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Effect of the combined inoculation of arbuscular mycorrhizal fungi and plant growth-promoting rhizobacteria on papaya (Carica papaya L.) infected with the root-knot nematode Meloidogyne incognita

Published online by Cambridge University Press:  30 June 2006

María del Carmen Jaizme-Vega
Dpto. Protección Vegetal, Instituto Canario Investigaciones Agrarias, Apdo. 60, 38200 La Laguna, Tenerife, España
Ana Sue Rodríguez-Romero
Dpto. Protección Vegetal, Instituto Canario Investigaciones Agrarias, Apdo. 60, 38200 La Laguna, Tenerife, España
Luis Antonio Barroso Núñez
Dpto. Protección Vegetal, Instituto Canario Investigaciones Agrarias, Apdo. 60, 38200 La Laguna, Tenerife, España
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Introduction. Arbuscular mycorrhizal fungi (AMF) and plant growth-promoting rhizobacteria (PGPR) can be considered important rhizospheric beneficial microorganisms. Their use as biocontrol strategies against soilborne pathogens such as nematodes should be taken into account. However, optimal management of soil microbiota communities is not easy because of the high specificity involved in these types of interactions. The aim of our study was to determine whether the combined inoculation of two AMF species and a Bacillus consortium based on three strains previously described as PGPR in other crops were able to reduce nematode infection and damage on papaya. Materials and methods. Papaya seedlings were inoculated with two AMF isolates (Glomus mosseae or G. manihotis) at the beginning of the nursery phase. Once the mycorrhizal symbiosis was established, a Bacillus consortium was applied. Nematode inoculum was applied 20 d after transplanting to individual pots. Plants were harvested 160 d after nematode inoculation. Results. In terms of plant development and nutrition, benefits due to AMF inoculation persisted in the presence of PGPR. However, the effect of dual inoculation was different, depending on the Glomus species. This positive effect was also evident in plants with nematode. Meloidogyne infection was significantly reduced in mycorrhizal plants. However, the addition of PGPR does not seem to improve the results of AMF single treatments in terms of nematode infection. Conclusion. Dual application of AMF and PGPR must be considered for papaya threatened by the root-knot nematode, although a previous screening should be done in order to select the best microbe combination to optimise results.

Research Article
© CIRAD, EDP Sciences, 2006

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Kennedy, A.C., Smith, K.L., Soil microbial diversity and the sustainability of agricultural soil, Plant Soil 170 (1995) 7586. CrossRef
Bowen, G.D., Rovira, A.D., The rhizosphere and its management to improve plant growth, Adv. Agron. 66 (1999) 1102. CrossRef
Hiltner, L., Über neuere Erfahrungen und Probleme auf dem Gebiet der Bodenbakteriologie und unter besonderer Berücksichtigung der Gründüngung und Brache, Arb. Dtsch. Landwirtsch. Ges. 98 (1904) 5978.
Lynch J.M., The rhizosphere, John Wiley, New York, USA, 1990.
Smith S.E., Read D.J., Mycorrhizal symbiosis, Acad. Press, London, UK, 1997.
Linderman R.G., Vesicular-arbuscular mycorrhizae and soil microbial interactions, in: Bethlenfalvay G.J., Lindeman R.G. (Eds.), Mycorrhizae in sustainable agriculture, ASA Spec. Publ., Madison, Wisconsin, USA, 1992, pp. 45–70.
Safir G.R., Involvement of cropping systems, plant produced compounds and inoculum production in the functioning of VAM fungi, in: Pfleger F.L., Linderman R.G. (Eds.), Mycorrhizae and Plant health, APS Press, Minnesota, USA, 1994, pp. 239–259.
Requena, N., Pérez-Solís, E., Azcón-Aguilar, C., Jeffries, P., Barea, J.M., Management of indigenous plant-microbe symbiosis aids restoration of desertified ecosystems, Appl. Environ. Microbiol. 67 (2001) 495498. CrossRef
Hetrick, B.A.D., Wilson, G.W.T., Figge, D.A.H., The influence of mycorrhizal symbiosis and fertilizer amendments on establishment of vegetation in heavy metal mine spoil, Environ. Pollut. 86 (1994) 171179. CrossRef
Azcón-Aguilar C., Jaizme-Vega M.C., Calvet C., The contribution of arbuscular mycorrhizal fungi to the control of soil-borne plant pathogens, in: Gianinazzi S., Schüepp H., Barea J.M., Haselwandter K. (Eds.), Mycorrhizal technology in agriculture: from genes to bioproducts, Birkhäuser Verlag, Switzerland, 2002, pp. 187–197.
