Plant and Soil

, Volume 379, Issue 1–2, pp 247–260 | Cite as

Life-history strategies of arbuscular mycorrhizal fungi determine succession into roots of Rosmarinus officinalis L., a characteristic woody perennial plant species from Mediterranean ecosystems

  • Álvaro López-GarcíaEmail author
  • Javier Palenzuela
  • José Miguel Barea
  • Concepción Azcón-Aguilar
Regular Article



Few studies have analyzed life-history strategies of arbuscular mycorrhizal fungi (AMF), in terms of the different propagule types they produce, and their ability to colonize new seedlings. The aim was to assess whether life-history strategies influence AMF successional dynamics and assemblages.


Rosemary (Rosmarinus officinalis L.) seedlings, grown in a mesocosm system, were colonized by either the AMF hyphae coming from a living rosemary plant, or from spores germinating in soil. The AMF community established in the plantlets was monitored every 3 months during 2 years, using terminal restriction fragment length polymorphism of genes coding for rDNA.


The two different sources of AMF propagules resulted in a different initial community colonizing rosemary roots. AMF propagating from hyphae attached to living mycorrhizal-roots seemed to colonize faster and were season-dependent. AMF taxa originating from soil-borne propagules were most frequent over time and exhibit the dominant colonization strategy in this system. The evolution of the AMF community also revealed different strategies in succession.


AMF associated with rosemary evidenced contrasting life-history strategies in terms of source of inoculum for new colonization and hence survival. The observed successional dynamics of AMF have implications for understanding the ecological processes in Mediterranean environments and seasonality of colonization processes.


Arbuscular mycorrhizal fungi Life-history strategies Mycorrhizal propagules Rosmarinus officinalis (rosemary) Succession TRFLP 



A. López-García thanks the Formación de Personal Investigador Programme (Ministerio de Ciencia e Innovación, Spain) for financial support. This research was supported by the Spanish Government under the Plan Nacional de I+D+I (project CGL-2009-08825). We sincerely thank Professor Peter Jeffries (Univ. of Kent) for editing comments and grammatical corrections to the manuscript, Dr. Nuria Ferrol for helpful discussions, Dr. Søren Rosendahl and Dr. Alicia Barroso for advices on optimizing the SSCP and TRFLP protocols. Additionally, we would like to thank the two anonymous reviewers and the Section Editor for their valuable comments and suggestions to improve the manuscript. We also thank the Consejería de Medio Ambiente, Junta de Andalucía (Spain) for permission to work in Sierra de Baza Natural Park.

Supplementary material

11104_2014_2060_MOESM1_ESM.pdf (60 kb)
Fig. S1 (PDF 60 kb)
11104_2014_2060_MOESM2_ESM.pdf (784 kb)
Fig. S2 (PDF 783 kb)
11104_2014_2060_MOESM3_ESM.pdf (112 kb)
Fig. S3 (PDF 112 kb)


