Interactions between engineered tomato plants expressing antifungal enzymes and nontarget fungi in the rhizosphere and phyllosphere

FEMS Microbiology Letters

Volumn 288, Issue 1, 2008, Pages 9-18

  Girlanda, Mariangela ^a   Bianciotto, Valeria ^a   Cappellazzo, Gilda Antonella ^a   Casieri, Leonardo ^a   Bergero, Roberta ^a   Martino, Elena ^a   Luppi, Anna Maria ^a   Perotto, Silvia ^a  

^a UNIVERSITY OF TURIN   (Italy)

Author keywords

Biodiversity; GMOs; GMPs; Pathogenesis related proteins; Risk assessment; Solanum lycopersicum

Indexed keywords

1,3 BETA GLUCANASE; CHITINASE;

ARBUSCULAR MYCORRHIZA; ARTICLE; CONTROLLED STUDY; DISCRIMINANT ANALYSIS; FUNGAL COLONIZATION; FUNGAL COMMUNITY; GENE EXPRESSION; GREENHOUSE; GROWTH CURVE; MICROBIAL DIVERSITY; MICROCOSM; MICROMYCETE; MORPHOTYPE; NONHUMAN; ORGANISM COLONY; PHYLLOSPHERE; PLANT FUNGUS INTERACTION; PLANT GROWTH; PRIORITY JOURNAL; RHIZOSPHERE; SAPROTROPH; TOBACCO; TOMATO; TRANSGENIC PLANT; WILD TYPE;

ANTIFUNGAL AGENTS; CHITINASE; FUNGI; GENETIC ENGINEERING; GLUCAN 1,3-BETA-GLUCOSIDASE; LYCOPERSICON ESCULENTUM; PLANT LEAVES; PLANT PROTEINS; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; TOBACCO;

ARBUSCULAR; FUNGI; LYCOPERSICON ESCULENTUM; NICOTIANA TABACUM;

EID: 52649083809     PISSN: 03781097     EISSN: 15746968     Source Type: Journal    
DOI: 10.1111/j.1574-6968.2008.01306.x     Document Type: Article

References (57)

