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Mycorrhiza

, Volume 18, Issue 1, pp 23–32 | Cite as

Inoculation of Pinus halepensis Mill. with selected ectomycorrhizal fungi improves seedling establishment 2 years after planting in a degraded gypsum soil

  • Ana RincónEmail author
  • M. R. de Felipe
  • M. Fernández-Pascual
Original Paper

Abstract

Vegetative inoculum of Amanita ovoidea (Bull.) Link and three isolates of Suillus collinitus (Fr.) Kuntze, as well as spore inoculum of Rhizopogon roseolus (Corda) Th. M. Fr. and S. collinitus, were evaluated for the production of Pinus halepensis Mill. in nursery and for the establishment of seedlings in a degraded gypsum soil. In nursery, most of the fungi significantly improved the height of seedlings and modified the accumulation of nutrients in needles. The percentage of ectomycorrhizas (ESR) per seedling ranged from 25 to 78%, depending on the fungi. One and 2 years after planting in the field, the survival of seedlings was significantly improved by inoculation with two isolates of S. collinitus and with spores of the same fungus. Inoculation with A. ovoidea had no significant effect on seedling survival, whilst R. roseolus caused a significant mortality of seedlings. Seedling height was significantly improved by inoculation with all fungi except R. roseolus and isolate CCMA-1 of S. collinitus. One year after planting, mycorrhization of control seedlings was negligible, and percentages of ESR were under 38% for the rest of treatments. In spring of the second year, seedlings in all treatments, including the control, became highly mycorrhizal (60-77% of ESR). Low ectomycorrhizal diversity (five morphotypes described) and seasonal variation on morphotype composition were detected 2 years after plantation. From a perspective of soil restoration management under limiting environmental conditions, nursery inoculation with selected fungi can be a key advantage for tree seedlings to surmount the initial transplant stress, assuring their establishment in the field. Our results emphasise the importance of selecting compatible fungal-host species combinations for nursery inoculation and sources of inoculum adapted to the environmental conditions of the transplantation site.

Keywords

Ectomycorrhizas Afforestation Soil restoration Nursery Pinus halepensis 

Notes

Acknowledgements

The authors thank Pedro Hernáiz and the group of “La Poveda” (CSIC) for technical assistance. This work was supported by grant GR/AMB/0735/2004 from the Comunidad de Madrid (Spain). A. Rincón holds a I3P postdoctoral fellowship awarded by the Consejo Superior de Investigaciones Científicas (CSIC, Spain).