  1. Allen MF, Kitajima K (2013) In situ high-frequency observations of mycorrhizas. New Phytol 200:222–228PubMedCrossRefGoogle Scholar
  2. Avio L, Pellegrino E, Bonari E, Giovannetti M (2006) Functional diversity of arbuscular mycorrhizal fungal isolates in relation to extraradical mycelial networks. New Phytol 172:347–357PubMedCrossRefGoogle Scholar
  3. Barea JM, Azcón-Aguilar C (2013) Evolution, biology and ecological effects of arbuscular mycorrhizas. In: Comisão AF, Pedroso CC (eds) Symbiosis: evolution, biology and ecological effects. Nova, New York, pp 1–34Google Scholar
  4. 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
  5. Bever JD, Richardson SC, Brandy ML, Holmes J, Watson M (2009) Preferential allocation to beneficial symbiont with spatial structure maintains mycorrhizal mutualism. Ecol Lett 12:13–21PubMedCrossRefGoogle Scholar
  6. Boddington CL, Dodd JC (1999) Evidence that differences in phosphate metabolism in mycorrhizas formed by species of Glomus and Gigaspora might be related to their life-cycle strategies. New Phytol 142:531–538CrossRefGoogle Scholar
  7. Chagnon PL, Bradley RL, Maherali H, Klironomos JN (2013) A trait-based framework to understand life history of mycorrhizal fungi. Trends Plant Sci 18:484–491PubMedCrossRefGoogle Scholar
  8. Collins RE, Rocap G (2007) REPK: an analytical web server to select restriction endonucleases for terminal restriction fragment length polymorphism analysis. Nucleic Acids Res 35:W58–W62PubMedCentralPubMedCrossRefGoogle Scholar
  9. Cornejo P, Azcón-Aguilar C, Barea JM, Ferrol N (2004) Temporal temperature gradient gel electrophoresis (TTGE) as a tool for the characterization of arbuscular mycorrhizal fungi. FEMS Microbiol Lett 241:265–270PubMedCrossRefGoogle Scholar
  10. Davison J, Öpik M, Daniell TJ, Moora M, Zobel M (2011) Arbuscular mycorrhizal fungal communities in plant roots are not random assemblages. FEMS Microbiol Ecol 178:103–115CrossRefGoogle Scholar
  11. Denison RF, Kiers ET (2011) Life histories of symbiotic rhizobia and mycorrhizal fungi. Curr Biol 21:775–785CrossRefGoogle Scholar
  12. Dickie IA, FitzJohn RG (2007) Using terminal restriction fragment length polymorphism (T-RFLP) to identify mycorrhizal fungi: a methods review. Mycorrhiza 17:259–270PubMedCrossRefGoogle Scholar
  13. Dufrêne M, Legendre P (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol Monogr 67:345–366Google Scholar
  14. Dumbrell AJ, Ashton PD, Aziz N, Feng G, Nelson M, Dytham C, Fitter AH, Helgason T (2011) Distinct seasonal assemblages of arbuscular mycorrhizal fungi revealed by massively parallel pyrosequencing. New Phytol 190:794–804PubMedCrossRefGoogle Scholar
  15. FitzJohn RG, Dickie IA (2007) TRAMPR: an R package for analysis and matching of terminal-restriction fragment length polymorphism (TRFLP) profiles. Mol Ecol Notes 7:583–587CrossRefGoogle Scholar
  16. Franson RL, Bethlenfalvay GJ (1989) Infection unit method of vesicular-arbuscular mycorrhizal propagule determination. Soil Sci Soc Am J 53:754–756CrossRefGoogle Scholar
  17. Grman E (2012) Plant species differ in their ability to reduce allocation to non-beneficial arbuscular mycorrhizal fungi. Ecology 93:711–718PubMedCrossRefGoogle Scholar
  18. Hart MM, Reader JR (2002) Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi. New Phytol 153:335–344CrossRefGoogle Scholar
  19. Hart MM, Reader RJ (2005) The role of the external mycelium in early colonization for three arbuscular mycorrhizal fungal species with different colonization strategies. Pedobiologia 49:269–279CrossRefGoogle Scholar
  20. Hart MM, Reader JR, Klironomos JN (2001) Life-history strategies of arbuscular mycorrhizal fungi in relation to their successional dynamics. Mycologia 93:1186–1194CrossRefGoogle Scholar
  21. Helgason T, Fitter AH (2009) Natural selection and the evolutionary ecology of the arbuscular mycorrhizal fungi (Phylum Glomeromycota). J Exp Bot 60:2465–2480PubMedCrossRefGoogle Scholar