1. Albo AG, Mila S, Digilio G, Motto M, Aime S Corpillo D (2007) Proteomic analysis of a genetically modified maize flour carrying Cry1Ab gene and comparison to the corresponding wild-type. Maydica 52 : 443 455.
2. Berg G, Zachow C, Lottmann J, Götz M, Costa R Smalla K (2005) Impact of plant species and site on rhizosphere-associated fungi antagonistic to Verticillium dahliae Kleb. Appl Environ Microb 71 : 4203 4213.
3. Bettini P, Cosi E, Pellegrini MG, Turbanti L, Vendramin GG Buiatti M (1998) Modification of competence for in vitro response to Fusarium oxysporum in tomato cells. III. PR-protein gene expression and ethylene evolution in tomato cell lines transgenic for phytohormone related bacterial genes. Theor Appl Genet 97 : 575 583.
4. Bieri S, Potrykus I Fütterer J (2003) Effects of combined expression of antifungal barley seed proteins in transgenic wheat on powdery mildew infection. Mol Breeding 11 : 37 48.
5. Boller T (1993) Antimicrobial functions of the plant hydrolases, chitinase and b-1,3-glucanase. Mechanisms of Plant Defense Responses (Fritig B Legrand M, eds), pp. 391 400. Kluwer Academic Publishers, Dordrecht.
6. 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.
7. Dighton J (2003) Fungi in Ecosystem Processes. Marcel Dekker Inc., New York, 432 pp.
8. Dix NJ Webster J (1995) Fungal Ecology. Chapman & Hall, London, 549 pp.
9. Domsch KH, Gams W Anderson TH (1980) Compendium of Soil Fungi. IHW-Verlag, Eching, 859 pp.
10. Donegan KK, Palm CJ, Fieland VJ, Porteus 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.
11. Donegan KK, Schaller DL, Stone JK, Ganio LM, Reed G, Hamm PB Seidler RJ (1996) Microbial populations, fungal species diversity and plant pathogen levels in field plots of potato plants expressing the Bacillus thuringiensis var tenebrionis endotoxin. Transgenic Res 5 : 25 35.
12. Donegan KK, Seidler RJ, Fieland VJ, Schaller DL, Palm CJ, Ganio LM, Cardwell DM Steinberger Y (1997) Decomposition of genetically engineered tobacco under field conditions: persistence of the proteinase inhibitor I product and effects on soil microbial respiration and protozoa, nematode and microarthropod populations. J Appl Ecol 34 : 767 777.
13. Escher N, Kach B Nentwig W (2000) Decomposition of transgenic Bacillus thuringiensis maize by micro-organisms and woodlice Porcello scaber (Crustacea: Isopoda). Basic Appl Entomol 1 : 161 169.
14. Fokkema NJ van den Heuvel J (1986) Microbiology of the Phyllosphere. Cambridge University Press, Cambridge.
15. Fuchs J-G, Moënne-Loccoz Y Défago G (1997) Nonpathogenic Fusarium oxysporum strain Fo47 induces resistance to Fusarium wilt in tomato. Plant Dis 81 : 492 496.
16. Gams W (1992) The analysis of communities of saprophytic microfungi with special reference to soil fungi. Fungi in Vegetation Science (Winterhoff W, ed), pp. 183 223. Kluwer Academic Publishers, Dordrecht.
17. Gerlach W Nirenberg H (1982) The genus Fusarium - A pictorial Atlas. Biologischen Bundesanstalt für Land und Forstwirtschaft, Berlin.
18. Girlanda M, Perotto S, Moënne-Loccoz Y, Bergero R, Lazzari A, Défago G, Bonfante P Luppi AM (2001) Impact of biocontrol Pseudomonas fluorescens CHA0 and a genetically modified derivative on the diversity of culturable fungi in the cucumber rhizosphere. Appl Environ Microb 67 : 1851 1864.
19. Glandorf DCM, Bakker PAHM van Loon LC (1997) Influence of the production of antibacterial and antifungal proteins by transgenic plants on the saprophytic soil microflora. Acta Bot Neerl 46 : 85 104.
20. Gongora CE Broadway RM (2002) Plant growth and development influenced by transgenic insertion of bacterial chitinolytic enzymes. Mol Breeding 9 : 123 135.
21. Halterman DA, Kramer LC, Wielgus S Jiang JM (2008) Performance of transgenic potato containing the late blight resistance gene RB. Plant Dis 92 : 339 343.
22. Han YH, Griffiths A, Li H Grierson D (2004) The effect of endogenous mRNA levels on co-suppression in tomato. FEBS Lett 563 : 123 128.
23. Honée G (1999) Engineered resistance against fungal plant pathogens. Eur J Plant Pathol 105 : 319 326.
24. Jongedijk E, Tigelaar H, Van Roekel JSC, Bres-Vloermans SA, Van de Elzen PJM, Cornelissen BJC Melchers LS (1995) Synergistic activity of chitinases and β-1,3-glucanases enhances fungal resistance in transgenic tomato plants. Euphytica 85 : 173 180.
25. Joosten MHAJ, Verbakel HM, Nettekooven ME, Van Leeuwen J, van der Vossen RTM deWit PJGM (1995) The phytopathogenic fungus Cladosporium fulvum is not sensitive to the chitinase and beta-1,3-glucanase defence proteins of its host tomato. Physiol Mol Plant P 46 : 45 59.
26. Kirk PM, Cannon PF, David JC Stalpers JA (2001) Ainsworth and Bisby's Dictionary of the Fungi, 9th edn. CABI Publishing, Egham, 655 pp.
27. Kunz C, Schob H, Leubner-Metzge G, Glazov E Meins F (2001) Beta-1,3-glucanase and chitinase transgenes in hybrids show distinctive and independent patterns of posttranscriptional gene silencing. Planta 212 : 243 249.
28. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 : 680 685.
29. Lanfranco L, Delpero M Bonfante P (1999) Intrasporal variability of ribosomal sequences in the endomycorrhizal fungus Gigaspora margarita. Mol Ecol 8 : 37 45.
30. Lawrence CB, Singh NP, Qiu J, Gardner RG Tuzun S (2000) Constitutive hydrolytic enzymes are associated with polygenic resistance of tomato to Alternaria solani and may function as an elicitor release mechanism. Physiol Mol Plant P 57 : 211 220.