References

  1. Agerer R (1987-1998) Colour atlas of ectomycorrhizae. Einhirn-Verlag Eduard Dietenberger, MunichGoogle Scholar
  2. 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
  3. Argillier C, Falconnet G, Tillard P, Mousain D (1997) Essais d’introduction dans un arénosol calcaire de Petite-Camargue de pins pignons (Pinus pinea L.) mycorhizés par Suillus collinitus. Rev For Fr 49(2):131-140CrossRefGoogle Scholar
  4. Barberá GG, Martinez-Fernandez F, Alvarez-Rogel J, Albaladejo J, Castillo V (2005) Short and intermediate-term effects of site and plant preparation techniques on reforestation of a Mediterranean semiarid ecosystem with Pinus halepensis Mill. New Forest 29:177-198CrossRefGoogle Scholar
  5. Brundrett M, Bougher N, Dell B, Grove T, Malajczuk N (1996) Working with mycorrhizas in forestry and agriculture, ACIAR Monograph 32. Camberra, AustraliaGoogle Scholar
  6. Brundrett M, Malajczuk N, Mingqin G, Dapin X, Snelling S, Dell B (2005) Nursery inoculation of Eucalyptus seedling in Western Australia and southern China using spore and mycelial inoculum of diverse ectomycorrhizal fungi from different climatic regions. Forest Ecol Manag 209:193-205CrossRefGoogle Scholar
  7. Buée M, Vairelles D, Garbaye J (2005) Year-round monitoring of diversity and potential metabolic activity of the ectomycorrhizal community in a beech (Fagus sylvatica) forest subjected to two thinning regimes. Mycorrhiza 15:235-245CrossRefPubMedGoogle Scholar
  8. Caravaca F, Alguacil MM, Azcón R, Parladé J, Torres P, Roldán A (2005) Establishment of two ectomycorrhizal shrub species in a semiarid site alter in situ amendment with sugar beet, rock phosphate and Aspergillus niger. Microbial Ecol 49:73-82CrossRefGoogle Scholar
  9. Castellano MA, Trappe JM, Molina R (1985) Inoculation of container grown Douglas-fir seedlings with basidiospores of Rhizopogon vinicolor and R. colossus: effects of fertility and spore application rate. Can J For Res 15:10-13CrossRefGoogle Scholar
  10. Clemente AS, Werner C, Maguas C, Cabral MS, Martins-Louçao MA, Correoa O (2004) Restoration of a limestone quarry: effect of soil amendments on the establishment of native Mediterranean sclerophyllous shrubs. Res Ecol 12:20-28CrossRefGoogle Scholar
  11. Cordell CE, Owen JH, Marx DH (1987) Mycorrhizae nursery management for improved seedling quality and field performance. In: Meeting the challenge of the nineties, Proc. Intermount. For. Nursery Assoc. Oklahoma City, Okla, GTR-RM-151, pp 105-115Google Scholar
  12. Dahlberg A, Finlay RD (1999) Suillus. In: Cairney JEGC, Chambers SM (eds) Ectomycorrhizal fungi, key genera in profile. Springer, Berlin, pp 33-64CrossRefGoogle Scholar
  13. Dana ED, Mota JF (2006) Vegetation and soil recovery on gypsum outcrops in semi-arid Spain. J Arid Environ 65:444-459CrossRefGoogle Scholar
  14. El Karkouri K, Martin F, Mousain D (2004) Diversity of ectomycorrhizal symbionts in a disturbed Pinus halepensis plantation in the Mediterranean region. Ann For Sci 61:705-710CrossRefGoogle Scholar
  15. El Karkouri K, Selosse MA, Mousain D (2006) Molecular markers detecting an ectomycorrhizal Suillus collinitus strain on Pinus halepensis roots suggest successful inoculation and persistence in Mediterranean nursery and plantation. FEMS Microbiol Ecol 55:146-158CrossRefPubMedGoogle Scholar
  16. Fujimura KE, Smith JE, Horton TR, Weber NS, Spatafora TR (2005) Pezizalean mycorrhizas and sporocarps in ponderosa pine (Pinus ponderosa) after prescribed fires in eastern Oregon, USA. Mycorrhiza 15:79-86CrossRefPubMedGoogle Scholar
  17. García C, Hernández T, Roldán A, Albaladejo J, Castillo V (2000) Organic amendment and mycorrhizal inoculation as a practice in afforestation of soils with Pinus halepensis Miller: effect on their microbial activity. Soil Biol Biochem 32:1173-1181CrossRefGoogle Scholar