  22. Hempel S, Renker C, Buscot F (2007) Differences in the species composition of arbuscular mycorrhizal fungi in spore, root and soil communities in a grassland ecosystem. Environ Microbiol 9:1930–1938PubMedCrossRefGoogle Scholar
  23. Holland SM (2008) Analytic rarefaction 1.3. UGA Stratigraphy Lab. Accessed 1 March 2012
  24. Husband R, Herre EA, Turner SL, Gallery R, Young JPW (2002) Molecular diversity of arbuscular mycorrhizal fungi and patterns of host association over time and space in a tropical forest. Mol Ecol 11:2669–2678PubMedCrossRefGoogle Scholar
  25. IJdo M, Schtickzelle N, Cranenbrouck S, Declerck S (2010) Do arbuscular mycorrhizal fungi with contrasting life-history strategies differ in their responses to repeated defoliation? FEMS Microbiol Ecol 72:114–122PubMedCrossRefGoogle Scholar
  26. Jansa J, Mozafar A, Kuhn G, Anken T, Ruh R, Sanders IR, Frossard E (2003) Soil tillage affects the community structure of mycorrhizal fungi in maize roots. Ecol Appl 13:1164–1176CrossRefGoogle Scholar
  27. Jasper DA, Abbott LK, Robson AD (1989) Soil disturbance reduces the infectivity of external hyphae of vesicular arbuscular mycorrhizal fungi. New Phytol 112:93–99CrossRefGoogle Scholar
  28. Kjøller R, Rosendahl S (2000) Detection of arbuscular mycorrhizal fungi (Glomales) in roots by nested PCR and SSCP (Single Strand Conformation Polymorphism). Plant Soil 226:189–196CrossRefGoogle Scholar
  29. Koide RT, Mosse B (2004) A history of research on arbuscular mycorrhiza. Mycorrhiza 14:145–163PubMedCrossRefGoogle Scholar
  30. Krüger M, Krüger C, Walker C, Stockinger H, Schüssler A (2012) Phylogenetic reference data for systematics and phylotaxonomy of arbuscular mycorrhizal fungi from phylum to species level. New Phytol 193:970–984PubMedCrossRefGoogle Scholar
  31. Lee J, Lee S, Young JPW (2008) Improved PCR primers for the detection and identification of arbuscular mycorrhizal fungi. FEMS Microbiol Ecol 65:339–349PubMedCrossRefGoogle Scholar
  32. López-Bermúdez F, Albadalejo J, Stocking MA, Díaz E (1990) Factores ambientales de la degradación del suelo en el área mediterránea. In: Albadalejo J, Stocking MA, Díaz E (eds) Degradation and rehabilitation of soil in Mediterranean environmental conditions. CSIC, Murcia, pp 15–45Google Scholar
  33. Maherali H, Klironomos JN (2012) Phylogenetic and trait-based assembly of arbuscular mycorrhizal fungal communities. PLoS ONE 7:e36695PubMedCentralPubMedCrossRefGoogle Scholar
  34. McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290–297CrossRefGoogle Scholar
  35. McGonigle T, Miller M, Evans D, Fairchild G, Swan J (1990) A new method which gives an objective-measure of colonization of roots. New Phytol 115:495–501CrossRefGoogle Scholar
  36. Médail F, Quézel P (1997) Hot-spots analysis for conservation of plant biodiversity in the Mediterranean basin. Ann Mo Bot Gard 84:112–127CrossRefGoogle Scholar
  37. Merryweather J, Fitter AH (1998) The arbuscular mycorrhizal fungi of Hyacinthoides non-scripta–II. Seasonal and spatial patterns of fungal populations. New Phytol 138:131–142CrossRefGoogle Scholar
  38. Munkvold L, Kjøller R, Vestberg M, Rosendahl S, Jakobsen I (2004) High functional diversity within species of arbuscular mycorrhizal fungi. New Phytol 164:357–364CrossRefGoogle Scholar
  39. Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858PubMedCrossRefGoogle Scholar
  40. Oehl F, Sieverding E, Palenzuela J, Ineichen K, da Silva GA (2011) Advances in Glomeromycota taxonomy and classification. IMA Fungus 2:191–199PubMedCentralPubMedCrossRefGoogle Scholar
  41. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Henry M, Stevens H et al. (2011) Vegan: community ecology package. R package version 2.0-1. R Project. Accessed 1 March 2012
  42. Öpik M, Vanatoa E, Moora M, Davison J, Kalwij JM, Reier Ü, Zobel M (2010) The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytol 188:223–241PubMedCrossRefGoogle Scholar
