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Phylogeny of chitinases and its implications for estimating horizontal gene transfer from chitinase-transgenic silver birch (Betula pendula)

Published online by Cambridge University Press:  29 October 2008

Katileena Lohtander ,
Hanna-Leena Pasonen ,
Markku K. Aalto ,
Tapio Palva ,
Ari Pappinen  and
Jouko Rikkinen
Katileena Lohtander
Affiliation:
Botanical Museum, P.O. Box 7, 00014 University of Helsinki, Finland
Hanna-Leena Pasonen
Affiliation:
Department of Applied Biology, P.O. Box 27, 00014 University of Helsinki, Finland
Markku K. Aalto
Affiliation:
Department of Biosciences, P.O. Box 47, 00014 University of Helsinki, Finland
Tapio Palva
Affiliation:
Department of Biosciences, P.O. Box 47, 00014 University of Helsinki, Finland
Ari Pappinen
Affiliation:
North Karelia University of Applied Sciences, Tikkarinne 9, 80200 Joensuu, Finland
Jouko Rikkinen
Affiliation:
Department of Ecology and Systematics, Division of Systematics, P.O. Box 47, 00014 University of Helsinki, Finland

Abstract

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Chitinases are hydrolytic enzymes that have been employed in biotechnology in attempts to increase plants' resistance against fungal pathogens. Genetically modified plants have given rise to concerns of the spreading of transgenes into the environment through vertical or horizontal gene transfer (HGT). In this study, chitinase-like sequences from silver birch (Betula pendula) EST-libraries were identified and their phylogenetic relationships to other chitinases were studied. Phylogenetic analyses were used to estimate the frequency of historical gene transfer events of chitinase genes between plants and other organisms, and the usefulness of phylogenetic analyses as a source of information for the risk assessment of transgenic silver birch carrying a sugar beet chitinase IV gene was evaluated. Thirteen partial chitinase-like sequences, with an approximate length of 600 bp, were obtained from the EST-libraries. The sequences belonged to five chitinase classes. Some bacterial chitinases from Streptomyces and Burkholderia, as well as a chitinase from an oomycete, Phytophthora infestans, grouped together with the class IV chitinases of plants, supporting the hypothesis that some class IV chitinases in bacteria have evolved from eukaryotic chitinases via horizontal gene transfer. According to our analyses, HGT of a chitinase IV gene from eukaryotes to bacteria has presumably occurred only once. Based on this, the likelihood for the HGT of chitinase IV gene from transgenic birch to other organisms is extremely low. However, as risk is a function of both the likelihood and consequences of an event, the effects of rare HGT event(s) will finally determine the level of the risk.

Keywords

birchchitinasehorizontal gene transferphylogenyrisk assessmenttransgenic tree
Type
Research Article
Information
Environmental Biosafety Research , Volume 7 , Issue 4 , October 2008 , pp. 227 - 239
Copyright
© ISBR, EDP Sciences, 2008

References

Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 24: 3389–3402
Arlorio, M, Ludwig, A, Boller, T, Bonfante, P (1992) Inhibition of fungal growth by plant chitinases and $\beta $ -1,3-glucanases. Protoplasma 171: 34–43 CrossRef
Asao H, Nishizawa Y, Arai S, Sato T, Hirai M, Yoshida K, Shinmyo A, Hibi T (1997) Enhanced resistance against a fungal pathogen Sphaerotheca humuli in transgenic strawberry expressing a rice chitinase gene. Plant Biotechnol. 14: 145–149
