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Mycorrhiza

, Volume 22, Issue 6, pp 449–460 | Cite as

Temporal dynamics of arbuscular mycorrhizal fungi colonizing roots of representative shrub species in a semi-arid Mediterranean ecosystem

  • Iván Sánchez-CastroEmail author
  • Nuria Ferrol
  • Pablo Cornejo
  • José-Miguel Barea
Original Paper

Abstract

Arbuscular mycorrhizal (AM) symbiosis plays an important role in improving plant fitness and soil quality, particularly in fragile and stressed environments, as those in certain areas of Mediterranean ecosystems. AM fungal communities are usually affected by dynamic factors such as the plant community structure and composition, which in turn are imposed by seasonality. For this reason, a one-year-round time-course trial was performed by sampling the root system of two representative shrubland species (Rosmarinus officinalis and Thymus zygis) within a typical Mediterranean ecosystem from the Southeast of Spain. The 18S rDNA gene, of the AM fungal community in roots, was subjected to PCR–SSCP, sequencing, and phylogenetic analysis. Forty-three different AM fungal sequence types were found which clustered in 16 phylotypes: 14 belonged to the Glomeraceae and two to the Diversisporaceae. Surprisingly, only two of these phylotypes were related with sequences of morphologically defined species: Glomus intraradices and Glomus constrictum. Significant differences were detected for the relative abundance of some phylotypes while no effects were found for the calculated diversity indices. These results may help to design efficient mycorrhizal-based revegetation programs for this type of ecosystems.

Keywords

Arbuscular mycorrhiza Mediterranean ecosystem Rosmarinus officinalis Thymus zygis Temporal dynamics Single-strand conformation polymorphism (SSCP) 

Notes

Acknowledgments

This research was supported by the Spanish CICyT project REN2003-968. We are also grateful for support from the Spanish National Research Program (R & D + i)-European Union (Feder) CGL2009-08825/BOS; and from the Andalusian (Spain) Autonomic Government, PAIDI (R & D + i) Programme: P07-CVI-02952. Iván Sánchez-Castro was supported by a fellowship from the Andalusian Autonomic Government.

