Abstract
Although mycorrhizal colonization provides a bioprotectional effect against a broad range of soil-borne pathogens, including plant parasitic nematodes, the commercial use of arbuscular mycorrhizal fungi (AMF) as biocontrol agents is still in its infancy. One of the main reasons is the poor understanding of the modes of action. Most AMF mode of action studies focused on AMF-bacterial/fungal pathogens. Only few studies so far examined AMF–plant parasitic nematode interactions. Therefore, the aim of the study was to determine whether the AMF Glomus intraradices was able to incite systemic resistance in banana plants towards Radopholus similis and Pratylenchus coffeae, two plant parasitic nematodes using a split-root compartmental set-up. The AMF reduced both nematode species by more than 50%, even when the AMF and the plant parasitic nematodes were spatially separated. The results obtained demonstrate for the first time that AMF have the ability to induce systemic resistance against plant parasitic nematodes in a root system.
References
Bakker PAHM, Pieterse CMJ, Van Loon LC (2007) Induced systemic resistance by fluorescent Pseudomonas spp. Phytopathology 97:239–243
Banerjee N, De Langhe E (1985) A tissue culture technique for rapid clonal propagation and storage under minimal growth conditions of Musa (banana and plantain). Plant Cell Rep 4:351–354
Borowicz VA (2001) Do arbuscular mycorrhizal fungi alter plant-pathogen relations. Ecology 82:3057–3068
Catford JG, Staehelin C, Lerat S, Piché Y, Vierheilig H (2003) Suppression of arbuscular mycorrhizal colonization and nodulation in split-root systems of alfalfa after pre-inoculation and treatment with Nod factors. J Exp Bot 54:1481–1487
Catford JG, Staehelin C, Larose G, Piché Y, Vierheilig H (2006) Systemically suppressed isoflavonoids and their stimulating effects on nodulation and mycorrhization in alfalfa split-root systems. Plant Soil 285:257–266
Cordier C, Pozo MJ, Barea JM, Gianinazzi S, Gianinazzi-Pearson V (1998) Cell defense responses associated with localized and systemic resistance to Phytophthora parasitica induced in tomato by an arbuscular mycorrhizal fungus. Mol Plant Microbe In 11:1017–1028
de la Peña E, Rodriguez-Echevarria S, van der Putten WH, Freitas H, Moens M (2006) Mechanism of control of root-feeding nematodes by mycorrhizal fungi in the dune grass Ammophila arenaria. New Phytol 169:829–840
Declerck S, Plenchette C, Strullu DG (1995) Mycorrhizal dependency of banana (Musa acuminata, AAA group) cultivars. Plant Soil 176:183–187
Dehne HW (1982) Interactions between vesicular-arbuscular mycorrhizal fungi and plant pathogens. Phytopathology 72:1115–1119
Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209
Elsen A, Baimey H, Swennen R, De Waele D (2003a) Relative mycorrhizal dependency and mycorrhiza-nematode interaction in banana cultivars (Musa spp.) differing in nematode susceptibility. Plant Soil 256:303–313
Elsen A, Beeterens R, Swennen R, De Waele D (2003b) Effects of an arbuscular mycorrhizal fungus and two plant-parasitic nematodes in Musa genotypes differing in root morphology. Biol Fert Soils 38:367–376
Fritz M, Jakobsen I, Lyngkjaer MF, Thordal-Christensen H, Pons-Kühnemann J (2006) Arbuscular mycorrhiza reduces susceptibility of tomato to Alternaria solani. Mycorrhiza 16:413–419
Gianinazzi-Pearson V, Dumas-Gaudot E, Golotte A, Tahiri-Alaoui A, Gianinazzi S (1996) Cellular and molecular defense-related root responses to invasion by arbuscular mycorrhizal fungi. New Phytol 133:45–57
Gowen SR, Quénéhervé P, Fogain R (2005) Nematode parasites of bananas and plantains. In: Luc M, Sikora R, Bridge J (eds) Plant parasitic nematodes in subtropical and tropical agriculture, 2nd edn. CABI Publishing, Wallingford, pp 611–643
Graham JH, Drouillard DL, Hodge NC (1996) Carbon economy of sour orange in response to different Glomus spp. Tree Physiol 16:1023–1029
Hasky-Günther K, Hoffmann-Hergarten S, Sikora RA (1998) Resistance against potato cyst nematode Globodera pallida systemically induced by the rhizobacteria Agrobacterium radiobacter (G12) and Bacillus sphaericus (B43). Fund Appl Nematol 21:511–517
Hol GWH, Cook R (2005) An overview of arbuscular mycorrhizal fungi-nematode interactions. Basic Appl Ecol 6:489–503
Hooper DJ, Hallman J, Subbotin S (2005) Methods for extraction, processing and detection of plant and soil nematodes. In: Luc M, Sikora R, Bridge J (eds) Plant parasitic nematodes in subtropical and tropical agriculture, 2nd edn. CABI Publishing, Wallingford, pp 53–86
Li HY, Yang GD, Shu HR, Yang YT, Ye BX, Nishida I, Zheng CC (2006) Colonization by the arbuscular mycorrhizal fungus Glomus versiforme induces a defense response against the root-knot nematode Meloidogyne incognita in the grapevine (Vitis amurensis Rupr.), which includes transcriptional activation of the class III chitinase gene VCH3. Plant Cell Physiol 47:154–163