Baker, ME (1998) Evolution of mammalian 11 beta- and 17 beta-hydroxysteroid dehydrogenases-type 2 and retinol dehydrogenases from ancestors in Caenorhabditis elegans and evidence for horizontal transfer of a eukaryote dehydrogenase to E. coli. J. Ster. Biochem. Mol. Biol. 66: 355–363 CrossRef
Bartnicki-Garcia S (1968) Cell wall chemistry, morphogenesis, and taxonomy of fungi. Ann. Rev. Microbiol. 22: 87–108
Bertolla F, Simonet P (1999) Horizontal gene transfers in the environment, natural transformation as a putative process for gene transfers between transgenic plants and micro-organisms. Res. Microbiol. 150: 375–384
Beintema, J (1994) Structural features of plant chitinases and chitin-binding proteins. FEBS Letters 350: 159–163 CrossRef
Bolar, JP, Norelli, JL, Wong, K-W, Hayes, CK, Harman, GE, Aldwinckle, HS (2000) Expression of endochitinase from Trichoderma harzianum in transgenic apple increases resistance to apple scab and reduces vigor. Phytopathology 90: 72–77 CrossRef
Bolar J, Norelli J, Harman G, Brown S, Aldwinckle H (2001) Synergistic activity of endochitinase and exochitinase from Trichoderma atroviride (T. harzianum) against the pathogenic fungus (Venturia inaequalis) in transgenic apple plants. Transgenic Res. 10: 533–543
Boller T (1987) Hydrolytic enzymes in plant disease resistance. In Kosuge T, Nester EW, eds, Plant-Microbe Interactions, Macmillan, New York, Vol. 2, pp 385–413
Brinkman, FSL, MacFarlane, ELA, Warrener, P, Hancoc R (2001) Evolutionary relationships among virulence-associated histidine kinases. Infect. Immun. 69: 5207–5211 CrossRef
Brinkman FSL, Blanchard JL, Cherkasov A, Av-Gay Y, Brunham RC, Fernandez RC, Finlay B, Otto SP, Ouellette BFF, Keeling PJ, Rose AM, Hancock REW, Jones SJM (2002) Evidence that plant-like genes in Chlamydia species reflect an ancestral relationship between Chlamydiaceae, cyanobacteria, and the choloroplast. Genome Res. 12: 11159–1167
Broglie, K, Chet, I, Holliday, M, Cressman, R, Biddle, P, Knowlton, S, Mauvais, CJ, Broglie, R (1991) Transgenic plants with enhanced resistance to the fungal pathogen Rhizoctonia solani. Science 254: 1194–1197 CrossRef
Buades, C, Moya, A (1996) Phylogenetic analysis of the isopenicillin-N-synthetase horizontal gene transfer. J. Mol. Evol. 42: 537–542 CrossRef
Collinge DB, Kragh KM, Mikkelsen JD, Nielsen KK, Rasmussen U, Vad K (1993) Plant chitinases. Plant J. 3: 31–40
Conner AJ, Glare TR, Nap J-P (2003) The release of genetically modified crops into the environment. Part II. Overview of ecological risk assessment. Plant J. 33: 19–46
Cottrell, MT, Wood, DN, Yu, L, Kirchman, DL (2000) Selected chitinase genes in cultured and uncultured marine bacteria in the $\alpha$ - and $\beta $ - subclasses of the Proteobacteria. Appl. Environ. Microbiol. 66: 1195–1201 CrossRef
Dale, PJ, Clarke, B, Fontes, EMG (2002) Potential for the environmental impact of transgenic crops. Nature Biotechnol. 20: 567–574 CrossRef
Datta, K, Koukolíková-Nicola, Z, Baisakh, N, Oliva, N, Datta, SK (2000) Agrobacterium-mediated engineering for sheath blight resistance of indica rice cultivars from different ecosystems. Theor. Appl. Genet. 100: 832–839 CrossRef
Davies, G, Henrissat, B (1995) Structures and mechanisms of glycosyl hydrolases. Structure 3: 853–859 CrossRef
