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Investigation of horizontal gene transfer in poplar/Amanita muscaria ectomycorrhizas

Published online by Cambridge University Press:  22 June 2006

Chi Zhang ,
Rüdiger Hampp  and
Uwe Nehls
Chi Zhang
Affiliation:
Universität Tübingen, Botanisches Institut, Physiologische Ökologie der Pflanzen, Auf der Morgenstelle 1, 72076 Tübingen, Germany
Rüdiger Hampp
Affiliation:
Universität Tübingen, Botanisches Institut, Physiologische Ökologie der Pflanzen, Auf der Morgenstelle 1, 72076 Tübingen, Germany
Uwe Nehls
Affiliation:
Universität Tübingen, Botanisches Institut, Physiologische Ökologie der Pflanzen, Auf der Morgenstelle 1, 72076 Tübingen, Germany

Abstract

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Fine roots of forest trees form together with certain soil fungi symbiotic structures (ectomycorrhizas), where fungal hyphae are in intimate contact with plant cells. Due to root cell degeneration, plant DNA is released and could be taken up by the fungus. The possibility that horizontal gene transfer might result in a risk for the environment should be evaluated before a massive release of genetically engineered trees into nature occurs, even though only a few convincing examples of horizontal gene transfer are known. Transgenic poplars containing a construct of the Streptomyces hygroscopicus bar gene under the control of the Cochliobolus heterostrophus GPD (glyceraldehyde-3-phosphate dehydrogenase) promoter were generated by Agrobacterium-mediated transformation. The functionality of this construct in the ectomycorrhizal model fungus Amanita muscaria was previously verified by protoplast-based fungal transformation. 35 000 ectomycorrhizas, formed between transgenic poplars and non-transgenic A. muscaria hyphae, were isolated and transferred to selective agar plates. Putative herbicide-resistant fungal colonies were obtained after the first round of selection. However, none of these colonies survived a transfer onto fresh selection medium, nor did they contain the bar gene, indicating that no horizontal gene transfer from poplar to A. muscaria occurred during symbiosis under axenic conditions. However, since ectomycorrhizas are associated under natural conditions with viruses, bacteria and other fungi, these additional associations should be evaluated in future.

Keywords

horizontal gene transferpoplarectomycorrhizatransformation
Type
Research Article
Information
Environmental Biosafety Research , Volume 4 , Issue 4 , October 2005 , pp. 235 - 242
Copyright
© ISBR, EDP Sciences, 2006

