray S, Lee SB (1998) Containment of herbicide resistance through genetic engineering of the chloroplast genome. Nature Biotechnol. 16: 345–348
De Vries, J, Herzfeld, T, Wackernagel, W (2004) Transfer of plastid DNA from tobacco to the soil bacterium Acinetobacter sp. by natural transformation. Mol. Microbiol. 53: 323334 CrossRef
Demanèche S, Kay E, Gourbiere F, Simonet P (2001) Natural transformation of Pseudomonas fluorescence and Agrobacterium tumefaciens in soil. Appl. Environ. Microbiol. 67: 2617–1621
Di Giovanni GD, Watrud LS, Seidler RJ, Widmer F (1999) Comparison of parental and transgenic alfalfa rhizosphere bacterial communities using Biolog GN metabolic fingerprinting and enterobacterial repetitive intergenic consensus sequence-PCR (ERIC-PCR). Microb. Ecol. 37: 129–139
Donegan KK, Palm CJ, Fieland VJ, Porteous LA, Ganio LM, Schaller DL, Bucao LQ, Seidler RJ (1995) Changes in levels, species and DNA fingerprints of soil microorganisms associated with cotton expressing the Bacillus thuringiensis var. kurstaki endotoxin. Appl. Soil Ecol. 2: 111–124
Dunfield, KE, Germida, JJ (2001) Diversity of bacterial communities in the rhizosphere and root interior of field-grown genetically modified Brassica napus. FEMS Microbiol. Ecol. 38: 19 CrossRef
Dunfield, KE, Germida, JJ (2003) Seasonal changes in the rhizosphere microbial communities associated with field-grown genetically modified canola (Brassica napus). Appl. Environ. Microbiol. 69: 73107318 CrossRef
Einspanier R, Klotz A, Kraft J, Aulrich K, Poser R, Schwägele F, Jahreis G, Flachowsky G (2001) The fate of forage plant DNA in farm animals: a collaborative case-study investigating cattle and chicken fed recombinant plant material. Eur. Food Res. Technol. 212: 129–134
Falchini, L, Naumova, N, Kuikman, PJ, Bloem, J, Nannipieri P (2002) CO2 evolution and denaturing gradient gel electrophoresis profiles of bacterial communities in soil following addition of low molecular weight substrates to simulate root exudation. Soil Biol. Biochem. 36: 775782
Fan, T, Lane, A, Pedler, J, Crowley, D, Higashi, R (1997) Comprehensive analysis of organic ligands in whole root exudates using Nuclear Magnetic Resonance and Gas Chromatography Mass Spectrometry. Anal. Biochem. 251: 5768 CrossRef
Figurski, D, Helinski, DR (1979) Replication of an origin containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. PNAS 76: 16481652 CrossRef
Fisher, MM, Triplett, EW (1999) Automated approach for ribosomal intergenic spacer analysis of microbial diversity and its application to freshwater bacterial communities. Appl. Environ. Microbiol. 65: 46304636
Gallori, E, Bazzicalupo, M, Dal Canto, L, Nannipieri, P, Vettori, C, Stotzky, G (1994) Transformation of Bacillus subtilis by DNA bound on clay in non-sterile soil. FEMS Microbiol. Ecol. 15: 119126 CrossRef
Gancedo, MC, Luth, BS (1986) HPLC analysis of organic acids and sugars in tomato juice. J. Food Science. 51: 571573 CrossRef
Gomes, NCM, Heuer, H, Schönfeld, J, Costa, R, Mendonça-Hagler, L, Smalla, K (2001) Bacterial diversity of the rhizosphere of maize (Zea mays) grown in tropical soil studied by temperature gradient gel electrophoresis. Plant Soil 232: 167180 CrossRef
Gries D, Brunn S, Crowley D, Parker D (1995) Phytosiderophore release in relation to micronutrient metal deficiencies in barley. Plant Soil 172: 299–308
Gyamfi, S, Pfeifer, U, Stierschneider, M, Sessitsch, A (2002) Effects of transgenic gluphosinate-tolerant oilseed rape (Brassica napus) and the associated herbicide application on eubacterial and Pseudomonas communities in the rhizosphere. FEMS Microbiol. Ecol. 41: 181190 CrossRef
Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontologia Electronica 4: 1–9
Heuer, H, Kroppenstedt, RM, Lottmann, J, Berg, G, Smalla, K (2002) Effects of T4 lysozyme release from transgenic potato roots on bacterial rhizosphere communities are negligible relative to natural factors. Appl. Environ. Microbiol. 68: 13251335 CrossRef
Hinsinger P, Gobran GR, Gregory PJ, Wenzel WW (2005) Rhizosphere geometry and heterogeneity arising from root-mediated physical and chemical processes. New Phytologist. 168: 293–303
Jackman LM, Sternhell S (1969) Applications of Nuclear Magnetic Resonance Spectroscopy in Organic Chemistry, 2nd edn. Pergamon Press, UK, pp 207–214
Kay, E, Vogel, TM, Bertolla, F, Nalin, R, Simonet, P (2002) In situ transfer of antibiotic resistance genes from transgenic (transplastomic) tobacco plants to bacteria. Appl. Environ. Microbiol. 68: 33453351 CrossRef
Kent AD, Triplett EW (2002) Microbial communities and their interactions in soil and rhizosphere ecosystems. Ann. Rev. Microbiol. 56: 211–36