Davis JM, Clarke HR, Bradshaw HD Jr, Gordon MP (1991) Populus chitinase genes, structure, organization, and similarity of translated sequences to herbaceous plant chitinases. Plant Mol. Biol. 17: 631–639
De Vries, J, Meier, P, Wackernagel, W (2001) The natural transformation of the soil bacteria Pseudomonas stutzeri and Acinetobacter sp. by transgenic plant DNA strictly depends on homologous sequences in the recipient cells. FEMS Microbiology Letters 195: 211–215 CrossRef
Emani C, Garcia JM, Lopata-Finch E, Pozo MJ, Uribe P, Kim D-J, Sunikumar G, Cook DR, Kenerley CM, Rathore KS (2003) Enhanced fungal resistance in transgenic cotton expressing an endochitinase gene from Trichoderma virens. Plant Biotech. J. 1: 321–336
Furner, IJ, Huffman, GA, Amasino, RM, Garfinkel, DJ, Gordon, MP, Nester, EW (1986) An Agrobacterium transformation in the evolution of the genus Nicotiana. Nature 319: 422–427 CrossRef
Gamieldien J, Ptitsyn A, Hide W (2002) Eukaryotic genes in Mycobacterium tuberculosis could have a role in pathogenesis and immunomodulation. Trends Genet. 18: 5–8
Garcia-Vallve S, Guzman E, Montero MA, Romeu A (2003) HGT-DB, a database of putative horizontally transferred genes in prokaryotic complete genomes. Nucleic Acids Res. 31: 187–189
Gay P (2001) The biosafety of antibiotic resistance markers in plant transformation and the dissemination of genes through horizontal gene flow. In Custers R, ed, Safety of genetically engineered crops, Zwijnaarde, Belgium, Flanders Interuniversity Institute for Biotechnology, pp 135–159
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
Grison R, Grezes-Besset B, Schneider M, Lucante N, Olsen L, Leguay JJ, Toppan A (1996) Field tolerance to fungal pathogens of Brassica napus constitutively expressing a chimeric chitinase gene. Nature Biotechnol. 14: 643–646
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41: 95–98
Hamel, F, Boivin, R, Tremblay, C, Bellemare, G (1997) Structural and evolutionary relationships among chitinases of flowering plants. J. Mol. Evol. 44: 614–624 CrossRef
Hawtin RE, Zarkowska T, Arnold K, Thomas CJ, Gooday GW, King LA, Kuzio JA, Possee RD (1997) Liquefaction of Autographa californica nucleopolyhedrovirus-infected insects is dependent on the integrity of virus-encoded chitinase and cathepsin genes. Virology 238: 243–253
Hay, I, Morency, M-J, Séguin, A (2002) Assessing the persistence of DNA in decomposing leaves of genetically modified poplar leaves. Can. J. For. Res. 32: 977–982 CrossRef
Heinemann JA, Traavik T (2004) Problems in monitoring horizontal gene transfer in field trials of transgenic plants. Nature Biotechnol. 22: 1105–1109
Heuer, H, Smalla, K (2007) Horizontal gene transfer between bacteria. Environ. Biosafety Res. 6: 3–13 CrossRef
Hoffman, 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
Holmgren, A, Bränden, C (1989) Crystal structure of chaperone protein PapD reveals an immunoglobulin fold. Nature 342: 248–251 CrossRef
Hon, WC, Griffith, M, Mlynarz, A, Kwok, YC, Yang, DSC (1995) Antifreeze proteins in winter rye are similar to pathogenesis-related proteins. Plant Physiol. 109: 879–889 CrossRef
Intrieri, M, Buiatti, M (2001) The horizontal transfer of Agrobacterium rhizogenes genes and the evolution of the genus Nicotiana. Mol. Phylogenet. Evol. 20: 100–110 CrossRef
Katz, LA (1996) Transkingdom transfer of the phosphoglucose isomerase gene. J. Mol. Evol. 43: 453–459 CrossRef