  43. Peay KG, Kennedy PG, Bruns TD (2011) Rethinking ectomycorrhizal succession: are root density and hyphal exploration types drivers of spatial and temporal zonation? Fungal Ecol 4:233–240CrossRefGoogle Scholar
  44. Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161CrossRefGoogle Scholar
  45. Powell JR, Parrent JL, Hart MM, Klironomos JN, Rillig MC, Maherali H (2009) Phylogenetic trait conservatism and the evolution of functional trade-offs in arbuscular mycorrhizal fungi. Proc R Soc B 276:4237–4245PubMedCentralPubMedCrossRefGoogle Scholar
  46. 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
  47. R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  48. Rillig MC (2004) Arbuscular mycorrhizae and terrestrial ecosystem processes. Ecol Lett 7:740–754CrossRefGoogle Scholar
  49. Roberts DW (2010) labdsv: ordination and multivariate analysis for ecology. R package version 1.4-1. R Project. Accessed 1 March 2012
  50. Rosendahl S, Stukenbrock EH (2004) Community structure of arbuscular mycorrhizal fungi in undisturbed vegetation revealed by analyses of LSU rDNA sequences. Mol Ecol 13:3179–3186PubMedCrossRefGoogle Scholar
  51. Sánchez-Castro I, Ferrol N, Barea JM (2012a) Analyzing the community composition of arbuscular mycorrhizal fungi colonizing the roots of representative shrubland species in a Mediterranean ecosystem. J Arid Environ 80:1–9CrossRefGoogle Scholar
  52. Sánchez-Castro I, Ferrol N, Cornejo P, Barea JM (2012b) Temporal dynamics of arbuscular mycorrhizal fungi colonizing roots of representative shrub species in a semi-arid Mediterranean ecosystem. Mycorrhiza 22:449–460PubMedCrossRefGoogle Scholar
  53. Schnoor TK, Lekberg Y, Rosendahl S, Olsson PA (2011) Mechanical soil disturbance as a determinant of arbuscular mycorrhizal fungal communities in semi-natural grassland. Mycorrhiza 21:211–220PubMedCrossRefGoogle Scholar
  54. Simon LM, Lalonde TD, Bruns TD (1992) Specific amplification of 18S fungal ribosomal genes from vesicular arbuscular endomycorrhizal fungi colonising roots. Appl Environ Microbiol 58:291–295PubMedCentralPubMedGoogle Scholar
  55. Sýkorová Z, Ineichen K, Wiemken A, Redecker D (2007) The cultivation bias: different communities of arbuscular mycorrhizal fungi detected in roots from the field, from bait plants transplanted to the field, and from a greenhouse trap experiment. Mycorrhiza 18:1–14PubMedCrossRefGoogle Scholar
  56. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599PubMedCrossRefGoogle Scholar
  57. Tommerup IC, Abbott LK (1981) Prolonged survival and viability of VA mycorrhizal hyphae after root death. Soil Biol Biochem 13:431–433CrossRefGoogle Scholar
  58. 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
  59. van der Heijden MGA, Scheublin TR (2007) Functional traits in mycorrhizal ecology: their use for predicting the impact of arbuscular mycorrhizal fungal communities on plant growth and ecosystem functioning. New Phytol 174:244–250PubMedCrossRefGoogle Scholar
  60. 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
  61. van der Heijden MGA, Streitwolf-Engel R, Riedl R, Siegrist S, Neudecker A, Ineichen K, Boller T, Wiemken A, Sanders IR (2006) The mycorrhizal contribution to plant productivity, plant nutrition and soil structure in experimental grassland. New Phytol 172:739–752PubMedCrossRefGoogle Scholar
  62. Vogelsang KM, Reynolds HL, Bever JD (2006) Mycorrhizal fungal identity and richness determine the diversity and productivity of a tallgrass prairie system. New Phytol 172:554–562PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Álvaro López-García
    • 1
    Email author
  • Javier Palenzuela
    • 1
  • José Miguel Barea
    • 1
  • Concepción Azcón-Aguilar
    • 1
  1. 1.Soil Microbiology and Symbiotic Systems DepartmentCSIC-Estación Experimental del ZaidínGranadaSpain

Personalised recommendations