References

  1. Alguacil MM, Roldán A, Torres MP (2009a) Assessing the diversity of AM fungi in arid gypsophilous plant communities. Environ Microbiol 11:2649–2659. doi: 10.1111/j.1462-2920.2009.01990.x PubMedCrossRefGoogle Scholar
  2. Alguacil MM, Roldán A, Torres MP (2009b) Complexity of semiarid gypsophilous shrub communities mediates the AMF biodiversity at the plant species level. Microb Ecol 57:718–727. doi: 10.1007/s00248-008-9438-z PubMedCrossRefGoogle Scholar
  3. Alguacil MM, Torres MP, Torrecillas E, Díaz G, Roldán A (2011) Plant type differently promote the arbuscular mycorrhizal fungi biodiversity in the rhizosphere after revegetation of a degraded, semiarid land. Soil Biol Biochem 43:167–173. doi: 10.1016/j.soilbio.2010.09.029 CrossRefGoogle Scholar
  4. Allen MF (2007) Mycorrhizal fungi: highways for water and nutrients in arid soils. Vadose Zone J 6:291–297. doi: 10.2136/vzj2006.0068 CrossRefGoogle Scholar
  5. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410PubMedGoogle Scholar
  6. Aroca R, Porcel R, Ruíz-Lozano JM (2007) How does arbuscular mycorrhizal symbiosis regulate root hydraulic properties and plasma membrane aquaporins in Phaseolus vulgaris under drought, cold or salinity stresses? New Phytol 173:808–816. doi: 10.1111/j.1469-8137.2006.01961.x PubMedCrossRefGoogle Scholar
  7. Azcón-Aguilar C, Palenzuela J, Roldán A, Bautista S, Vallejo R, Barea JM (2003) Analysis of the mycorrhizal potential in the rhizosphere of representative plant species from desertification-threatened Mediterranean shrublands. Appl Soil Ecol 22:29–37CrossRefGoogle Scholar
  8. Barea JM, Palenzuela J, Cornejo P, Sánchez I, Navarro C, Quiñones PB, Azcón R, Ferrol N, Azcón-Aguilar C (2007) Significado, diversidad e impacto de los hongos de las micorrizas arbusculares en ambientes mediterráneos. In: Barea-Azcón JM, Moleón M, Travesí R, Ballesteros E, Luzón JM, Tierno JM (eds) Biodiversidad y Conservación de Fauna y Flora en Ambientes Mediterráneos. Sociedad Granatense de Historia Natural, Granada, España, pp 155–185Google Scholar
  9. Barea JM, Palenzuela J, Cornejo P, Sánchez-Castro I, Navarro-Fernández C, Lopéz-García A, Estrada B, Azcón R, Ferrol N, Azcón-Aguilar C (2011) Ecological and functional roles of mycorrhizas in semi-arid ecosystems of Southeast Spain. J Arid Environ 75:1292–1301CrossRefGoogle Scholar
  10. Bever JD, Schultz PA, Pringle A, Morton JB (2001) Arbuscular mycorrhizal fungi: more diverse than meets the eye, and the ecological tale of why. Bioscience 51:923–931CrossRefGoogle Scholar
  11. Caravaca F, Barea JM, Palenzuela J, Figueroa D, Alguacil MM, Roldán A (2003) Establishment of shrubs species in a degraded semiarid site after inoculation with native or allochthonous arbuscular mycorrhizal fungi. Appl Soil Ecol 22:103–111CrossRefGoogle Scholar
  12. Cesaro P, van Tuinen D, Copetta A, Chatagnier O, Berta G, Gianinazzi S, Lingua G (2008) Preferential colonization of Solanum tuberosum L. roots by the fungus Glomus intraradices in arable soil of a potato farming area. Appl Environ Microbiol 74:5776–5783. doi: 10.1128/aem.00719-08 PubMedCrossRefGoogle Scholar
  13. Dag A, Yermiyahu U, Ben-Gal A, Zipori I, Kapulnik Y (2009) Nursery and post-transplant field response of olive trees to arbuscular mycorrhizal fungi in an arid region. Crop Pasture Sci 60:427–433. doi: 10.1071/cp08143 CrossRefGoogle Scholar
  14. Daniell TJ, Husband R, Fitter AH, Young JPW (2001) Molecular diversity of arbuscular mycorrhizal fungi colonising arable crops. FEMS Microbiol Ecol 36:203–209PubMedCrossRefGoogle Scholar
  15. Eom AH, Hartnett DC, Wilson GWT (2000) Host plant species effects on arbuscular mycorrhizal fungal communities in tallgrass prairie. Oecologia 122:435–444CrossRefGoogle Scholar
  16. Felstein (1993) PHYLIP, version 3.66. Department of Genetics, University of Washington, SeattleGoogle Scholar
  17. Ferrol N, Calvente R, Cano C, Barea JM, Azcón-Aguilar C (2004) Analysing arbuscular mycorrhizal fungal diversity in shrub-associated resource islands from a desertification-threatened semiarid Mediterranean ecosystem. Appl Soil Ecol 25:123–133. doi: 10.1016/j.apsoil.2003.08.006 CrossRefGoogle Scholar
