Abstract
Endophytic bacteria (Pseudomonas aeruginosa UPMP3 and Burkholderia cepacia UMPB3), isolated from within roots of oil palm (Elaeis guineensis Jacq.) were tested for their presymbiotic effects on two arbuscular mcorrhizal fungi, Glomus intraradices UT126 and Glomus clarum BR152B). These endophytic bacteria were also tested for antagonistic effects on Ganoderma boninense PER 71, a white wood rot fungal pathogen that causes a serious disease in oil palm. Spore germination and hyphal length of each arbuscular mycorrhizal fungal (AMF) pairing with endophytic bacteria was found to be significantly higher than spores plated in the absence of bacteria. Scanning electron microscopy (SEM) showed that the endophytic bacteria were scattered, resting or embedded on the surface hyaline layer or on the degraded walls of AMF spores, possibly feeding on the outer hyaline spore wall. The antagonistic effect of the endophytic bacteria was expressed as severe morphological abnormalities in the hyphal structures of G. boninense PER 71. The effects of the endophytic bacteria on G. boninense PER 71 hyphal structures were observed clearly under SEM. Severe inter-twisting, distortion, lysis and shriveling of the hyphal structures were observed. This study found that the effect of endophytic bacteria on G. intraradices UT126 and G. clarum BR152B resembled that of a mycorrhiza helper bacteria (MHB) association because the association significantly promoted AMF spore germination and hyphal length. However, the endophytic bacteria were extremely damaging to G. boninense PER 71.
We’re sorry, something doesn't seem to be working properly.
Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.
References
Barea, J.M., G. Andrade, V. Bianciatto, D. Dowling, S. Lohrke, P. Bonfante, F. O’gara, and C. Azcon-Aguilar. 1998. Impact on arbuscular mycorrhiza formation on Pseudomonas strains used as inoculants for biocontrol of soil borne fungal plant pathogens. Appl. Environ. Microbiol. 64, 2304–2307.
Bianciotto, V. and P. Bonfante. 2002. Arbuscular mycorrhizal fungi: a specialized niche for rhizospheric and endocellular bacteria. Antonie van Leeuwenhoek 81, 365–371.
Blal, B. and V. Gianizazzi-Pearson. 1990. Interest of endomycorrhizae for the production of micropropagated oil palm clones. Agric. Ecosyst. Environ. 29, 39–43.
Brooks, D.S., C.F. Gonzales, D.N. Appel, and T.H. Filer. 1994. Evaluation of endophytic bacteria as potential biological control agents for oak wilt. Biol. Control 4, 373–381. DOI:10.1006/bcon.1994.1047.
Brundrett, M., N. Bougher, B. Dell, and N. Malajczuk. 1997. Working with mycorrhizas in forestry and agriculture, pp. 162–171. ACIAR Monograph 32, Pirie Printers, Canberra, Australia.
Budi, S.W., D. van Tuinen, G. Martinotti, and S. Gianinazzi. 1999. Isolation from the Sorghum bicolor mycorrhizosphere of a bacterium compatible with arbuscular mycorrhiza development and antagonistic towards soil borne fungal pathogens. Appl. Environ. Microbiol. 65, 5148–5150.
Chen, C., R.R. Belanger, N. Benhamou, and T.C. Paulitz. 2000. Defense enzymes induced in cucumber roots by treatment with plant growth promoting rhizobacteria (PGPR) and Pythium aphanidermatum. J. Physiol. Mol. Plant Pathol. 56, 13–23.
Fisher, P.J., O. Petrini, and S.H.M. Lazpin. 1992. The distribution of some fungal and bacterial endophytes in maize (Zea mays L.). New Phytol. 122, 299–305.
Frey-Klett, P., J. Garbaye, and M. Tarkka. 2007. The mycorrhiza helper bacteria revisited. New Phytol. 176, 22–36.
Gamalero, E., M.G. Martinotti, A. Trotta, P. Lemanceau, and G. Berta. 2002. Morphogenetic modifications induced by Pseudomonas fluorescens A6RI and Glomus mosseae BEG12 in the root system of tomato differ according to plant growth. New Phytol. 155, 293–300.
Garbaye, J. 1994. Helper bacteria: a new dimension to the mycorrhizal symbiosis. New Phytol. 128, 197–210.
Gomez, K.A. and A.A. Gomez. 1984. Statistical procedures for agricultural research, 2nd ed., p. 680. J. Wiley, New York, NY, USA.