Barea J.M., Azcón-Aguilar C., Azcón R., Interactions between mycorrhizal fungi and rhizosphere microorganisms within the context of sustainable soil-plant systems, in: Gange A.C., Brown V.K., (Eds.), Multitrophic interactions in terrestrial systems, Blackwell Science, Oxford, UK, 1997, pp. 65–77.
Kloepper J.W., Plant growth-promoting rhizobacteria (other systems), in: Okon Y. (Ed.), Azospirillum / plant associations, CRC Press, Boca Ratón, USA, 1994, pp. 111–118.
Burr, T.J., Schroth, M.N., Suslow, T.V., Increased potato yields by treatments of seed pieces with specific strains of Pseudomonas fluorescens and P. putida, Phytopathol. 68 (1978) 13771383. CrossRef
Polonenko, D.R., Scher, F.M., Kloepper, J.W., Singleton, C.A., Laliberté, M., Zaleska, I., Effects of root colonizing bacteria on inoculation of soybean roots by Bradyrhizobium japonicum, Can. J. Microbiol. 33 (1987) 498503. CrossRef
Caesar, A.J., Burr, T.J., Growth promotion of apple seedlings and rootstocks by specific strains of bacteria, Phytopathol. 77 (1987) 15831588. CrossRef
Gardner, J.M., Chandler, J.L., Feldman, A.W., Growth promotion and inhibition by antibiotic-producing fluorescent Pseudomonads on Citrus roots, Plant Soil 77 (1984) 103113. CrossRef
Dobbelaere, S., Croonenborghs, A., Thys, A., Vande Browk, A., Vanderleyden, J., Phytostimulatory effect of Azospirillum brasilense strains and auxins on wheat, Plant Soil 212 (1999) 155164. CrossRef
Ompal, S., Panwar, J.D.S., Effect of nitrogen fixing and phosphorus solubilizing bacteria on nutrient uptake and yield of wheat, Indian J. Plant Physiol. 2 (1997) 211213.
Kloepper J.W., Plant growth-promoting rhizobacteria as biological control agents, in: Metting F.B., Dekker M. (Eds.), Soil microbial ecology, applications in agriculture, forestry and environmental management, Dekker M., Inc., New York, USA, 1992, pp. 255–274.
Barea J.M., Rhizosphere and mycorrhiza of field crops, in: Toutant J.P., Balazs E., Galante E., Lynch J.M., Schepers J.S., Werner D., Werry P.A. (Eds.), Biological resource management: connecting science and policy (OECD), INRA éditions and Springer, Paris, France, 2000, pp. 110–125.
Azcón, R., Selective interactions between free-living rhizospheric bacteria and vesicular-arbuscular mycorrhizal fungi, Soil Biol. Biochem. 21 (1989) 639644. CrossRef
Rodríguez R., Los nematodos de la platanera (Musa acuminata AAA, sub grupo Cavendish Enana) en Canarias (1963–1984), XOBA-Monografía 4, Caja Insul. Ahorr. Canar., Las Palmas de Gran Canaria, Spain, 1990, 58 pp.
Singh, V.S., Nath, R.P., Pathogenicity of root-knot nematode Meloidogyne incognita on papaya, Indian J. Nematol. 26 (1996) 115116.
Ramakrishnan, S., Rajendran, G., Influence of Meloidogyne incognita on yield components and physiological functions of papaya, Nematol. Med. 26 (1998) 225228.
Jaizme-Vega, M.C., Azcón, R., Response of some tropical and subtropical cultures to endomycorrhizal fungi, Mycorrhiza 5 (1995) 213217. CrossRef
Balakrishna, R., Bararaj, D.J., Mallesha, B.C., Selection of efficient VA mycorrhizal fungi for papaya, Biol. Agric. Hortic. 13 (1996) 16.
Trindade, A.V., Siqueira, J.O., Almeida, F.P., Mycorrhizal dependency of papaya commercial varieties, Pesqui. Agropecu. Bras. 36 (2001) 14851494. CrossRef
Jaizme-Vega, M.C., Tenoury, P., Pinochet, J., Jaumot, M., Interactions between the root-knot nematode Meloidogyne incognita and the mycorrhizal association Glomus mosseae and Grande Naine banana, Plant Soil 196 (1997) 2735. CrossRef
Alarcón, A., Davies, F.T. Jr., Egilla, J.N., Fox, T.C., Estrada- Luna, A.A., Ferrera-Cerrato, R., Short term effects of Glomus claroideum and Azospirillum brasilense on growth and root acid phosphatase activity of Carica papaya L. under phosphorus stress, Rev. Latinoam. Microbiol. 44 (2002) 3137.
