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Plant and Soil

, Volume 320, Issue 1–2, pp 169–179 | Cite as

Responses of Pinus halepensis growth, soil microbial catabolic functions and phosphate-solubilizing bacteria after rock phosphate amendment and ectomycorrhizal inoculation

  • L. Ouahmane
  • J. C. Revel
  • M. Hafidi
  • J. Thioulouse
  • Y. Prin
  • A. Galiana
  • B. Dreyfus
  • R. Duponnois
Regular Article

Abstract

We examined the effects of an ectomycorrhizal (EM) fungus, Pisolithus sp., on of the growth of Pinus halepensis (Allepo pine) seedlings, soil microbial functions and rock phosphate solubilization in a un-disinfected soil amended or not with a Moroccan rock phosphate. Allepo pine seedlings were inoculated with an EM fungus (Pisolithus sp. strain PH4) isolated from a P. halepensis plantation and selected for its high ability to mobilize P from an inorganic form of phosphate. After 4 month’s culture in a disinfected substrate, plants were transferred in 10 l-containers filled with a natural forest soil and amended or not with rock phosphate powder. After 12 month’s culturing, the growth, needle nutrient concentrations of P. halepensis plants were measured. Soil microbial catabolic diversity was assessed by measuring CO2 production of substrate induced respiration responses. Fluorescent pseudomonads were isolated from each soil treatment and tested in axenic conditions for their ability to solubilize a source of inorganic phosphate. The results clearly showed that (i) P. halepensis growth was greatly promoted by the presence of the ectomycorrhizal fungus Pisolithus strain PH4 in a disinfected soil/vermiculite mixture and in a non disinfected soil, (ii) ectomycorrhizal inoculation induced significant changes in the functions of soil microbial communities and selected microorganisms potentially beneficial to the plant growth (i.e. phosphate-solubilizing fluorescent pseudomonad) and (iii) rock phosphate solubilisation was mainly dependent on EM inoculation and mycorrhizosphere microorganisms. These results were in accordance with previous studies where it was demonstrated that EM symbiosis has a beneficial effect on plant growth through a direct effect on the host plant but also an indirect effect via a selective pressure on soil microbiota that favours microorganisms potentially beneficial to plant growth.

Keywords

Bacteria Ectomycorrhizosphere effect Fluorescent pseudomonads Pinus halepensis Pisolithus sp. Rock phosphate Soil functional abilities Morocco 

Notes

Acknowledgements

This work was funded by the Moroccan-France PRAD programme (PRAD 05/12). Programme de Recherche Agronomique pour le Développement) and by IRD (Institut de Recherche pour le Développement (Jeune Equipe Associée à l’IRD, JEAI « Usen »).