Gordon, T.R. and D. Okamoto. 1992. Population structure and relationship between pathogenic and non-pathogenic strains of Fusarium oxysporum. Phytopathology 82, 73–77.
Gupta, C.P., R.C. Dubey, S.C. Kang, and D.K. Maheswari. 2001. Antibiosis-mediated necrotrophic effect of Pseudomonas GRC2 against two fungal pathogens. Curr. Sci. 81, 91–94.
Hildebrandt, U., F. Ouziad, F.J. Marner, and H. Bothe. 2006. The bacterium Paenibacillus validus stimulates growth of the arbuscular mycorrhizal fungus Glomus intraradices up to the formation of fertile spores. FEMS Microbiol. Lett. 254, 258–267.
Hollis, J.P. 1951. Bacteria in healthy potato tissue. Phytopathology 41, 320–366.
Jinantana, J. and M. Sariah. 1998. Potential for biological control of Slerotium foot rot of chilli by Trichoderma spp. Pertanika J. Tropical Agriculture Sci. 21, 1–10.
Lieven, K.H., V.R. Rijsbergen, F.R. Leyns, B.J. Lambert, P. Tenning, J. Swings, and H.J.P. Joos. 1989. Dominant rhizosphere bacteria as a source of antifungal agents. J. Pestic. Sci. 27, 141–154.
Liu, S.F. and W.H. Tang. 1996. The study on endophytic streptomyces of cotton, pp. 212–213. In W.H. Tang, R.J. Cook, and A. Rovira (eds.), Advances in biological control of plant diseases. China Agricultural University Press, China.
Macdonald, R.M. and M.R. Chandler. 1981. Bacterium like organelles in the vesicular mycorrhizal fungus Glomus caledonius. New Phytol. 89, 241–246.
Mathivanan, N., V.R. Prabavathy, and V.R. Vijayanandraj. 2005. Application of talc formulations of Pseudomonas fluorescens Migula and Trichoderma viride Pers. ex S. F. Gray decrease the sheath blight disease and enhance the plant growth and yield in rice. J. Phytopathol. 153, 697–701.
Mosse, B. 1962. The establishment of vesicular-arbuscular mycorrhiza under aseptic conditions. J. Gen. Microbiol. 27, 509–520.
Nadarajah, P. 1980. Species of endogonaceae and mychorrhizal association of Elaeis guineensis and Theobroma cacao, pp. 232–237. In P. Mikola (ed.), Tropical Mycorrhiza Research. Clarendon Press, Oxford, USA.
Offre, P., B. Pivato, S. Siblot, E. Gamalero, T. Corberand, P. Lemanceau, and C. Mougel. 2007. Identification of bacterial groups preferentially associated with mycorrhizal roots of Medicago truncatula. Appl. Environ. Microbiol. 73, 913–921.
Pivato, B., P. Offre, S. Marchelli, B. Barbonaglia, C. Mougel, P. Lemanceau, and G. Berta. 2009. Bacterial effects on arbuscular mycorrhizal fungi and mycorrhiza development as influenced by the bacteria, fungi and host plant. Mycorrhiza 19, 81–90.
Rees, R.W., J. Flood, Y. Hasan, and R.M. Cooper. 2007. Effects of inoculum potential, shading and soil temperature on root infection of oil palm seedlings by the basal stem rot pathogen Ganoderma boninense. Plant Pathol. 56, 862–870.
Roesti, D., K. Ineichen, O. Braissant, D. Redecker, A. Wiemken, and M. Aragno. 2005. Bacteria associated with spores of the arbuscular mycorrhizal fungi Glomus geosporum and Glomus constrictum. Appl. Environ. Microbiol. 71, 6673–6679.
Sanderson, F.R. 2005. An insight into dispersal of Ganoderma boninense on oil palm. Mycopathologia 159, 139–141.
Sbrana, C., L. Avio, and M. Giovannetti. 1995. The occurrence of Calcofluor and lectin-binding polysaccharides in the outer wall of arbuscular mycorrhiza fungal spores. Mycol. Res. 99, 1249–1252.
Schippers, B., A.W. Bakker, P.A.H.M. Bakker, and R. Van Peer. 1991. Beneficial and deleterious effects of HCN-producing Pseudomonads on rhizosphere interactions, pp. 211–219. In D.L. Keister and P.B. Cregan (eds.), The rhizosphere and plant growth. Kluwer, Dordrecht, The Netherlands.
