Plant and Soil

, Volume 257, Issue 2, pp 459–470 | Cite as

Impact of auxin-compounds produced by the antagonistic fungus Pythium oligandrum or the minor pathogen Pythium group F on plant growth

  • Gaétan Le Floch
  • Patrice Rey
  • Emile Benizri
  • Nicole Benhamou
  • Yves Tirilly


Plant growth promotion induced by the antagonistic fungus, Pythium oligandrum, is the result of a complex interaction which includes an indirect effect through control of pathogens in the rhizosphere and/or a direct one mediated by plant-induced resistance. The present study shows an increased plant growth associated with direct interaction between P. oligandrum and roots, which is mediated by a fungus-produced auxin compound, tryptamine (TNH2). In vitro experiments provided evidence that P. oligandrum metabolised specifically indole derivatives, such as tryptophan and indole-3-acetaldehyde, to produce THN2 through the tryptamine pathway. When P. oligandrum grew in sterile root exudates, it also produced an auxin-like compound. Additional experiments on P. oligandrum–root interaction showed that, in amended nutrient solution of plants, the antagonist metabolised Trp into TNH2 and that root absorption of this newly formed auxin-compound in appropriate concentrations was associated with enhancement of plant growth. This phenomenon was observed only when nutrient solution was amended with low tryptophan (Trp) concentrations, i.e. 0.05 and 0.1 mM; higher concentration (0.5 and 1 mM Trp) induced abnormal root development. Similar experiments were performed with Pythium group F, a minor pathogen known for its ability to produce auxin-compounds through the tryptamine pathway. In this case, irregular root development was always noticed with all Trp concentrations added to the nutrient solution of plants. Moreover, Pythium group F colonization of roots was associated with leakage of auxin-compounds in the nutrient solution. Our results, therefore, highlight that the production of similar auxin-compounds by two Pythium species has contrary effects on plant development.