Khaosaad T, Garcia-Garrido JM, Steinkellner S, Vierheilig H (2007) Take-all disease is systemically reduced in roots of mycorrhizal barley plants. Soil Biol Biochem 39:727–734
Knoester M, Pieterse CMJ, Bol JF, Van Loon LC (1999) Systemic resistance in Arabidopsis induced by rhizobacteria requires ethylene-dependent signaling at the site of application. Mol Plant Microbe In 12:720–727
Liu J, Maldonado-Mendoza I, Lopez-Meyer M, Cheung F, Town CD, Harrison MJ (2007) Arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots. Plant J 50:529–544
Munif A, Hallman J, Sikora RA (2001) Induced systemic resistance of selected endophytic bacteria against Meloidogyne incognita on tomato. Med Fac Landbouww Univ Gent 66:663–669
Paulitz TC, Bélanger RR (2001) Biological control in greenhouse systems. Annu Rev Phytopathol 39:303–308
Pieterse CMJ, Van Wees SCM, Hoffland E, Van Pelt JA, Van Loon LC (1996) Systemic resistance in Arabidopsis induced by biocontrol bacteria independent of salicylic acid accumulation and pathogenesis-related gene expression. Plant Cell 8:1225–1237
Pieterse CMJ, Van Wees SCM, Van Pelt JA, Knoester M, Laan R, Gerris H, Weisbeek PJ, Van Loon LC (1998) A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10:1571–1580
Pinochet J, Fernandez C, Sarah JL (1995) Influence of temperature on in vitro reproduction of Pratylenchus coffeae, P. goodeyi and Radopholus similis. Fund Appl Nematol 18:391–392
Pinochet J, Calvet C, Camprubi A, Fernandez C (1996) Interactions between migratory endoparasitic nematodes and arbuscular mycorrhizal fungi in perennial crops: a review. Plant Soil 185:183–190
Plenchette C, Morel C (1996) External phosphorus requirements of mycorrhizal and non-mycorrhial barley and soybean plants. Biol Fert Soils 21:303–308
Pozo MJ, Cordier C, Dumas-Gaudot E, Gianinazzi S, Barea JM, Azcon-Aguilar C (2002) Localized versus systemic effect of arbuscular mycorrhizal fungi on defense responses to Phytophthora infection in tomato plants. J Exp Bot 53:525–534
Sena JOA, Labate CA, Cardoso EJBN (2004) Physiological characterization of growth depression in arbuscular mycorrhizal citrus seedlings under high P levels. Rev Bras Ciencia Solo 28:827–832
Siddiqui IA, Shaukat SS (2002) Rhizobacteria-mediated induction of systemic resistance (ISR) in tomato against Meloidogyne javanica. J Phytopathol 150:469–473
Singh R, Adholeya A, Mukerij KG (2000) Mycorrhiza in control of soil-borne pathogens. In: Mukerij KG, Chamalo BP, Singh J (eds) Mycorrhizal biology. Academic-Plenum Publishers, New York, pp 173–196
Slezack S, Dumas-Gaudot E, Paynot M, Gianinazzi S (2000) Is a fully established arbuscular mycorrhizal symbiosis required for bioprotection of Pisum sativum roots against Aphanomyces eusteiches. Mol Plant Microbe In 13:238–241
Speijer PR, De Waele D (1997) Screening of Musa germplasm for resistance and tolerance to nematodes. INIBAP Technical Guidelines N°1. INIBAP, Montpellier, France
St-Arnaud M, Vujanovic V (2007) Effect of the arbuscular mycorrhizal symbiosis on plant diseases and pests. In: Hamel C, Plenchette C (eds) Mycorrhizae in crop production: applying knowledge. Haworth Press, Binghampton, New York, pp 67–122
Vallad GE, Goodman RM (2004) Systemic acquired resistance and induced systemic resistance in conventional agriculture. Crop Sci 44:1920–1934
Van Loon LC, Bakker PAHM, Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol 36:453–483
Vierheilig H (2004) Further colonization by arbuscular mycorrhizal fungi in already mycorrhizal plants is suppressed after critical level of root colonization. J Physiol 161:339–341
Vierheilig H, Coughlan AP, Wyss U, Piché Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl Environl Microb 64:5004–5007
Vierheilig H, Garcia-Garrido JM, Wyss U, Piché Y (2000) Systemic suppression of mycorrhizal colonization of barley roots already colonized by AM fungi. Soil Biol Biochem 32:589–595
Vu T, Hauschild R, Sikora RA (2006) Fusarium oxysporum endophytes induced systemic resistance against Radopholus similis on banana. Nematology 8:847–852
Whipps JM (2004) Prospects and limitations for mycorrhizals in biocontrol of root pathogens. Can J Botany 82:1198–1227
Zhu HH, Yao Q (2004) Localized and systemic increase of phenols in tomato roots induced by Glomus versiforme inhibit Ralstonia solanacearum. J Phytopathol 152:537–542
Acknowledgement
This study was supported by a VLIR-UDC grant from the Belgian government to D. Gervacio and by a Postdoctoral Fellowship of the Research Foundation—Flanders (FWO-Vlaanderen) to A. Elsen.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Elsen, A., Gervacio, D., Swennen, R. et al. AMF-induced biocontrol against plant parasitic nematodes in Musa sp.: a systemic effect. Mycorrhiza 18, 251–256 (2008). https://doi.org/10.1007/s00572-008-0173-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00572-008-0173-6