  18. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for Basidomycetes: application to identification of mycorrhizae and rusts. Mol Ecol 2:113-118CrossRefPubMedGoogle Scholar
  19. Gardes M, Bruns TD (1996) Community structure of ectomycorrhial fungi in a Pinus muricata forest: above and below-ground views. Can J Bot 74:1572-1583CrossRefGoogle Scholar
  20. González-Ochoa AI, de las Heras H, Torres P, Sánchez-Gómez E (2003) Mycorrhization of Pinus halepensis Mill. and Pinus pinaster Aiton seedlings in two commercial nurseries. Ann For Sci 60:43-48CrossRefGoogle Scholar
  21. Grayston SJ, Vaughan D, Jones D (1996) Rhizosphere carbon flow in trees, in comparison with annual plants: the importance of root exudation and its impact on microbial activity and nutrient availability. App Soil Ecol 5:29-56CrossRefGoogle Scholar
  22. Grossnickle SC (2005) Importance of root growth in overcoming planting stress. New For 30:273-294CrossRefGoogle Scholar
  23. Guerrero-Campo J, Alberto F, Maestro M, Hodgson J, Montserrat-Martí G (1999) Plant community patterns in a gypsum area of NE Spain. II. Effects of ion washing on topographic distribution of vegetation. J Arid Environm 41:411-419CrossRefGoogle Scholar
  24. Honrubia M (2000) Mycorrhizas in Pinus halepensis Miller.. In: Neeman G, Trabaud L (eds) Ecology biogeography and management of Pinus halepensis and P. brutia forest ecosystems in the Mediterranean basin. Backhuys, Leiden, pp 191-202Google Scholar
  25. Isaac RA, Kerber JD (1971) Atomic absorption and flame photometry: techniques and uses in soil, plant and water analysis. In: Walsh LM (ed) Instrumental methods for analysis of soils, plant, tissue. Soil Science Society of America, Madison, WIGoogle Scholar
  26. Le Tacon F, Álvarez IF, Bouchard D, Henrion B, Jackson RM, Luff S, Parladé J, Pera J, Stenström E, Villeneuve N, Walker C (1992) Variations in field response of forest trees to nursery ectomycorrhizal inoculation in Europe. In: Read DJ, Lewis DH, Fitter AH, Alexander IJ (eds) Mycorrhizas in ecosystems. CAB, Oxford, pp 119-134Google Scholar
  27. Maestre FT, Cortina J (2004) Are Pinus halepensis plantations useful as a restoration tool in semiarid Mediterranean areas? For Ecol Manag 198:303-317CrossRefGoogle Scholar
  28. Manian S, Sreenivasaprasad S, Bending GD, Mills PR (2001) Genetic diversity and interrelationships among common European Suillus species based on ribosomal DNA sequences. FEMS Microbiol Lett 204:117-121CrossRefPubMedGoogle Scholar
  29. Marschner H (1986) Mineral nutrition in higher plants. Academic, San Diego, CAGoogle Scholar
  30. Marx DH (1969) The influence of ectotrophic mycorrhizal fungi on the resistance of pine roots to pathogenic infections. I. Antagonism of mycorrhizal fungi to root pathogenic fungi and soil bacteria. Phytopathol 59:153-163Google Scholar
  31. Marx DH (1991) The pratical significance of ectomycorrhizae in forest establishment. In: Hägglund B (ed) Ecophysiology of ectomycorrhizae of forest trees. Symposium Proceedings no. 7. The Marcus Wallenberg Foundation, Stockholm, Sweden, pp 54-90Google Scholar
  32. Mousain D, Plassard C, Argillier C, Sardin T, Leprince F, El Karkouri K, Arvieu JC, Cleyet-Marel JC (1994) Stratégie d’amélioration de la qualité des plants forestiers et des reboisements méditerranéens par utilisation de la mycorhization contrôlée en pépinière. Acta Bot Gall 141:571-580CrossRefGoogle Scholar
  33. Olsson PA, Jakobsen I, Wallander H (2002) Foraging and resource allocation strategies of mycorrhizal fungi in a patchy environment. In: Van der Heijden MGA, Sanders IR (eds) Mycorrhizal ecology. Springer, Berlin, pp 93-115CrossRefGoogle Scholar
  34. Palacio S, Escudero A, Montserrat-Martí G, Maestro M, Milla R, Albert MJ (2007) Plants living on gypsum: beyond the specialist model. Ann Bot 99:333-343CrossRefPubMedPubMedCentralGoogle Scholar