References

  1. Agerer R (1995) Anatomical characteristics of identified ectomycorrhizas: an attempt towards a natural classification. In: Varma A, Hock B (eds) Mycorrhiza: structure, function, molecular biology and biotechnology. Springer, Berlin, pp 687–734Google Scholar
  2. Appuhn A, Joergensen RG, Raubuch M, Scheller E, Wilke B (2004) The automated determination of glucosamine, galactosamine, muramic acid and mannosamine in soil and root hydrolysates by HMPLC. J Plant Nutr Soil Sci 167:17–21 doi: 10.1002/jpln.200321302 CrossRefGoogle Scholar
  3. Bartnicki-Garcia S (1968) Cell wall chemistry, morphogenesis, and taxonomy of fungi. Ann Rev Microbiol 22:87–108CrossRefGoogle Scholar
  4. Caravaca F, Garcia C, Hernandez MT, Roldan A (2002) Aggregate stability changes after organic amendment and mycorrhizal inoculation in the afforestation of a semiarid site with Pinus halepensis. Appl Soil Ecol 19:199–208 doi: 10.1016/S0929-1393(01)00189-5 CrossRefGoogle Scholar
  5. Caravaca F, Alguacil MM, Azcon R, Diaz G, Roldan A (2004) Comparing the effectiveness of mycorrhizal inoculum and amendment with sugar beet, rock phosphate and Aspergillus niger to enhance field performance of the leguminous shrub Dorycnium pentaphyllum L. Appl Soil Ecol 25:169–180 doi: 10.1016/j.apsoil.2003.08.002 CrossRefGoogle Scholar
  6. Caravaca F, Alguacil MM, Azcon R, Parladé J, Torres P, Roldan A (2005) Establishment of two ectomycorrhizal shrub species in a semiarid site after in situ amendment with sugar beet, rock phosphate, and Aspergillus niger. Microb Ecol 49:73–82 doi: 10.1007/s00248-003-0131-y PubMedCrossRefGoogle Scholar
  7. Culhane AC, Perriere G, Considine EC, Cotter TG, Higgins DG (2002) Between-group analysis of microarray data. Bioinformatics 18:1600–1608 doi: 10.1093/bioinformatics/18.12.1600 PubMedCrossRefGoogle Scholar
  8. Degens BP, Harris JA (1997) Development of a physiological approach to measuring the metabolic diversity of soil microbial communities. Soil Biol Biochem 29:1309–1320 doi: 10.1016/S0038-0717(97)00076-X CrossRefGoogle Scholar
  9. Degens BP, Vojvodic-Vukovic M (1999) A sampling strategy to assess the effects of land use on microbial functional diversity in soils. Aust J Soil Res 37:593–601Google Scholar
  10. Degens BP, Schipper LA, Sparling GP, Vojvodic-Vukovic M (2000) Decreases in organic C reserves in soils can reduce the catabolic diversity of soil microbial communities. Soil Biol Biochem 32:189–196 doi: 10.1016/S0038-0717(99)00141-8 CrossRefGoogle Scholar
  11. Drever JI, Vance GF (1994) Role of soil organic acids in mineral weathering processes. In: Lewan MD, Pittman ED (eds) The role of organic acids in geological processes. Springer, Berlin, pp 138–161Google Scholar
  12. Duponnois R, Garbaye J (1991) Techniques for controlled synthesis of the Douglas fir—Laccaria laccata ectomycorrhizal symbiosis. Ann Sci 48:239–251 doi: 10.1051/forest:19910301 CrossRefGoogle Scholar
  13. Duponnois R, Founoune H, Masse D, Pontanier R (2005) Inoculation of Acacia holosericea with ectomycorrhizal fungi in a semiarid site in Senegal: growth response and influences on the mycorrhizal soil infectivity after 2 years plantation. For Ecol Manage 207:351–362CrossRefGoogle Scholar
  14. Duponnois R, Kisa M, Prin Y, Ducousso M, Plenchette C, Lepage M, Galiana A (2007) Soil factors influencing the growth response of Acacia holosericea A; Cunn. Ex G. Don to ectomycorrhizal inoculation. New For 35:105–117 doi: 10.1007/s11056-007-9066-3 Google Scholar
  15. Ekblad A, Näsholm T (1996) Determination of chitin in fungi and mycorrhizal roots by an improved HPLC analysis of glucosamine. Plant Soil 178:29–35 doi: 10.1007/BF00011160 CrossRefGoogle Scholar
  16. Frey P, Frey-Klett P, Garbaye J, Berge O, Heulin T (1997) Metabolic and genotypic fingerprinting of fluorescent pseudomonads associated with the Douglas Fir-Laccaria bicolor mycorrhizosphere. Appl Environ Microbiol 63:1852–1860PubMedGoogle Scholar