Ke, D, Boissinot, M, Huletsky, A, Picard, FJ, Frenette, J, Ouellette, M, Roy, PH, Bergeron, MG (2000) Evidence for horizontal gene transfer in evolution of elongation factor Tu in enterococci. J. Bacteriol. 182: 6913–6920 CrossRef
Klotz, MG, Klassen, GR, Loewen, PC (1997) Phylogenetic relationships among prokaryotic and eukaryotic catalases. Mol. Biol. Evol. 14: 951–958 CrossRef
Kong, H, Shimosaka, M, Ando, Y, Nishiyama, K, Fujii, T, Miyashita, K (2001) Species-specific distribution of a modular family 19 chitinase gene in Burkholderia gladioli. FEMS Microbiol. Ecol. 37: 135–141 CrossRef
Koonin EV, Makarova KS, Aravind L (2001) Horizontal gene transfer in prokaryotes, quantification and classification. Ann. Rev. Microbiol. 55: 709–742
Koski, LB, Morton, RA, Golding, GB (2000) Codon bias and base composition are poor indicators of horizontally transferred genes. Mol. Biol. Evol. 18: 404–412 CrossRef
Lilley, AK, Fry, JC, Day, MJ, Bailey, MJ (1994) In situ transfer of an exogenously isolated plasmid between Pseudomonas spp. in sugar beet rhizosphere. Microbiology 140: 27–33 CrossRef
Lorito, M, Woo, SL, Fernandez, IG, Colucci, G, Harman, GE, Pintor-Toro, JA, Filippone, E, Muccifora, S, Lowrence, CB, Zoina, A, Tuzun, S, Scala, F (1998) Genes from mycoparasitic fungi as a source for improving plant resistance to fungal pathogens. Proc. Natl. Acad. Sci. USA 95: 7860–7865 CrossRef
Mauch F, Mauch-Mani B, Boller T (1988) Antifungal hydrolases in pea tissue. II. Inhibition of fungal growth by combinations of chitinase and $\beta $ -1,3-glucanase. Plant Physiol. 88: 936–942
Melchers LS, Apotheker-de Groot M, van der Knaap JA, Ponstein AS, Sela-Buurlage MB, Bol JF, Cornelissen BJ, van den Elzen PJM, Linthorst HJM (1994) A new class of tobacco chitinases homologous to bacterial exo-chitinases displays antifungal activity. Plant J. 5: 469–480
Monier, JM, Bernillon, D, Kay, E, Faugier, A, Rybalka, O, Dessaux, Y, Simonet, P, Vogel, TM (2007) Detection of potential transgenic plant DNA recipients among bacteria. Environ. Biosafety Res. 6: 71–83 CrossRef
Nielsen KM, Townsend JP (2004) Monitoring and modeling horizontal gene transfer. Nature Biotechnol. 22: 1110–1114
Nielsen, KM, Gebhard, F, Smalla, K, Bones, AM, van Elsas, JD (1997) Evaluation of possible horizontal gene transfer from transgenic plants to the soil bacterium Acinetobacter calcoaceticus BD413. Theor. Appl. Genet. 95: 815–821 CrossRef
Nielsen, KM, Bones, AM, Smalla, K, van Elsas, JD (1998) Horizontal gene transfer from transgenic plants to terrestrial bacteria – rare event. FEMS Microbiol. Res. 22: 79–103 CrossRef
Nielsen, KM, van Elsas, JD, Smalla, K (2000) Transformation of Acinetobacter sp. Strain BD413 (pFGnptII) with transgenic plant DNA in soil microcosms and effects of kanamycin on selection of transformants. Appl. Environ. Microbiol. 66: 1237–1242 CrossRef
Nielsen, KM, Johnsen, PJ, Bensasson, D, Daffonchio, D (2007) Release and persistence of extracellular DNA in the environment. Environ. Biosafety Res. 6: 37–53 CrossRef
Ochman, H, Lawrence, JG, Groisman, EA (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405: 299–304 CrossRef
Ohno, T, Armand, S, Hata, T, Nikaidou, N, Henrissat, B, Mitsutomi, M, Watanabe, T (1996) A modular family 19 chitinase found in the prokaryotic organism Streptomyces griseus HUT 6037. J. Bacteriol. 17: 5065–5070 CrossRef
Pappinen A, Degefu Y, Syrjälä L, Keinonen K, von Weissenberg K (2002) Transgenic silver birch (Betula pendula) expressing a sugar beet chitinase 4 gene shows enhanced resistance to Pyrenopeziza betulicola. Plant Cell Rep. 20: 1046–1051
