Skip to main content

Advertisement

SpringerLink
Log in

The influence of environmental degradation processes on the arbuscular mycorrhizal fungal community associated with yew (Taxus baccata L.), an endangered tree species from Mediterranean ecosystems of Southeast Spain

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Aims

To assess whether the yew roots, which are able to provide a very constant environment due to their long life-span, can maintain the original arbuscular mycorrhizal (AM) fungal community during yew population decline.

Methods

The diversity of AM fungi (AMF) colonizing the roots of yew was analyzed by selecting the small subunit ribosomal RNA genes to construct a database of the overall community of AMF in the experimental area. A terminal restriction fragment length polymorphism (TRFLP) approach was used to identify the AMF communities present in yew roots. Physiological and environmental variables related to topology and soil and plant characteristics were determined as markers of habitat degradation.

Results

The AMF communities within yew roots were found to be dependent on soil, plant and topological variables indicative of habitat degradation surrounding the yew. The phylogenetic diversity of AMF associated to the yews was lower in habitats more exposed to degradation than in those better conserved.

Conclusions

The target yews can be grouped into two degradation levels. AMF communities were also affected by the degradation processes affecting their hosts. This finding rules out the role of these trees as refugia for their original AMF community, a fact that should be considered in plant reintroduction programs using AMF as bioenhancers.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

AM:

Arbuscular mycorrhizal

AMF:

Arbuscular mycorrhizal fungi

PCA:

Principal component analysis

PCR:

Polymerase chain reaction

RDA:

Redundancy analysis

SLA:

Specific leaf area

TRFLP:

Terminal restriction fragment length polymorphism

References

  • Allen MF (1988) Belowground structure: A key to reconstructing a productive arid ecosystem. In: Allen EB (ed) Reconstruction of disturbed arid ecosystems. Westview Press, Boulder, pp 113–135

    Google Scholar 

  • Allen MF (2007) Mycorrhizal fungi: highways for water and nutrients in arid soils. Vadose Zone J 6:291–297

    Article  Google Scholar 

  • Angold PG (1997) The impact of a road upon adjacent heathland vegetation: effects on plant species composition. J Appl Ecol 34:409–417

    Article  Google Scholar 

  • Antunes PM, Koch AM, Dunfield KE, Hart MM, Downing A, Rillig MC, Klironomos JN (2009) Influence of commercial inoculation with Glomus intraradices on the structure and functioning of an AM fungal community from an agricultural site. Plant Soil 317:257–266

    Article  CAS  Google Scholar 

  • Azcón-Aguilar C, Palenzuela J, Roldán A, Bautista S, Vallejo R, Barea JM (2003) Analysis of the mycorrhizal potential in the rizhosphere of representative plant species from desertification-threatened Mediterranean shrublands. Appl Soil Ecol 22:29–37

    Article  Google Scholar 

  • Barea JM, Pozo MJ, Azcón R, Azcón-Aguilar C (2005) Microbial co-operation in the rhizosphere. J Exp Bot 417:1761–1778

    Article  Google Scholar 

  • Barea JM, Palenzuela J, Cornejo P, Sánchez-Castro I, Navarro-Fernández C, López-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 75:1292–1301

    Article  Google Scholar 

  • Blanca G, Morales C (1991) Flora del parque natural de la Sierra de Baza. University of Granada, Granada

    Google Scholar 

  • Brundrett MC (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320:37–77

    Article  CAS  Google Scholar 

  • Caravaca F, Alguacil MM, Barea JM, Roldán A (2005) Survival of inocula and native AM fungi species associated with shrubs in a degraded Mediterranean ecosistema. Soil Biol Biochem 37:227–233

    Article  CAS  Google Scholar 

  • Centro Nacional de Información Geográfica (2004) MDT200. Plan Nacional de Ortofotografía Aérea. Ministerio de Fomento, Spain

    Google Scholar 

  • Collins RE, Rocap G (2007) REPK: an analytical web server to select retriction endonucleases for terminal restriction fragment length polymorphism analysis. Nucleic Acids Res 35:W58–W62. doi:10.1093/nar/gkm384