  18. Giovannetti M, Mosse B (1980) Evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500CrossRefGoogle Scholar
  19. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis. Available at http://www.mbio.ncsu.edu/BioEdit/bioedit.html
  20. Hart MM, Reader RJ, Klironomos JN (2003) Plant coexistence mediated by arbuscular mycorrhizal fungi. Trends Ecol Evol 18:418–423. doi: 10.1016/s0169-5347(03)00127-7 CrossRefGoogle Scholar
  21. Helgason T, Daniell TJ, Husband R, Fitter AH, Young JPW (1998) Ploughing up the wood-wide web? Nature 394:431PubMedCrossRefGoogle Scholar
  22. Helgason T, Fitter AH, Young JPW (1999) Molecular diversity of arbuscular mycorrhizal fungi colonising Hyacinthoides non-scripta (bluebell) in a seminatural woodland. Mol Ecol 8:659–666CrossRefGoogle Scholar
  23. Hijri I, Sykorova Z, Oehl F, Ineichen K, Mader P, Wiemken A, Redecker D (2006) Communities of arbuscular mycorrhizal fungi in arable soils are not necessarily low in diversity. Mol Ecol 15:2277–2289. doi: 10.1111/j.1365-294X.2006.02921.x PubMedCrossRefGoogle Scholar
  24. Hurlbert SH (1971) Nonconcept of species diversity—critique and alternative parameters. Ecology 52:577–586CrossRefGoogle Scholar
  25. Husband R, Herre EA, Young JPW (2002) Temporal variation in the arbuscular mycorrhizal communities colonising seedlings in a tropical forest. FEMS Microbiol Ecol 42:131–136PubMedCrossRefGoogle Scholar
  26. Jeffries P, Craven-Griffiths A, Barea JM, Levy Y, Dodd JC (2002) Application of arbuscular mycorrhizal fungi in the revegetation of desertified Mediterranean ecosystems. In: Gianinazzi S, Schüepp H, Barea JM, Haselwandter K (eds) Mycorrhiza technology in agriculture: from genes to bioproducts. Birkhäuser, Basel, pp 151–174CrossRefGoogle Scholar
  27. Kovacs GM, Balazs T, Penzes Z (2007) Molecular study of arbuscular mycorrhizal fungi colonizing the sporophyte of the eusporangiate rattlesnake fern (Botrychium virginianum, Ophioglossaceae). Mycorrhiza 17:597–605. doi: 10.1007/s00572-007-0137-2 PubMedCrossRefGoogle Scholar
  28. Lee PJ, Koske RE (1994) Gigaspora gigantea: seasonal abundance and aging of spores in a sand dune. Mycol Res 98:453–457CrossRefGoogle Scholar
  29. Liang ZB, Drijber RA, Lee DJ, Dwiekat IM, Harris SD, Wedin DA (2008) A DGGE-cloning method to characterize arbuscular mycorrhizal community structure in soil. Soil Biol Biochem 40:956–966. doi: 10.1016/j.soilbio.2007.11.016 CrossRefGoogle Scholar
  30. Liu Y, He L, An LZ, Helgason T, Feng HY (2009) Arbuscular mycorrhizal dynamics in a chronosequence of Caragana korshinskii plantations. FEMS Microbiol Ecol 67:81–92. doi: 10.1111/j.1574-6941.2008.00597.x PubMedCrossRefGoogle Scholar
  31. López-Bermúdez F, Albaladejo J, Stocking MA, Díaz E (1990) Factores ambientales de la degradación del suelo en el area mediterranea. In: Albaladejo J, Stocking MA, Díaz E (eds) Degradation and rehabilitation of soil in Mediterranean environmental conditions. CSIC, Murcia, pp 15–45Google Scholar
  32. Maidak BL, Cole JR, Lilburn TG, Parker CT, Saxman PR, Farris RJ, Garrity GM, Olsen GJ, Schmidt TM, Tiedje JM (2001) The RDP-II (Ribosomal Database Project). Nucleic Acids Res 29:173–174PubMedCrossRefGoogle Scholar
  33. Martinez-García LB, Armas C, Miranda JD, Padilla FM, Pugnaire FI (2011) Shrubs influence arbuscular mycorrhizal fungi communities in a semi-arid environment. Soil Biol Biochem 43:682–689. doi: 10.1016/j.soilbio.2010.12.006 CrossRefGoogle Scholar
  34. Merryweather J, Fitter A (1998) The arbuscular mycorrhizal fungi of Hyacinthoides non-scripta—II. Seasonal and spatial patterns of fungal populations. New Phytol 138:131–142CrossRefGoogle Scholar
  35. Oehl F, Sieverding E, Ineichen K, Mäder P, Wiemken A, Boller T (2009) Distinct sporulation dynamics of arbuscular mycorrhizal fungal communities from different agroecosystems in long-term microcosms. Agric Ecosyst Environ 134:257–268CrossRefGoogle Scholar
  36. Oehl F, da Silva GA, Goto BT, Costa-Maia L, Sieverding E (2011) Glomeromycora: two new classes and a new order. Mycotaxon 116:365–379CrossRefGoogle Scholar