Khanna, M, Stotzky, G (1992) Transformation of Bacillus subtilis by DNA bound on montmorillonite and effect of DNase on the availability of bound DNA. Appl. Environ. Microbiol. 58: 19301939
Kok, RG, Young, DM, Ornston, LN (1999) Phenotypic expression of PCR-generated random mutations in a Pseudomonas putida gene after its introduction into an Acinetobacter chromosome by natural transformation. Appl. Environ. Microbiol. 65: 16751780
Lynch, JM, Whipps, JM (1990) Substrate flow in the rhizosphere. Plant Soil 129: 110 CrossRef
Magurran AE (1988) Ecological diversity and its measurement. Cambridge University Press, UK
Mansouri, H, Petit, A, Oger, P, Dessaux, Y (2002) Engineered rhizosphere: the trophic bias generated by opine-producing plants is independent of the opine type, the soil origin, and the plant species. Appl. Environ. Microbiol. 68: 25622566 CrossRef
McBee GG, Manes NO (1983) Determination of sucrose, glucose and fructose in plant tissue by HPLC. J. Chrom. 264: 474–478
Milling, A, Smalla, K, Maidl, FX, Schloter, M, Munch, JC (2004) Effects of transgenic potatoes with an altered starch composition on the diversity of soil and rhizosphere bacteria and fungi. Plant Soil 266: 2339 CrossRef
Nielsen KM, Ray JL, Van Elsas JD (2004) Natural transformation in soil: microcosm studies. In Molecular Microbial Ecology Manual, 2nd edn, Kluwer Academic Publishers, The Netherlands, pp 1–12
Oger, P, Petit, A, Dessaux, Y (1997) Genetically engineered plants producing opines alter their biological environment. Nature Biotech. 15: 369372 CrossRef
Oger, P, Mansouri, H, Dessaux, Y (2000) Effect of crop rotation and soil cover on alteration of the soil microflora generated by the culture of transgenic plants producing opines. Mol. Ecol. 9: 881890 CrossRef
Paget E, Monrozier LJ, Simonet P (1992) Adsorption of DNA on clay minerals: protection against DNase I and influence on gene transfer. FEMS Microbiol. Lett. 97: 31–40
Pal, KK, Tilak, KVBR, Saxena, AK, Dey, R, Singh, CS (2001) Suppression of maize root diseases caused by Macrophomina phaseolina, Fusarium moniliforme and Fusarium graminearum by plant growth promoting rhizobacteria. Microbiol. Res. 156: 209223 CrossRef
Persello-Cartieaux F, Nussaume L, Robaglia C (2003) Tales from the underground: molecular plant-rhizobacteria interactions. Plant Cell Environ. 26: 189–199
Pietramellara, G, Dal Canto, L, Vettori, C, Gallori, E, Nannipieri, P (1997) Effects of air-drying and wetting cycles on the transforming ability of DNA bound on clay minerals. Soil Biol. Biochem. 29: 5561 CrossRef
Savka MA, Farrand SK (1997) Modification of rhizobacterial populations by engineering bacterium utilisation of a novel plant produced resource. Nature Biotech. 15: 363-368
Sessitsch, A, Kan, F-Y, Pfeifer, U (2003) Diversity and community structure of culturable Bacillus spp. populations in the rhizospheres of transgenic potatoes expressing the lytic peptide cecropin B. Appl. Soil Ecol. 22: 149158 CrossRef
Siciliano, SD, Germida, JJ (1999) Taxonomic diversity of bacteria associated with the roots of field-grown transgenic Brassica napus cv. Quest, compared to the non-transgenic B. napus cv. Excel and B. rapa cv. Parkland. FEMS Microbiol. Ecol. 29: 263272 CrossRef
Smalla, K, Wieland, G, Buchner, A, Zock, A, Parzy, J, Kaiser, S, Roskot, N, Heuer, H, Berg, G (2001) Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: plant-dependent enrichment and seasonal shifts revealed. Appl. Environ. Microbiol. 67: 47424751 CrossRef
Smit, E, Leeflang, P, Gommans, S, van den Broek, J, van Mil, S, Wernars, K (2001) Diversity and seasonal fluctuations of the dominant members of the bacterial soil community in a wheat field as determined by cultivation and molecular methods. Appl. Environ. Microbiol. 67: 2284-2291 CrossRef
Tepfer, D, Garcia-Gonzaleset, R, Mansouri, H, Seruga, M, Message, B, Leach, F, Curkovic Perica M (2003) Homology-dependent DNA transfer from plants to a soil bacterium under laboratory conditions: implications in evolutions and horizontal gene transfer. Trans. Res. 12: 425437 CrossRef
Vaneechoutte, M, Young, DM, Ornston, LN, De Baere, T, Nemec, A, Van Der Reijden, T, Carr, E, Tjernberg, I, Dijkshoorn, L (2006) Naturally transformable Acinetobacter sp. strain ADP1 belongs to the newly described species Acinetobacter baylyi. Appl. Environ. Microbiol. 72: 932936 CrossRef
Widmer, F, Seidler, RJ, Donegan, KK, Reed, GL (1997) Quantification of transgenic marker gene persistence in the field. Mol. Ecol. 6: 17 CrossRef
Wiren, N, von Romheld, V, Shioiri, T, Marschner, H (1995) Competition between micro-organism and roots of barley and sorghum for iron accumulated in the root apoplasm. New Phytol. 130: 511521 CrossRef