    Article  PubMed  Google Scholar 

  • Cornelissen JHC, Lavorel S, Garnier E, Díaz S, Buchmann N, Gurvich DE, Reich PB, ter Steege H, Morgan HD, van der Heijden MGA, Pausas JG, Poorter H (2003) A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Aust J Bot 51:335–380

    Article  Google Scholar 

  • Davison J, Öpik M, Daniell TJ, Moora M, Zobel M (2011) Arbuscular mycorrhizal fungal communitites in plant roots are not random assemblages. FEMS Microbiol Ecol 78:103–115

    Article  PubMed  CAS  Google Scholar 

  • Dickie IA, FitzJohn RG (2007) Using terminal restriction fragment length polymorphism (T-RFLP) to identify mycorrhizal fungi: a methods review. Mycorrhiza 17:259–270

    Article  PubMed  CAS  Google Scholar 

  • Egerton-Warburton LM, Allen EB (2000) Shifts in arbuscular mycorrhizal communities along an anthropogenic nitrogen deposition gradient. Ecol Appl 10:484–496

    Google Scholar 

  • FitzJohn RG, Dickie IA (2007) TRAMPR: an R package for analysis and matching of terminal-restriction fragment length polymorphism (TRFLP) profiles. Mol Ecol Notes 7:583–587

    Article  CAS  Google Scholar 

  • Fitzsimons MS, Miller RM, Jastrow JD (2008) Scale-dependent niche axes of arbuscular mycorrhizal fungi. Oecologia 158:117–127

    Article  PubMed  Google Scholar 

  • García D, Zamora R, Hódar JA, Gómez JM, Castro J (2000) Yew (Taxus baccata L.) regeneration is facilitated by fleshy-fruited shrubs in Mediterranean environments. Biol Conserv 95:31–38

    Article  Google Scholar 

  • Grilli G, Urcelay C, Galetto L (2012) Forest fragment size and nutrient availability: complex responses of mycorrhizal fungi in native-exotic hosts. Plant Ecol 213:155–165

    Article  Google Scholar 

  • Grime JP, Mackey JML, Hillier SH, Read DJ (1987) Floristic diversity in a model system using experimental microcosms. Nature 328:420–422

    Article  Google Scholar 

  • Hammer O, Harper DAT, Ryan PD (2001) PAST: Paleontological Statistics Software Package for education and data analysis. Palaeontol Electron 4

  • Harley JL, Harley EL (1987) A check-list of mycorrhiza in the British flora. New Phytol (Suppl) 105:1–102

    Article  Google Scholar 

  • Holland SM (2008) Analytic Rarefaction 1.3. http://strata.uga.edu/software/anRareReadme.html

  • Ijdo M, Schtickzelle N, Cranenbrouck S, Declerk S (2010) Do arbuscular mycorrhizal fungi with contrasting life-history strategies differ in their responses to repeated defoliation? FEMS Microbiol Ecol 72:114–122

    Article  PubMed  CAS  Google Scholar 

  • 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 13:1164–1176

    Article  Google Scholar 

  • Jeffries P, Barea JM (2012) Arbuscular mycorrhiza - a key component of sustainable plant-soil ecosystems. In: Hock B (ed) The mycota, vol IX. Fungal Associations, 2nd edn. Springer-Verlag, Berlin, Heidelberg (in press)

  • Johnson NC (2010) Resource stoichiometry elucidates th estructure and function of arbuscular mycorrhizas across scales. New Phytol 185:631–647

    Article  PubMed  CAS  Google Scholar 

  • Junier P, Junier T, Witzel KP (2008) TRiFLe, a program for in silico terminal restriction fragment length polymorphism analysis with user-defined sequence sets. Appl Environ Microbiol 74:6452–6456

    Article  PubMed  CAS  Google Scholar 

  • Junta de Andalucía (2003) Ortofotografía digital de Andalucía, provincia de Granada. Junta de Andalucía, Sevilla

  • Kéfi S, Rietkerk M, Alados CL, Pueyo Y, ElAich A, Papanastasis V, de Ruiter PC (2007) Spatial vegetation patterns and imminent desertification in Mediterranean arid ecosystems. Nature 449:213–218