  37. Öpik M, Moora M, Liira J, Koljalg U, Zobel M, Sen R (2003) Divergent arbuscular mycorrhizal fungal communities colonize roots of Pulsatilla spp. in boreal Scots pine forest and grassland soils. New Phytol 160:581–593CrossRefGoogle Scholar
  38. Öpik M, Moora M, Liira J, Zobel M (2006) Composition of root-colonizing arbuscular mycorrhizal fungal communities in different ecosystems around the globe. J Ecol 94:778–790CrossRefGoogle Scholar
  39. Öpik M, Saks Ü, Kennedy J, Daniell T (2008) Global diversity patterns of arbuscular mycorrhizal fungi-community composition and links with functionality. In: Varma A (ed) Mycorrhiza: state of the art, genetics and molecular biology, eco-function, biotechnology, eco-physiology, structure and systematics, 3rd edn. Springer, Berlin, pp 89–111Google Scholar
  40. Ouahmane L, Thioulouse J, Hafidi M, Prin Y, Ducousso M, Galiana A, Plenchette C, Kisa M, Duponnois R (2007) Soil functional diversity and P solubilization from rock phosphate after inoculation with native or allochtonous arbuscular mycorrhizal fungi. For Ecol Manag 241:200–208CrossRefGoogle Scholar
  41. Page RDM (1996) TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358PubMedGoogle Scholar
  42. Phillips JM, Hayman DS (1970) Improved procedure of clearing roots and staining parasitic and vesicular–arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:159–161CrossRefGoogle Scholar
  43. Piotrowski JS, Denich T, Klironomos JN, Graham JM, Rillig MC (2004) The effects of arbuscular mycorrhizas on soil aggregation depend on the interaction between plant and fungal species. New Phytol 164:365–373. doi: 10.1111/j.1469-8137.2004.01181.x CrossRefGoogle Scholar
  44. Pringle A, Bever JD (2002) Divergent phenologies may facilitate the coexistence of arbuscular mycorrhizal fungi in a North Carolina grassland. Am J Bot 89:1439–1446PubMedCrossRefGoogle Scholar
  45. Redecker D (2000) Specific PCR primers to identify arbuscular mycorrhizal fungi within colonized roots. Mycorrhiza 10:73–80CrossRefGoogle Scholar
  46. Renker C, Weisshuhn K, Kellner H, Buscot F (2006) Rationalizing molecular analysis of field-collected roots for assessing diversity of arbuscular mycorrhizal fungi: to pool, or not to pool, that is the question. Mycorrhiza 16:525–531. doi: 10.1007/s00572-006-0067-4 PubMedCrossRefGoogle Scholar
  47. Requena N, Jeffries P, Barea JM (1996) Assessment of natural mycorrhizal potential in a desertified semiarid ecosystem. Appl Environ Microbiol 62:842–847PubMedGoogle Scholar
  48. Requena N, Pérez-Solis E, Azcón-Aguilar C, Jeffries P, Barea JM (2001) Management of indigenous plant–microbe symbioses aids restoration of desertified ecosystems. Appl Environ Microbiol 67:495–498PubMedCrossRefGoogle Scholar
  49. Rosendahl S, Stukenbrock EH (2004) Community structure of arbuscular mycorrhizal fungi in undisturbed vegetation revealed by analyses of LSU rDNA sequences. Mol Ecol 13:3179–3186. doi: 10.1111/j.1365-294.2004.02295.x PubMedCrossRefGoogle Scholar
  50. Ruíz-Lozano JM, Porcel R, Aroca R (2008) Evaluation of the possible participation of drought-induced genes in the enhanced tolerance of arbuscular mycorrhizal plants to water deficit. In: Varma A (ed) Mycorrhiza: state of the art, genetics and molecular biology, eco-function, biotechnology, eco-physiology, structure and systematics. Springer, Berlin, pp 185–207Google Scholar
  51. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning a laboratory manual. 2nd ed. Vols. 1 2 and 3. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  52. Sánchez-Castro I, Barea JM, Ferrol N (2008) Analyzing the community composition of arbuscular mycorrhizal fungi colonizing the roots of representative shrubland species in a Mediterranean ecosystems (Granada, Spain). In: Book of Abstracts Plant–Microbial Interactions 2008 2–6 July Krakow, Poland, pp. 38–39Google Scholar
  53. Santos-González JC, Finlay RD, Tehler A (2006) Molecular analysis of arbuscular mycorrhizal fungi colonising a semi-natural grassland along a fertilisation gradient. New Phytol 172:159–168. doi: 10.1111/j.1469-8137.2006.01799.x CrossRefGoogle Scholar