31. Lorito M, Woo SL, Fernandez IG et al 1998) Genes from mycoparasitic fungi as a source for improving plant resistance to fungal pathogens. Proc Natl Acad Sci USA 95 : 7860 7865.
32. Lynch JM, Benedetti A, Insam H, Nuti MP, Smalla K, Torsvik V Nannipieri P (2004) Microbial diversity in soil: ecological theories, the contribution of molecular techniques and the impact of transgenic plants and transgenic microorganisms. Biol Fertil Soils 40 : 363 385.
33. Magurran AE (1988) Ecological Diversity and Its Measurement. Chapman and Hall, London.
34. Melchers LS, Sela-Buurlage MB, Vloemans SA, Woloshuk CP, Vanroekel JSC, Pen J, van den Elzen PJM Cornelissen BJC (1993) Extracellular targeting of the vacuolar tobacco proteins AP24, chitinase and beta-1,3- glucanase in transgenic plants. Plant Mol Biol 21 : 583 593.
35. 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 : 23 39.
36. Mondal KK, Chatterjee SC, Viswakarma N, Bhattacharya RC Grover A (2003) Chitinase-mediated inhibitory activity of Brassica transgenic on growth of Alternaria brassicae. Curr Microbiol 47 : 171 173.
37. Montesinos E (2007) Antimicrobial peptides and plant disease control. FEMS Microbiol Lett 270 : 1 11.
38. O'Callaghan M, Gerard EM, Waipara NW, Young SD, Glare TR, Barrell PJ Conner AJ (2004) Microbial communities of Solanum tuberosum and magainin-producing transgenic lines. Plant Soil 266 : 47 56.
39. Ohme-Takagi M Shinshi H (1990) Structure and expression of a tobacco beta-1,3-glucanase gene. Plant Mol Biol 15 : 941 946.
40. Sanders M, Maddelein W, Depicker A, Van Montagu M, Cornelissen M Jacobs J (2002) An active role for endogenous beta-1,3-glucanase genes in transgene-mediated co-suppression in tobacco. EMBO J 21 : 5824 5832.
41. Sela-Buurlage MB, Ponstein AS, Bres Vloemans SA, Melchers LS, Van den Elzen PJM Cornelissen BJC (1993) Only specific tobacco (Nicotiana tabacum) chitinases and beta-1,3-glucanases exhibit antifungal activity. Plant Physiol 101 : 857 863.
42. Siddiqui IA Shaukat SS (2003) Effects of Pseudomonas aeruginosa on the diversity of culturable microfungi and nematodes associated with tomato: impact on root-knot disease and plant growth. Soil Biol Biochem 35 : 1359 1368.
43. Singh OV, Shivani G, Debarati P Rakesh KJ (2006) Genetically modified crops: success, safety assessment, and public concern. Appl Microbiol Biot 71 : 598 607.
44. Smith CJ, Watson CF, Bird CR, Ray J, Schuch W Grierson D (1990) Expression of a truncated tomato polygalacturonase gene inhibits expression of the endogenous gene in transgenic plants. Mol Gen Genet 224 : 477 481.
45. Stam M, Mol JNM Kooter JM (1997) The silence of genes in transgenic plants. Ann Bot 79 : 3 12.
46. Tabaeizadeh Z, Agharbaoui Z, Harrak H Poysa V (1999) Transgenic tomato plants expressing a Lycopersicon chilense chitinase gene demonstrate improved resistance to Verticillium dahliae race 2. Plant Cell Rep 19 : 197 202.
47. Tahiri-Alaoui GR, Gianinazzi-Pearson V, Toppan A Gianinazzi S (1994) The impact of the constitutive expression of chitinases in roots of transgenic tobacco on arbuscular mycorrhizal fungi. Edinburgh: 7th International Symposium on Molecular Plant Microbe Interactions, p. 406.
48. Trouvelot A, Kough JL Gianinazzi-Pearson V (1986) Mesure du taux de mycorhization VA d'un système radiculaire. Recherche de méthodes d'estimation ayant une signification fonctionnelle. Physiological and Genetical Aspects of Mycorrhizae (Gianinazzi-Pearson V Gianinazzi S, eds), pp. 217 221. INRA Press, Paris.
49. Van Buuren M, Neuhaus JM, Shinshi H, Ryals J Meins FJR (1992) The structure and regulation of homologous tobacco endochitinase genes of Nicotiana sylvestris and N. tomentosiformis origin. Mol Gen Genet 232 : 460 469.
50. Van Kan JAL, Joosten MHAJ, Wagemakers CAM, Van Den Bergvelthuis GCM deWit PJGM (1992) Differential accumulation of messenger RNAs encoding extracellular and intracellular PR proteins in tomato induced by virulent and avirulent races of Cladosporium fulvum. Plant Mol Biol 20 : 513 527.
51. Viebahn M, Glandorf DCM, Ouwens TWM, Smit E, Leeflang P, Wernars K, Thomashow LS, van Loon LC Bakker PAHM (2003) Repeated introduction of genetically modified Pseudomonas putida WCS358r without intensified effects on the indigenous microflora of field-grown wheat. Appl Environ Microbiol 69 : 3110 3118.
52. Vierheilig H, Alt M, Neuhaus JM, Böller T Wiemken A (1993) Colonization of transgenic Nicotiana sylvestris plants, expressing different forms of Nicotiana tabacum chitinase, by the root pathogen Rhizoctonia solani and by the mycorrhizal symbiont Glomus mosseae. Mol Plant Microbe Int 6 : 261 264.
53. Vierheilig H, Alt M, Lange J, Gut-Rella M, Wiemken A Böller T (1995) Colonization of transgenic tobacco constitutively expressing pathogenesis-related proteins by the vescicular-arbuscular mycorrhizal fungus Glomus mosseae. Appl Environ Microbiol 61 : 3031 3034.
54. von Arx JA (1980) The Genera of Fungi Sporulating in Pure Culture, 3rd edn. J. Cramer, Vaduz 424 pp.
55. Widden P (1986) Microfungal community structure from forest soils in southern Quebec, using discriminant function and factor analysis. Can J Bot 64 : 1402 1412.
56. Wróbel-Kwiatkowskaa M, Lorenc-Kukulaa K, Starzyckib M, Oszmiañskic J, Kepczyñskad E Szopaa J (2004) Expression of b-1,3-glucanase in flax causes increased resistance to fungi. Physiol Mol Plant P 65 : 245 256.
57. Wubben JP, Joosten MHAJ, Van Kan JAL deWit PJGM (1992) Subcellular localization of plant chitinases and beta-1,3-glucanases in Cladosporium fulvum (syn. Fulvia fulva)-infected tomato leaves. Physiol Mol Plant P 41 : 23 32.