    Article  PubMed  Google Scholar 

  • 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 193:970–984

    Article  PubMed  Google Scholar 

  • Lee J, Lee S, Young PW (2008) Improved PCR primers for the detection and identification of arbuscular mycorrhizal fungi. FEMS Microbiol Ecol 65:339–349

    Article  PubMed  CAS  Google Scholar 

  • Lucas-Borja ME, Bastida F, Moreno JL, Nicolás C, Andres M, López FR, del Cerro A (2011) The effects of human trampling on the microbiological properties of soil and vegetation in mediterranean mountain areas. Land Degrad Dev 22:383–394

    Article  Google Scholar 

  • Malmivaara-Lämsä M, Hamberg L, Haapamäki E, Liski J, Kotze DJ, Lehvävirta S, Fritze H (2008) Edge effects and trampling in boreal urban forest fragments – impacts on the soil microbial community. Soil Biol Biochem 40:1612–1621

    Article  Google Scholar 

  • McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290–297

    Article  Google Scholar 

  • McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol 115:495–501

    Article  Google Scholar 

  • Mummey DL, Rillig MC (2008) Spatial characterization of arbuscular mycorrhizal fungal molecular diversity at the submetre scale in a temperate grassland. FEMS Microbiol Ecol 64:260–270

    Article  PubMed  CAS  Google Scholar 

  • Mummey DL, Clarke JT, Cole A, O’Connor BG, Gannon JE, Ramsey PW (2010) Spatial análisis reveals differences in soil microbiol community interactions between adjacent coniferous forest and clearcut ecosystems. Soil Biol Biochem 42:1138–1147

    Article  CAS  Google Scholar 

  • 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 134:257–268

    Article  Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Henry M, Stevens H, Wagner H (2011) Vegan: Community ecology package. R package version 2.0-1. http://CRAN.R-project.org/package=vegan

  • Olsen SR, Cole CV, Watanabe FS, Dean LA (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. USDA Circular 939. US gov Print Office, Washington DC

    Google Scholar 

  • Öpik M, Metsis M, Daniell TJ, Zobel M, Moora M (2009) Large-scale parallel 454 sequencing reveals host ecological group specifity of arbuscular mycorrhizal fungi in a boreonemoral forest. New Phytol 184:424–437

    Article  PubMed  Google Scholar 

  • Öpik M, Vanatoa E, Moora M, Davison J, Kalwij JM, Reier Ü, Zobel M (2010) The online database MarrjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytol 188:223–241

    Article  PubMed  Google Scholar 

  • Ordiales-Plaza R (2000) Midebmp, Version 4.2. Estación Experimental de Zonas Áridas (CSIC), Almería

    Google Scholar 

  • Peay KG, Bruns TD, Kennedy PG, Bergemann SE, Garbelotto M (2007) A strong species-area relationship for eukariotic soil microbes: island size matters for ectomycorrhizal fungi. Ecol Lett 10:470–480

    Article  PubMed  Google Scholar 

  • 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 55:158–161

    Article  Google Scholar 

  • Pons A (1981) The History of the Mediterranean shrublands. In: Di Castri F, Goodall DW, Specht RL (eds) Mediterranean-type shrublands. Elsevier Academic Press, Amsterdam, pp 131–138

    Google Scholar 

  • 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 Biol Sci 276:4237–4245

    Article  Google Scholar 

  • R Development Core Team (2010) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Requena N, Perez-Solis E, Azcón-Aguilar C, Jeffries P, Barea JM (2001) Management of indigenous plant-microbe symbioses aids restoration of desertified. Appl Environ Microbiol 67:495–498

    Article  PubMed  CAS  Google Scholar 

  • Rillig MC, Mummey DL (2006) Mycorrhizas and soil structure. New Phytol 171:41–53

    Article  PubMed  CAS  Google Scholar 

  • Robinson-Boyer L, Grzyb I, Jeffries P (2009) Shifting the balance from qualitative to quantitative analysis of arbuscular mycorrhizal communities in field soils. Fungal Ecol 2:1–9