  54. Santos-González JC, Finlay RD, Tehler A (2007) Seasonal dynamics of arbuscular mycorrhizal fungal communities in roots in a seminatural grassland. Appl Environ Microbiol 73:5613–5623. doi: 10.1128/aem.00262-07 PubMedCrossRefGoogle Scholar
  55. Schechter SP, Bruns TD (2008) Serpentine and non-serpentine ecotypes of Collinsia sparsiflora associate with distinct arbuscular mycorrhizal fungal assemblages. Mol Ecol 17:3198–3210. doi: 10.1111/j.1365-294X.2008.03828.x PubMedCrossRefGoogle Scholar
  56. Scheublin TR, Ridgway KP, Young JPW, van der Heijden MGA (2004) Nonlegumes, legumes, and root nodules harbor different arbuscular mycorrhizal fungal communities. Appl Environ Microbiol 70:6240–6246PubMedCrossRefGoogle Scholar
  57. Scheublin TR, Van Logtestijn RSP, Van der Heijden MGA (2007) Presence and identity of arbuscular mycorrhizal fungi influence competitive interactions between plant species. J Ecol 95:631–638. doi: 10.1111/j.1365-2745.2007.01244.x CrossRefGoogle Scholar
  58. Shannon CE, Weaver W (1963) The mathematical theory of communication. The University of Illinois Press, UrbanaGoogle Scholar
  59. Simon L, Lalonde M, Bruns TD (1992) Specific amplification of 18S fungal ribosomal genes from vesicular–arbuscular endomycorrhizal fungi colonizing roots. Appl Environ Microbiol 58:291–295PubMedGoogle Scholar
  60. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Elsevier Academic, New YorkGoogle Scholar
  61. Sonjak S, Beguiristain T, Leyval C, Regvar M (2009) Temporal temperature gradient gel electrophoresis (TTGE) analysis of arbuscular mycorrhizal fungi associated with selected plants from saline and metal polluted environments. Plant Soil 314:25–34. doi: 10.1007/s11104-008-9702-5 CrossRefGoogle Scholar
  62. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882PubMedCrossRefGoogle Scholar
  63. Vallejo VR, Bautista S, Cortina J (1999) Restoration for soil protection after disturbances. In: Trabaud L (ed) Life and environment in the Mediterranean. Advances in ecological sciences. WIT, Wessex, pp 301–343Google Scholar
  64. Vallino M, Massa N, Lumini E, Bianciotto V, Berta G, Bonfante P (2006) Assessment of arbuscular mycorrhizal fungal diversity in roots of Solidago gigantea growing in a polluted soil in Northern Italy. Environ Microbiol 8:971–983. doi: 10.1111/j.1462-2920.2005.00980.x PubMedCrossRefGoogle Scholar
  65. van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72CrossRefGoogle Scholar
  66. van der Heijden MGA, Scheublin TR, Brader A (2004) Taxonomic and functional diversity in arbuscular mycorrhizal fungi—is there any relationship? New Phytol 164:201–204CrossRefGoogle Scholar
  67. Vandenkoornhuyse P, Husband R, Daniell TJ, Watson IJ, Duck JM, Fitter AH, Young JPW (2002) Arbuscular mycorrhizal community composition associated with two plant species in a grassland ecosystem. Mol Ecol 11:1555–1564PubMedCrossRefGoogle Scholar
  68. 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, San Diego, pp 315–322Google Scholar
  69. Wu SC, Cheung KC, Luo YM, Wong MH (2006) Effects of inoculation of plant growth-promoting rhizobacteria on metal uptake by Brassica juncea. Environ Pollut 140:124–135PubMedCrossRefGoogle Scholar
  70. Wubet T, Weiss M, Kottke I, Oberwinkler F (2006) Two threatened coexisting indigenous conifer species in the dry Afromontane forests of Ethiopia are associated with distinct arbuscular mycorrhizal fungal communities. Can J Bot 84:1617–1627. doi: 10.1139/b06-121 CrossRefGoogle Scholar
  71. Yang C, Hamel C, Schellenberg MP, Pérez JC, Berbara RL (2010) Diversity and functionality of arbuscular mycorrhizal fungi in three plant communities in semiarid grasslands National Park, Canada. Microb Ecol 59:724–733. doi: 10.1007/s00248-009-9629-2 PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Iván Sánchez-Castro
    • 1
    Email author
  • Nuria Ferrol
    • 1
  • Pablo Cornejo
    • 2
  • José-Miguel Barea
    • 1
  1. 1.Departamento de Microbiología del Suelo y Sistemas SimbióticosEstación Experimental del Zaidín, CSICGranadaSpain
  2. 2.Scientific and Technological Bioresource NucleusUniversidad de La FronteraTemucoChile

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