biocontrol agent plant growth promoting fungi tomato tryptamine pathway 


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  1. Bashan Y 1998 Azospirillum plant growth-promoting strains are non pathogenic on tomato, pepper, cotton, and wheat. Åan J. Microbiol. 44, 168–174.Google Scholar
  2. Benhamou N, Rey P, Åherif M, Hockenhull J and Tirilly Y 1997 Treatment with the mycoparasite, Pythium oligandrum, triggers the induction of defense related reactions in tomato roots upon challenge with Fusarium oxysporum f. sp. radicis lycopersici. Phytopathology 87, 108–122.Google Scholar
  3. Benhamou N, Bélanger R R, Rey P and Tirilly Y 2001 Oligandrin, the elicitin-like protein produced by the mycoparasite Pythium oligandrum, induces systemic resistance to Fusarium crown and root rot in tomato plants. Plant Physiol. Biochem. 39, 681–696.Google Scholar
  4. Benizri E, Åourtade A, Picard Å and Guckert A 1998 Role of maize root exudates in the production of auxins by Pseudomonas fluorescens M.3.1. Soil Biol. Biochem. 30, 1481–1484.Google Scholar
  5. Benizri E, Baudoin E and Guckert A 2001 Root colonization by inoculated plant-growth rhizobacteria. Biocontrol Sci. Techn. 11, 557–574.Google Scholar
  6. Bloemberg G V and Lugtenberg B J J 2001 Molecular basis of plant growth promotion and biocontrol by rhizobacteria. Åurr. Opin. Plant Biol. 4, 343–350.Google Scholar
  7. Åooney T P and Nonhebel H M 1991 Biosynthesis of indole-3-acetic acid in tomato shoots: measurement, mass spectral identi-fication and incorporation of 2H from 2H2O into indole-3-acetic acid, D-and L-tryptophan, indole-3-pyruvate and tryptamine. Planta 184, 368–376.Google Scholar
  8. Åostacurta A and Vanderleyden J 1995 Synthesis of phytohormones by plant-associated bacteria. Årit. Rev. Microbiol. 21, 1–18.Google Scholar
  9. Frankenberger WT and Arshad M 1995 Phytohormones in soil: microbial production and function. Dekker, New York, USA. 493 pp.Google Scholar
  10. Gagné S, Dehbi L, Le Quéré D, Åayer F, Morin J L, Lemay R and Fournier N 1993 Increase of greenhouse tomato fruit yields by plant growth-promoting rhizobacteria (PGPR) inoculated into the peat-based growing media. Soil Biol. Biochem. 25, 269–272.Google Scholar
  11. Gay G, Rouillon R, Bernillon J and Favre-Bonvin J 1989 IAA biosynthesis by the ectomycorrhizal fungus Hebeloma hiemale as affected by different precursors. Åan. J. Bot. 67, 2235–2239.Google Scholar
  12. Hoagland D R and Arnon D I 1938 The water culture method of growing plants without soil. Univ. Åalif. Åoll. Agric. Exp. Sta. Åirc. Berkeley. 347–352.Google Scholar
  13. Hong Y, Pasternak J J and Glick B R 1991 Biological consequences of plasmid transformation of the plant growth-promoting rhibacterium Pseudomonas putida GR12-2. Åan. J. Microbiol. 37, 796–799.Google Scholar
  14. Kampert M and Strzelczyk E 1975 Synthesis of auxins by fungi isolated from the roots of pine seedlings (Pinus silvestris L.) and from soil. Acta Microbiol. Pol. 7, 223–230.Google Scholar
  15. Keogh R Å and Deverall B J 1980 Åomparison of histological and physiological responses to Phakopsora pachyrhizi in resistant and susceptible soybean. Trans. Br. Mycol. Soc. 74, 329–333.Google Scholar
  16. Kleifeld O and Åhet I 1992 Trichoderma harzanium – Interaction with plants and effect on growth response. Plant Soil 144, 267–272.Google Scholar
  17. Kloepper J W, Leong J, Teintze M and Schroth M N 1980 Enhancement of plant growth by siderophores produced by plant growth promoting rhizobacteria. Nature 286, 885–886.Google Scholar
  18. Kloepper J W, Zablotowicz R M, Tipping E M and Lifshitz R 1991 Plant growth promotion mediated by bacterial rhizosphere colonizers. In The Rhizosphere and Plant Growth. Eds. D L Keister and P B Åregan. pp. 315–326. Kluwer Academic Publishers, Dordrecht, The Netherlands.Google Scholar
  19. Kratka J, Bergmanova E and Kudelova A 1994 Effect of Pythium oligandrum and Pythium ultimum on biochemical changes in cucumber (Åucumis sativus L.). J. Plant Dis. Protect. 92, 417–419.Google Scholar
  20. Lalande R, Bissonnette N, Åoutlée D and Antoun H 1989 Identification of rhizobacteria from maize and determination of their plant growth promoting potential. Plant Soil 115, 7–11.Google Scholar
  21. Le Floch G, Rey P, Déniel F, Benhamou N, Picard K and Tirilly Y 2003 Enhancement of development and induction of resistance in tomato plants by the antagonist, Pythium oligandrum. Agronomie. 23, 455–460.Google Scholar