References

Barret, V, Dixon, RK, Lemke, PA (1990) Genetic transformation of a mycorrhizal fungus. Appl. Microbiol. Biot. 33: 313–316 CrossRef
Bills, S, Podila, GK, Hiremath, S (1999) Genetic engineering of an ectomycorrhizal fungus Laccaria bicolor for use as a biological control agent. Mycologia 91: 237–242 CrossRef
Boerjan W, Baucher M, Chabbert B, PetitConil M, Leple JC, Pilate G, Cornu D, Monties B, Inze D, VanDoorsselaere J, Jouanin L, VanMontagu M, Tsai CJ, Podila GK, Joshi CP, Chiang VL (1997) Micropropagation, genetic engineering, and molecular biology of Populus. US Department of Agriculture, Forest Service, Rocky Mountain Forest and Range Experiment Station, Fort Collins, CO
Bryngelsson T, Gustafsson M, Green B, Lind C (1988) Uptake of host DNA by the parasitic fungus Plasmodiophora brassicae. Physiol. Mol. Plant P. 33: 163–171 CrossRef
Chen, XY, Hampp, R (1993) Sugar uptake by protoplasts of the ectomycorrhizal fungus, Amanita muscaria (L. ex fr.) Hooker. New Phytol. 125: 601–608 CrossRef
Combier, JP, Melayah, D, Raffier, C, Pepin, R, Marmeisse, R, Gay, G (2004) Nonmycorrhizal (myc-) mutants of Hebeloma cylindrosporum obtained through insertional mutagenesis. Mol. Plant Microbe Int. 17: 1029–1038 CrossRef
De Vries, J, Wackernagel, W (2002) Integration of foreign DNA during natural transformation of Acinetobacter sp. by homology-facilitated illegitimate recombination. Proc. Natl. Acad. Sci. USA 99: 2094–2099 CrossRef
Fincham, JR (1989) Transformation in fungi. Microbiol. Rev. 53: 148–170
Garcia-Vallvé, S, Romeu, A, Palau, J (2000) Horizontal gene transfer of glycosyl hydrolases of the rumen fungi. Mol. Biol. Evol. 17: 352–361 CrossRef
Gebhard, F, Smalla, K (1998) Transformation of Acinetobacter sp. strain BD413 by transgenic sugar beet DNA. Appl. Environ. Microbiol. 64: 1550–1554
Gebhard, F, Smalla, K (1999) Monitoring field releases of genetically modified sugar beets for persistence of transgenic plant DNA and horizontal gene transfer. FEMS Microbiol. Ecol. 28: 261–272 CrossRef
Hampp, R, Ecke, M, Schaeffer, C, Wallenda, T, Wingler, A, Kottke, I, Sundberg, B (1996) Axenic mycorrhization of wild type and transgenic hybrid aspen expressing T-DNA indoleacetic acid-biosynthetic genes. Trees 11: 59–64 CrossRef
Hampp R, Stülten C, Nehls U (1998) Isolation and regeneration of protoplasts from ectomycorrhizal fungi. In Varma A, ed, Modern manual of mycorrhiza, Springer-Verlag, Berlin Heidelberg, Germany, pp 115–126
Hanif, M, Pardo, AG, Gorfer, M, Raudaskoski, M (2002) T-DNA transfer and integration in the ectomycorrhizal fungus Suillus bovinus using hygromycin B as a selectable marker. Curr. Genet. 41: 183–188 CrossRef
Hoffmann, T, Golz, C, Schieder, O (1994) Foreign DNA sequences are received by a wild type strain of Aspergillus niger after co culture with transgenic higher plants. Curr. Genet. 27: 70–76 CrossRef
Koncz CJ, Schell J, Redei GP (1992) Methods in Arabidopsis research, World scientific, London
Kottke, I, Guttenberger, M, Hampp, R, Oberwinkler F (1987) An in vivo method for establishing mycorrhizae on coniferous tree seedlings. Trees 1: 191–194 CrossRef
Kottke, I, Oberwinkler, F (1987) The cellular structure of the Hartig net: coenocytic and transfer-cell like organization. Nord. J. Bot. 7: 85–95 CrossRef
Lapierre, C, Pollet, B, Petit-Conil, M, Toval, G, Romero, J, Pilate, G, Leplé, JC, Boerjan, W, Ferret, VV, De Nadai, V, Jouanin, L (1999) Structural alterations of lignins in transgenic poplars with depressed cinnamyl alcohol dehydrogenase or caffeic acid O-methyltransferase activity have an opposite impact on the efficiency of industrial kraft pulping. Plant Physiol. 119: 153–164 CrossRef
Leplé, JC, Brasileiro, ACM, Michel, MF, Delmotte, F, Jouanin, L (1992) Transgenic poplars: Expression of chimeric genes using four different constructs. Plant Cell Rep. 11: 137–141 CrossRef
Magee, PT, Gale, C, Berman, J, Davis, D (2003) Molecular genetic and genomic approaches to the study of medically important fungi. Infect. Immun. 71: 2299–2309 CrossRef
Marmeisse R, Gay G, Debaud JC, Casselton LA (1992) Genetic transformation of the symbiotic basidiomycete fungus Hebeloma cylindrosporum. Curr. Genetics 22: 41–45
Murray, MG, Thompson, WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res. 8: 4321–4325 CrossRef
Nehls, U, Friedrich, T, Schmiede, A, Ohnishi, T, Weiss, H (1992) Characterization of assembly intermediates of NADH: ubiquinone oxidoreductase (complex I) accumulated in Neurospora mitochondria by gene disruption. J. Mol. Biol. 227: 1032–1042 CrossRef
Nehls, U, Mikolajewski, S, Ecke, M, Hampp, R (1999) Identification and expression analysis of two fungal cDNAs regulated by ectomycorrhiza and fruit body formation. New Phytol. 144: 195–202 CrossRef
Nielsen, KM, Elsas, JD, Smalla, K (2000) Transformation of Acinetobacter sp. strain BD413 (pFG4DnptII) with transgenic plant DNA in soil microcosms and effects of kanamycin on selection of transformants. Appl. Environ. Microb. 66: 1237–1242 CrossRef
Olmedo-Monfil, V, Cortes-Penagos, C, Herrera-Estrella A (2004) Three decades of fungal transformation: key concepts and applications. Meth. Molec. Biol. 267: 297–313
Owen, MDK (2000) Current use of transgenic herbicide-resistant soybean and corn in the USA. Crop Prot. 19: 765–771 CrossRef
Pardo AG, Hanif M, Raudaskoski M, Gorfer M (2002) Genetic transformation of ectomycorrhizal fungi mediated by Agrobacterium tumefaciens. Brit. Mycol. Soc. Trans. 106: 132–137 CrossRef
Ruiz-Diez, B (2002) Strategies for the transformation of filamentous fungi. J. Appl. Microbiol. 92: 189–195 CrossRef
Saroha, MK, Sridhar, P, Malik, VS (1998) Glyphosate-tolerant crops: Genes and enzymes. J. Plant Biochem. Biot. 7: 65–72 CrossRef
Schaeffer, C, Johann, P, Nehls, U, Hampp, R (1996) Evidence for an up-regulation of the host and a down-regulation of the fungal phosphofructokinase activity in ectomycorrhizas of Norway spruce and fly agaric. New Phytol. 134: 697–702 CrossRef
Schlüter, K, Fütterer, J, Potrykus, I (1995) “Horizontal” gene transfer from a transgenic potato line to a bacterial pathogen (Erwinia chrysanthemi) occurs – if at all – at an extremely low frequency. Biotechniques 13: 1094–1098
Smith SE, Read DJ (1997) Mycorrhizal symbiosis: Second edition, Academic Press, London
Straubinger B, Straubinger E, Wirsel S, Turgeon G, Yoder O (1992) Versatile fungal transformation vectors carrying the selectable bar gene of Streptomyces hygroscopicus. Fungal Genet. Newsl. 39: 82–83 CrossRef
Tuominen, H, Sitbon, F, Jacobsson, C, Sandberg, G, Olsson, O, Sundberg, B (1995) Altered growth and wood characteristics in transgenic hybrid aspen expressing Agrobacterium tumefaciens T-DNA indoleacetic acid-biosynthetic genes. Plant Physiol. 109: 1179–1189 CrossRef
Warwick, SI, Beckie, HJ, Small, E (1999) Transgenic crops: new weed problems for Canada? Phytoprotection 80: 71–84 CrossRef