    Article  Google Scholar 

  • 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 80:1–9

    Article  Google Scholar 

  • 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 22:449–460

    Article  PubMed  Google Scholar 

  • 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 21:211–220

    Google Scholar 

  • Simon LM, Lalonde TD, Bruns TD (1992) Specific amplification of 18S fungal ribosomal genes from vesicular arbuscular endomycorrhizal fungi colonising roots. Appl Environ Microbiol 58:291–295

    PubMed  CAS  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Elsevier Academic Press, New York

    Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Thomas PA, Polwart A (2003) Taxus baccata L. J Ecol 91:489–524

    Article  Google Scholar 

  • Truscott AM, Palmer SCF, McGowan GM, Cape JN, Smart S (2005) Vegetation composition of roadside verges in Scotland: the effects of nitrogen deposition, disturbance and management. Environ Pollut 136:109–118

    Article  PubMed  CAS  Google Scholar 

  • Tutin TG, Heywood VH, Burges NA, Moore DM, Valentine DH, Walters SM, Webb DA (eds) (1980) Flora Europaea, vols. 1-5. Cambridge University Press, Cambridge

    Google Scholar 

  • 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 396:69–72

    Article  Google Scholar 

  • 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 172:739–752

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

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 Goverment under the Plan Nacional de I+D+I (project CGL-2009-08825). We strongly thank Dr. I. Sánchez-Castro for the permission to use the Sierra de Baza AMF database created during his PhD Thesis. We also sincerely thank Professor P. Jeffries (Univ. of Kent) for grammatical corrections to the manuscript. We thank the Consejería de Medio Ambiente, Junta de Andalucía (Spain) for permission to work in Sierra de Baza Natural Park and to Drs. F. Bruno and J. Molero for helping us to identify and interpret vegetation inventories. Additionally, we would like to thank the two anonymous reviewers and the Section Editor for their valuable comments and suggestions to improve the manuscript.

Author information

Authors and Affiliations

  1. Soil Microbiology and Symbiotic Systems Department, Estación Experimental del Zaidín, CSIC, C/ Profesor Albareda 1, 18008, Granada, Spain

    Álvaro López-García, Juan de D. Miranda, José M. Barea & Concepción Azcón-Aguilar

  2. Plant Ecology, Institut für Biologie, Freie Universität Berlin, Altensteinstr. 6, 14195, Berlin, Germany

    Stefan Hempel & Matthias C. Rillig

Authors
  1. Álvaro López-García
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stefan Hempel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Juan de D. Miranda
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Matthias C. Rillig
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. José M. Barea
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Concepción Azcón-Aguilar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Álvaro López-García.

Additional information

Responsible Editor: Thom W. Kuyper.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 19 kb)

Fig. S1

Neighbor-joining phylogenetic tree based on the NS31-AML2 fragment of the SSU rDNA gene. Sequences from single AMF spores and root samples from the Sierra de Baza Natural Park are showed together with reference sequences from GeneBank. Numbers above branches indicate the bootstrap values. Only topologies with values ≥50 % are shown (1,000 replicates). Sequences are labelled according to the data set from which it originated (Tb-root = obtained from T. baccata roots; SB-root = from roots of other plants characteristic of the site; SB-spore = from spores isolated from the Sierra de Baza Natural Park), followed by the clone identity number. Sequences having a pairwise similarity higher than 97 % were clustered as phylotypes (delimited by vertical lines). Phylotypes are named following the closest virtual taxa code of MaarjAM database (Öpik et al. 2010). The prefix corresponds to the glomeromycotan family (following Krüger et al. 2012): Aca-Acaulosporaceae, Glo-Glomeraceae, Cla-Claroideoglomeraceae, Par-Paraglomeraceae, Pac-Pacisporaceae, Div-Diversisporaceae and Gig-Gigasporaceae. Mortierella polycephala was used as out-group. To reduce the size of the tree, half of the sequences were removed (JPEG 78 kb)

High Resolution Image (TIFF 10489 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

López-García, Á., Hempel, S., de D. Miranda, J. et al. The influence of environmental degradation processes on the arbuscular mycorrhizal fungal community associated with yew (Taxus baccata L.), an endangered tree species from Mediterranean ecosystems of Southeast Spain. Plant Soil 370, 355–366 (2013). https://doi.org/10.1007/s11104-013-1625-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-013-1625-0

Keywords

Search

Navigation