  35. Parladé J, Pera J, Álvarez IF (1996) Inoculation of containerised Pseudotsuga menziesii and Pinus pinaster seedlings with spores of five species of ectomycorrhizal fungi. Mycorrhiza 6:237-245CrossRefGoogle Scholar
  36. Parladé J, Luque J, Pera J, Rincón A (2004) Field performance of Pinus pinea and P. halepensis seedlings inoculated with Rhizopogon spp. and outplanted in formerly arable land. Ann For Sci 61:507-514CrossRefGoogle Scholar
  37. Posta K, Marschner H, Römheld V (1994) Manganese reduction in the rhizosphere of mycorrhizal and non mycorrhizal maize. Mycorrhiza 5:119-124CrossRefGoogle Scholar
  38. Querejeta JI, Roldán 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
  39. Rincón A, Álvarez IF, Pera J (2001) Inoculation of containerized Pinus pinea L. seedlings with seven ectomycorrhizal fungi. Mycorrhiza 11:265-271CrossRefPubMedGoogle Scholar
  40. Rincón A, Parladé J, Pera J (2005) Effects of ectomycorrhizal inoculation and the type of substrate on mycorrhization, growth and nutrition of containerised Pinus pinea L. seedlings produced in a commercial nursery. Ann For Sci 62:1-6CrossRefGoogle Scholar
  41. Rincón 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 34:42-51CrossRefGoogle Scholar
  42. Rincón A, Parladé J, Pera J (2007) Influence of the fertilisation method in controlled ectomycorrhizal inoculation of two Mediterranean pines. Ann For Sci 64:577-583CrossRefGoogle Scholar
  43. Roldán A, Albaladejo J (1994) Effect of mycorrhizal inoculation and soil restoration on the growth of Pinus halepensis seedlings in a semiarid soil. Biol Fertil Soils 18:143-149CrossRefGoogle Scholar
  44. Roldán A, Querejeta JI, Albadalejo J, Castillo V (1996) Growth response of Pinus halepensis to inoculation with Pisolithus arhizus in a terraced rangeland amended with urban refuse. Plant Soil 179:35-43CrossRefGoogle Scholar
  45. Román R, Fortun C, Garcia-Lopez de Sa ME, Almendros G (2003) Successful soil remediation and reforestation of a calcic regosol amended with composted urban waste. Arid Land Res Manag 17:311-397CrossRefGoogle Scholar
  46. Ruiz-Díez B, Rincón A, de Felipe MR, Fernandez-Pascual M (2006) Molecular characterisation and evaluation of mycorrhizal capacity of Suillus isolates from Central Spain for the selection of fungal inoculants. Mycorrhiza 16:465-474CrossRefPubMedGoogle Scholar
  47. Selosse MA, Martin F, Bouchard D, Le Tacon F (1999) Structure and dynamics of experimentally introduced and naturally occurring Laccaria sp. discrete genotypes in a Douglas fir plantation. Appl Environ Microbiol 65:2006-2014PubMedPubMedCentralGoogle Scholar
  48. Simard SW, Jones MD, Durral DM (2002) Carbon and nutrient fluxes within and between mycorrhizal plants. In: van der Heijden MGA, Sanders I (eds) Mycorrhizal ecology. Springer, Berlin, pp 34-74Google Scholar
  49. Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic, Cambridge, UKGoogle Scholar
  50. Thedesshoo L, Hansen K, Perry BA, Kjoller R (2006) Molecular and morphological diversity of pezizalean ectomycorrhiza. New Phytol 170:581-596CrossRefGoogle Scholar
  51. Torres P, Honrubia M (1994) Inoculation of containerized Pinus halepensis seedlings with basidiospores of Pisolithus tinctorius, Rhizopogon roseolus and Suillus collinitus. Ann Sci For 51:521-528CrossRefGoogle Scholar
  52. Trappe JM (1977) Selection of fungi for ectomycorrhizal inoculation in nurseries. Annu Rev Phytopathol 15:203-222CrossRefGoogle Scholar
  53. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic, New York, pp 315-322Google Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Ana Rincón
    • 1
    Email author
  • M. R. de Felipe
    • 1
  • M. Fernández-Pascual
    • 1
  1. 1.Departamento de Fisiología y Bioquímica Vegetal, Instituto de Recursos NaturalesCentro de Ciencias Medioambientales (IRN-CCMA-CSIC)MadridSpain

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