  17. Frey-Klett P, Chavatte M, Clausse ML, Courrier S, Le Roux C, Raaijmakers J, Martinotti MG, Pierrat JC, Garbaye J (2005) Ectomycorrhizal symbiosis affects functional diversity of rhizosphere fluorescent pseudomonads. New Phytol 165:317–328 doi: 10.1111/j.1469-8137.2004.01212.x PubMedCrossRefGoogle Scholar
  18. Giller KE, Beare MH, Lavelle P, Izac A-MN, Swift MJ (1997) Agricultural intensification, soil biodiversity and agroecosystem function. Appl Soil Ecol 6:3–16 doi: 10.1016/S0929-1393(96)00149-7 CrossRefGoogle Scholar
  19. Gonzalez-Ochoa AI, de las Heras J, Torres P, Sanchez-Gomez E (2003) Mycorrhization of Pinus halepensis Mill. and Pinus pinaster Aiton seedlings in two commercial nurseries. Ann Sci 60:43–48 doi: 10.1051/forest:2002072 CrossRefGoogle Scholar
  20. Grayston SJ, Campell CD, Vaughan D (1994) Microbial diversity in the rhizospheres of different tree species. In: Pankhurst CE (ed) Soil biota: management in sustainable farming systems. CSIRO, Adelaide, pp 155–157Google Scholar
  21. Hafidi M (1996) Enrichissement du compost par addition des phosphates naturels. Thèse d’Etat, Faculté des Sciences Semlalia, MarrakechGoogle Scholar
  22. Heinemeyer O, Insam H, Kaiser EA, Walenzik G (1989) Soil microbial biomass and respiration measurements: an automated technique based on infrared gas analysis. Plant Soil 116:77–81 doi: 10.1007/BF02214547 CrossRefGoogle Scholar
  23. Huberty CJ (1994) Applied discriminant analysis. John Wiley & Sons, New YorkGoogle Scholar
  24. Illmer P, Schinner F (1992) Solubilization of inorganic phosphates by microorganisms isolated from forest soils. Soil Biol Biochem 24:389–395 doi: 10.1016/0038-0717(92)90199-8 CrossRefGoogle Scholar
  25. Illmer P, Barbato A, Schinner F (1995) Solubilization of hardly-soluble AlPO4 with P-solubilizing microorganism. Soil Biol Biochem 27:265–270 doi: 10.1016/0038-0717(94)00205-F CrossRefGoogle Scholar
  26. John MK (1970) Colorimetric determination of phosphorus in soil and plant material with ascorbic acid. Soil Sci 68:171–177Google Scholar
  27. King EO, Ward MK, Raney DE (1954) Two simple media for the demonstration of pyocyanine and fluorescein. J Lab Clin Med 44:301–307PubMedGoogle Scholar
  28. Lapeyrie F, Ranger J, Vairelles D (1990) Phosphate-solubilizing activity of ectomycorrhzial fungi in vitro. Can J Bot 69:342–346 doi: 10.1139/b91-046 CrossRefGoogle Scholar
  29. Linderman RG (1988) Mycorrhizal interactions with the rhizosphere microflora: the mycorrhizosphere effect. Phytopathology 78:366–371Google Scholar
  30. Lopez-Bucio J, de la Vega OM, Guevara-Garcia A, Herrera-Estrella L (2000) Enhanced phosphorus uptake in transgenic tobacco plants that overproduce citrate. Nat Biotechnol 18:450–453 doi: 10.1038/74531 PubMedCrossRefGoogle Scholar
  31. Magurran AE (1988) Ecological diversity and its measurement. Croom Helm, LondonGoogle Scholar
  32. Marx DH (1991) The practical significance of ectomycorrhizae in forest establishment. Ecophysiology of forest trees. Marcus Wallenberg Found Symp Proc 7:54–90Google Scholar
  33. Muthukumar T, Udaiyan K, Rajeshkannan V (2001) Response of neem (Azadirachta indica A. Juss) to indigenous arbuscular mycorrhizal fungi, phosphate-solubilizing and asymbiotic nitrogen-fixing bacteria under tropical nursery conditions. Biol Fertil Soils 34:417–426Google Scholar
  34. Ochs M (1996) Influence of humidified and non-humidified natural organic compounds on mineral dissolution. Chem Geol 132:119–124 doi: 10.1016/S0009-2541(96)00046-0 CrossRefGoogle Scholar
  35. Plenchette C, Fortin JA, Furlan V (1983) Growth responses of several plant species to mycorrhizae in a soil of moderate P-fertility. I. Mycorrhizal dependency under field conditions. Plant Soil 70:199–209 doi: 10.1007/BF02374780 CrossRefGoogle Scholar