Schulz, B. and B. Boyle. 2006. What are endophytes?, pp. 2–13. In B. Schulz, C. Boyle, and T.N. Sieber (eds.), Microbial root endophytes. Springer-Verlag Berlin Heidelberg, Germany.
Selim, S., J. Negrel, C. Govaerts, S. Gianinazzi, and D. van Tuinen. 2005. Isolation and partial characterization of antagonistic peptides produced by Paenibacillus sp. strain B2 isolated from the sorghum mycorrhizosphere. Appl. Environ. Microbiol. 71, 6501–6507.
Shamala, S., F. Abdullah, A.M. Zainal, and K.Y. Umi. 2008. Efficacy of single and mixed treatments of Trichoderma harzianum as biocontrol agents of Ganoderma basal stem rot in oil palm. J. Oil Palm Res. 20, 470–483.
Siddiqui, Z.A. 2005. PGPR: Prospective biocontrol agents of plant pathogens, pp. 111–142. In Z.A. Siddiqui (ed.), PGPR: Biocontrol and biofertilization. Springer, The Netherlands.
Siddiqui, I.A. and S.S. Shaukat. 2003. Combination of Pseudomonas aeruginosa and Pochonia chlamydosporia for control of root-infecting fungi in tomato. J. Phytopathol. 151, 215–222.
Siti Ramlah, A.A. and D.M. Tayeb. 1991. Status of mycorrhizal research in oil palm. PORIM Buletin 23, 4–14.
Smith, S.E. and D.J. Read. 2008. Arbuscular Mycorrhiza, pp. 14–15. In Mycorrhizal symbiosis (Third edition). Academic Press Elsevier, London, UK.
Strobel, G.A. and D.M. Long. 1998. Endophytic microbes embody pharmaceutical potential. ASM News 64, 263–268.
Sturtz, A.V., B.R. Christie, and J. Nowak. 2000. Bacterial endophytes: potential role in developing sustainable systems of crop production. Crit. Rev. Plant Sci. 19, 1–30.
Sumathi, S., S.P. Chai, and A.R. Mohamed. 2008. Utilization of oil palm as a source of renewable energy in Malaysia. Renew Sust. Energ. Rev. 12, 2404–2421.
Susanto, A., P.S. Sudharto, and R.Y. Purba. 2005. Enhancing biological control of basal stem rot disease (Ganoderma boninense) in oil palm plantations. Mycopathologia 159, 153–157.
Sylvie, C., V. Liesbeth, B. Celine, R. Laurent, S. Désiré-Georges, and D. Stéphane. 2005. Methodologies for in vitro cultivation of arbuscular mycorrhizal fungi with root organs, pp. 341–372. In S. Declerck, D.G. Strullu, and J.A. Fortin (eds.). In vitro culture of mycorrhizas. Springer-Verlag Berlin, Hiedelberg, Germany.
Szczech, M. and M. Shoda. 2004. Biocontrol of Rhizoctonia damping-off of tomato by Bacillus subtilis combined with Burkholderia cepacia. J. Phytopathol. 152, 549–556.
Van Loon, L.C. and P.A.H.M. Bakker. 2005. Induced systemic resistance as a mechanism of disease suppression by rhizobacteria, pp. 39–66. In Z.A. Siddiqui (ed.), PGPR: Biocontrol and biofertilization. Springer, The Netherlands.
Viswanathan, R. and R. Samiyappan. 2002. Induced systemic resistance by fluorescent pseudomonas against red rot disease of sugarcane caused by Colletotrichum falcatum. Crop Prot. 21, 1–10.
Whitesides, S.K. and R.A. Spotts. 1991. Frequency, distribution and characteristics of endophytic Pseudomonas syringae in pear trees. J. Phytopathol. 81, 453–457.
Xavier, L.J.C. and J.J. Germida. 2003. Bacteria associated with Glomus clarum spores influence mycorrhizal activity. Soil Biol. iochem. 35, 471–478.
Zaiton, S., M. Sariah, and Z.A.M. Ahmad. 2008. Effect of endophytic bacteria on growth and suppression of Ganoderma boninense infection in oil palm. Int. J. Agricul. Biol. 10, 127–132.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Sundram, S., Meon, S., Seman, I.A. et al. Symbiotic interaction of endophytic bacteria with arbuscular mycorrhizal fungi and its antagonistic effect on Ganoderma boninense . J Microbiol. 49, 551–557 (2011). https://doi.org/10.1007/s12275-011-0489-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12275-011-0489-3