  22. Lifshitz R, Kloepper J W, Koslowski M, Simonson Å, Åarlson J, Tipping E M and Zaleska I 1987 Growth promotion of canola seedlings by a strain of Pseudomonas putida under gnotobiotic conditions. Åan. J. Microbiol. 33, 390–395.Google Scholar
  23. Noel T Å, Sheng Å, Yost Å K, Pharis R P and Hynes M F 1996 Rhizobium leguminosarum as a plant growth-promoting rhizobacterium: direct growth promotion of canola and lettuce. Åan. J. Microbiol. 42, 279–283.Google Scholar
  24. Patten Å L and Glick B R 1996 Bacterial biosynthesis of indole-3-acetic acid. Åan. J. Microbiol. 42, 207–220.Google Scholar
  25. Picard K, Ponchet M, Blein J P, Rey P, Tirilly Y and Benhamou N 2000 Oligandrin, a proteinaceous molecule produced by the mycoparasite, Pythium oligandrum, induces resistance to Phytophthora parasitica infection in tomato plants. Plant Physiol. 124, 379–395.Google Scholar
  26. Pilet P E and Saugy M 1987 Effect on root growth of endogenous and applied IAA and ABA. Plant Physiol. 83, 33–38.Google Scholar
  27. Raupach G S and Kloepper J W 1998 Mixtures of plant growthpromoting rhizobacteria enhance biological control of multiple cucumber pathogens. Phytopathology 88, 1158–1164.Google Scholar
  28. Rey P, Benhamou N and Tirilly Y 1996 Ultrastructural and cytochemical studies of cucumber root infected by two Pythium species with different modes of pathogenicity. Physiol. Mol. Plant P. 44, 213–231.Google Scholar
  29. Rey P, Nodet P and Tirilly Y 1997 Pythium F induce a minor but ubiquitous disease in tomato soilless cultures. J. Plant Pathol. 79, 173–180.Google Scholar
  30. Rey P, Benhamou N and Tirilly Y 1998a Ultrastructural and cytochemical investigation of asymptomatic infection by Pythium spp. Phytopathology 88, 234–244.Google Scholar
  31. Rey P, Benhamou N, Wulff E and Tirilly Y 1998b Interactions between tomato (Lycopersicon esculentum) root tissues and the mycoparasite Pythium oligandrum. Physiol. Mol. Plant P. 53, 105–123.Google Scholar
  32. Rey P, Leucart S, Désilets H, Bélanger R, Larue J P and Tirilly Y 2001 Production of auxin and tryptophol by Pythium ul470 timum and minor pathogen, Pythium group F: Possible role in pathogenesis. Eur. J. Plant Pathol. 107, 895–904.Google Scholar
  33. Rybicka H 1981 Tryptophan in root exudate of mock orange and tomato. Acta Physiol. Plant. 3, 95–98.Google Scholar
  34. Simons M, Permentier H, De Weger L A, Wijffelman Å A and Lugtenberg B J J 1997 Amino acid synthesis is necessary for tomato root colonization by Pseudomonas fluorescens strain WÅS365. Mol. Plant Microbe In. 10, 102–106.Google Scholar
  35. Taiz L and Zeiger E 1998 Auxins. In Plant Physiology. Eds. L Taiz and E Zeiger. pp. 543–589. Sinauer Associates, Sunderland, Massassuchets, USA.Google Scholar
  36. Tudzynski B 1997 Fungal phytohormones in pathogenic and mutualistic associations. In The Mycota V Part A Plant relationships. Eds. G Å Åarroll and B Tudzynski. pp. 167–184. Springer Verlag, Berlin.Google Scholar
  37. Whipps J M 1997 Developments in the biological control of soilborne plant pathogens. Adv. Bot. Res. 26, 1–134.Google Scholar
  38. Whipps J M 2001 Microbial interactions and biocontrol in the rhizosphere. J. Exp. Bot. 52, 487–511.Google Scholar
  39. Wulff E, Pham A T H, Åhérif M, Rey P, Tirilly Y and Hockenhull J 1998 Inoculation of cucumber roots with zoospore of mycoparasitic and plant pathogenic Pythium species: Differential zoospore accumulation, colonization ability and plant growth response. Eur. J. Plant. Pathol. 104, 69–76.Google Scholar
  40. Yedidia I, Benhamou N and Åhet I 1999 Induction of defense responses in cucumber plants (Åucumis sativus L.) by the biocontrol agent Trichoderma harzianum. Appl Environ. Microb. 65, 1061–70.Google Scholar
  41. Yedidia I, Srivastva A K, Kapulnik Y and Åhet I 2001 Effect of Trichoderma harzianum on microelement concentrations and increased growth of cucumber plants. Plant Soil. 235, 235–242.Google Scholar

Copyright information

© Kluwer Academic Publishers 2003

Authors and Affiliations

  • Gaétan Le Floch
    • 1
  • Patrice Rey
    • 1
  • Emile Benizri
    • 2
  • Nicole Benhamou
    • 3
  • Yves Tirilly
    • 1
  1. 1.Laboratoire de Microbiologie et Sécurité AlimentaireUniversité de Bretagne Occidentale-Brest, Technopôle Brest-IroisePlouzanéFrance
  2. 2.UMR Agronomie Environnement INPL-ENSAIA-INRAVandoeuvre-les-NancyFrance
  3. 3.Département Recherche en Sciences de la Vie et de la Santé, Pav. Ch.E. MarchandUniversité LavalSainte-FoyCanada

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