Jaizme-Vega, M.C., Rodríguez-Romero, A.S., Piñero Guerra, M.S., Potential use of rhizobacteria from the Bacillus genus to stimulate the plant growth of micropropagated banana, Fruits 59 (2004) 8390. CrossRef
Hussey, R.S., Barker, K.R., A comparison of method of collecting inocula of Meloidogyne spp. including a new technique, Plant Dis. Rep. 57 (1973) 10251028.
Hewitt E.J., Sand and water culture method used in the study of plant nutrition, Techn. Comm. 22, Farnham R. Commonw. Agric. Burlaux, Bucks, UK, 1952.
Jones J.B., Benjamin B., Mills H.A., Plant analysis handbook. 1. Methods of plant analysis and interpretation, Micro-Macro Publ., Athens, GA, USA, 1991, 213 p.
Rund R.C., Fertilizers, in: Williams S. (Ed.), Official Methods of Analysis of the Association of Official Analytic Chemist, 14th Edition, AOAC, Ed. Sidney Williams, Arlington, Virginia, USA, 1984, pp. 8–37.
Baker K.R., Nematode extraction and bioassays, in: Barker K.R., Carter C.C., Sasser J.N. (Eds.), An advanced treatise on Meloidogyne, Vol. II. Methodology, North Carol. State Univ., Graphics Raleigh, NC, USA, 1985.
Phillips, J.M., Hayman, D.S., Improved procedures for cleaning roots and stain parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection, Trans. Brit. Mycol. Soc. 55 (1970) 158161. CrossRef
Koske, R.E., Gemma, J.H., A modified procedure for staining root to detect VA mycorrhizas, Mycol. Res. 92 (1989) 486505. CrossRef
Giovanetti M., Mosse B., An evaluation of techniques for measuring vesicular-arbuscular mycorrhizal infection in roots, New Phytol., 84 (1980) 489–500.
Dhillion, S.S., Dual inoculation of pretransplant stage Oryza sativa L. plants with indigenous vesicular-arbuscular mycorrhizal fungi and fluorescent Pseudomonas spp., Biol. Fertil. Soils 13 (1992) 147151. CrossRef
Singh, S., Kapoor, K.K., Effects of inoculation of phosphate-solubilizing microorganisms and an arbuscular mycorrhizal fungus on mungbean grown under natural soil conditions, Mycorrhiza 7 (1998) 249253. CrossRef
Ravnskov, S., Jakobsen, I., Effects of Pseudomonas fluorescens DF57 on growth and P uptake of two arbuscular mycorrhizal fungi in symbiosis with cucumber, Mycorrhiza 8 (1999) 329334. CrossRef
Attia, M., The efficiency improvements of mineral fertilizers used and maize yield by arbuscular mycorrhizal fungus and plant growth-promoting rhizobacteria, Ann. Agr. Sci. Cairo 44 (1999) 4153.
Germida, J.J., Walley, F.L., Plant growth-promoting rhizobacteria alters rooting patterns and arbuscular mycorrhizal fungi colonization of field-grown spring wheat, Biol. Fertil. Soils 23 (1997) 113120. CrossRef
Andreucci F., Fusconi A., Gamalero E., Piras R., Repetto O., Sampó S., Trotta A., Martinotti M.G., Berta G., Reduction of the chemical inputs in a vegetable crop by the use of beneficial rhizospheric microorganisms, INCO-DC, Second Ann. Rep., INCO, 1999.
Siddiqui, I.A., Ehteshamul-Haque, S., Shaukat, S.S., Use of Pseudomonas aeruginosa in the control of root-knot disease complex in tomato: the effects of different inoculum of Meloidogyne javanica and Rhizoctonia solani, Acta Agrobot. 54 (2001) 4554. CrossRef
Khan, M.R., Kounsar, K., Hamid, A., Effect of certain rhizobacteria and antagonistic fungi on root-nodulation and root-knot nematode disease of green gram, Nematol. Med. 30 (2002) 8589.
Jaizme-Vega, M.C., Pinochet, J., Growth response of banana to three mycorrhizal fungi in Pratylenchus goodeyi infested soil, Nematropica 27 (1997) 6976.
Siddiqui, I.A., Mahmood, I., Effect of a plant growth-promoting bacterium, an AM fungus and soil types on the morphometrics and reproduction of Meloidogyne javanica on tomato, Appl. Soil Ecol. 8 (1998) 7784. CrossRef