Pasonen, H-L, Seppänen, S-K, Degefu, Y, Rytkönen, A, von Weissenberg, K, Pappinen, A (2004) Field performance of chitinase transgenic silver birches (Betula pendula): resistance to fungal diseases. Theor. Appl. Genet. 109: 562–570 CrossRef
Pontiroli A, Simonet P, Frostegard A, Vogel TM, Monier J-M (2007) Fate of transgenic plant DNA in the environment. Environ. Biosafety Res. 6: 15–35
Robinson, SP, Jacobs, AK, Dry, IB (1997) A class IV chitinase is highly expressed in grape berries during ripening. Plant Physiol. 114: 771–778 CrossRef
Royo J, Gimez E, Hueros G (2000) CMP-KDO synthetase, a plant gene borrowed from gram negative eubacteria. Trends Genet. 16: 432–433
Schlumbaum, A, Mauch, F, Vögeli, U, Boller, T (1986) Plant chitinases are potent inhibitors of fungal growth. Nature 324: 365–367 CrossRef
Snowden K, Logan K, Didier ES (1999) Encephalitozoon cuniculi strain III is a cause of encephalitozoonosis in both humans and dogs. J. Infect Dis. 180: 2086–2088
Sowka S, Hsieh LS, Krebitz M, Akasawa A, Martin BM, Starrett D, Peterbauer CK, Scheiner O, Breiteneder H (1998) Identification and cloning of Prs a 1, a 32-kDa endochitinase and major allergen of avocado, and its expression in the yeast Pichia pastoris. J. Biol. Chem. 273: 28091–28097
Sun, L, Adams, B, Gurnon, JR, Ye, Y, Van Etten J (1999) Characterization of two chitinase genes and one chitisanase gene encoded by Chlorella virus PBCV-1. Virology 263: 376–387 CrossRef
Swofford DL (2000) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates, Sunderland, Massachusetts
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W, improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap-penalties and weigh matrix choise. Nucleic Acids Res. 22: 4673–4680
Troxler J, Azelvandre P, Zala M, Defago G, Haas D (1997) Conjugative transfer of chromosomal genes between fluorescent pseudomonas in the rhizosphere of wheat. Appl. Environ. Microbiol. 63: 213–219
van Elsas, JD, Nikkel, M, van Overbeek, LS (1989) Detection of plasmid RP4 transfer in soil and rhizosphere, and the occurrence of homology to RP4 in soil bacteria. Curr. Microbiol. 19: 375–381 CrossRef
van Elsas JD, Turner S, Bailey MJ (2003) Horizontal gene transfer in the phytosphere. New Phytol. 157: 525–537
van Frankenhuyzen K, Beardmore T (2004) Current status and environmental impact of transgenic forest trees. Can. J. For. Res. 34: 1163–1180
Vellice GR, Diaz Ricci JC, Hernández L, Castagnaro AP (2006) Enhanced resistance to Botrytis cinerea mediated by the transgenic expression of the chitinase gene ch5B in strawberry. Transgenic Res. 15: 57–68
Vierheilig, H, Alt-Hug, M, Wiemken, A, Boller, T (2001) Hyphal in vitro growth of the arbuscular mycorrhizal fungus Glomus mossae is affected by chitinase but not by $\beta $ -1,3-glucanase. Mycorrhiza 11: 279–282 CrossRef
Watanabe, T, Kanai, R, Kawase, T, Tanabe, T, Mitsutomi, M, Sakuda, S, Miyashita, K (1999) Family 19 chitinases of Streptomyces species, characterization and distribution. Microbiology 145: 3353–3363 CrossRef
Wiener P, Egan S, Huddleston A, Wellington E (1998) Evidence for transfer of antibiotic-resistance genes in soil populations of Streptomycetes. Mol. Ecol. 7: 1205–1216
Wolfenbarger, LL, Pfifer, PR (2000) The ecological risks and benefits of genetically engineered plants. Science 290: 2088–2093 CrossRef