  36. Querejeta JI, Roldan A, Albadalejo J, Castillo V (1998) The role of mycorrhizae, site preparation, and organic amendment in the afforestation of a semi-arid Mediterranean site with Pinus halepensis. For Sci 44:203–211Google Scholar
  37. Quezel P, Barbero M (1992) Le pin d’Alep et les espèces voisines. Répartition et caractères écologiques généraux, sa dynamique récente en France méditerranéenne. Foret Mediterraneenne 3:158–170Google Scholar
  38. Read DJ, Perez-Moreno J (2003) Mycorrhizas and nutrient cycling in ecosystems—a journey towards relevance? New Phytol 157:475–492 doi: 10.1046/j.1469-8137.2003.00704.x CrossRefGoogle Scholar
  39. Requena N, Perez-Solis E, Azcon-Aguilar C, Jeffries P, Barea JM (2001) Management of indigenous plant—microbe symbioses aids restoration of desertified ecosystems. Appl Environ Microbiol 67:495–498 doi: 10.1128/AEM.67.2.495-498.2001 PubMedCrossRefGoogle Scholar
  40. Rincon A, Ruiz-Diez B, Fernandez-Pascual M, Probanza A, Pozuelo JM, de Felipe MR (2006) Afforestation of degraded soils with Pinus halepensis Mill.: effects of inoculation with selected microorganisms and soil amendment on plant growth, rhizospheric microbial activity and ectomycorrhizal formation. Appl Soil Ecol 34:42–51 doi: 10.1016/j.apsoil.2005.12.004 CrossRefGoogle Scholar
  41. Rincon A, de Felipe MR, Fernandez-Pascual M (2007) Inoculation of Pinus halepensis Mill. With selected ectomycorrhizal fungi improves seedling establishment 2 years after planting in a degraded gypsum soil. Mycorrhiza 18:23–32 doi: 10.1007/s00572-007-0149-y PubMedCrossRefGoogle Scholar
  42. Slankis V (1974) Soil factors influencing formation of mycorrhizae. Annu Rev Phytopathol 12:437–457 doi: 10.1146/annurev.py.12.090174.002253 CrossRefGoogle Scholar
  43. Smith S, Read J (1997) Mycorrhizal symbiosis, 2nd edn. Academic, LondonGoogle Scholar
  44. Sparling GP (1995) The substrate induced respiration method. In: Alef K, Nannipieri P (eds) Methods in applied soil microbiology and biochemistry. Academic, London, pp 397–404Google Scholar
  45. Thioulouse J, Chessel D, Dolédec S, Olivier JM (1997) ADE-4: a multivariate analysis and graphical display software. Stat Comput 7:75–83 doi: 10.1023/A:1018513530268 CrossRefGoogle Scholar
  46. Wallander H (2000) Uptake of P from apatite by Pinus sylvestris seedlings colonized by different ectomycorrhizal fungi. Plant Soil 218:249–256 doi: 10.1023/A:1014936217105 CrossRefGoogle Scholar
  47. West AW, Sparling GP (1986) Modifications of the substrate-induced respiration method to permit measurements of microbial biomass in soils of differing water contents. J Microbiol Methods 5:177–189 doi: 10.1016/0167-7012(86)90012-6 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • L. Ouahmane
    • 1
    • 2
  • J. C. Revel
    • 3
  • M. Hafidi
    • 1
  • J. Thioulouse
    • 4
  • Y. Prin
    • 5
  • A. Galiana
    • 5
  • B. Dreyfus
    • 6
  • R. Duponnois
    • 6
    • 7
  1. 1.Laboratoire Ecologie et Environnement, Faculté des Sciences SemlaliaUniversité Cadi AyyadMarrakechMaroc
  2. 2.Direction Régionale des Eaux & Forêts du Haut AtlasMarrakechMaroc
  3. 3.Ecole Nationale Supérieure Agronomique de Toulouse, Castanet-Tolosan, Eco. Lab., UMR 5245, CNRS-UPS-INPTToulouseFrance
  4. 4.Laboratoire de Biométrie et Biologie Evolutive (UMR 5558); CNRS; Univ. Lyon 1Villeurbanne CedexFrance
  5. 5.CIRAD. UMR 113 CIRAD/INRA/IRD/SUP-AGRO/UM2. Laboratoire des Symbioses Tropicales et Méditerranéennes (LSTM). TA10/J, Campus International de BaillarguetMontpellierFrance
  6. 6.IRD. UMR 113 CIRAD/INRA/IRD/SUP-AGRO/UM2. Laboratoire des Symbioses Tropicales et Méditerranéennes (LSTM). TA10/J, Campus International de BaillarguetMontpellierFrance
  7. 7.IRD. Laboratoire Commun de Microbiologie IRD/ISRA/UCAD. Centre de Recherche de Bel AirDakarSénégal

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