Skip to main content

Potato-associated arbuscular mycorrhizal fungal communities in the Peruvian Andes

Abstract

The world's fourth largest food crop, potato, originates in the Andes. Here, the community composition of arbuscular mycorrhizal fungi (AMF) associated with potato in Andean ecosystems is described for the first time. AMF were studied in potato roots and rhizosphere soil at four different altitudes from 2,658 to 4,075 m above mean sea level (mamsl) and in three plant growth stages (emergence, flowering, and senescence). AMF species were distinguished by sequencing an approx. 1,500 bp nuclear rDNA region. Twenty species of AMF were identified, of which 12 came from potato roots and 15 from rhizosphere soil. Seven species were found in both roots and soil. Interestingly, altitude affected species composition with the highest altitude exhibiting the greatest species diversity. The three most common colonizers of potato roots detected were Funneliformis mosseae, an unknown Claroideoglomus sp., and Rhizophagus irregularis. Notably, the potato-associated AMF diversity observed in this Andean region is much higher than that reported for potato in other ecosystems. Potato plants were colonized by diverse species from 8 of the 11 Glomeromycota families. Identification of the AMF species is important for their potential use in sustainable management practices to improve potato production in the Andean region.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  • Alguacil MM, Díaz-Pereira E, Caravaca F, Fernández DA, Roldán A (2009) Increased diversity of arbuscular mycorrhizal fungi in a long-term field experiment via application of organic amendments to a semiarid degraded soil. Appl Environ Microbiol 75:4254–4263

    CAS  Article  Google Scholar 

  • Bharadwaj DP, Lundquist PO, Alström S (2007) Impact of plant species grown as monocultures on sporulation and root colonization by native arbuscular mycorrhizal fungi in potato. Appl Soil Ecol 35:213–225

    Article  Google Scholar 

  • Bhattarai I, Mishra R (1984) Study on the vesicular–arbuscular mycorrhiza of three cultivars of potato (Solanum tuberosum). Plant Soil 79:299–303

    Article  Google Scholar 

  • Birch PJ, Bryan G, Fenton B, Gilroy E, Hein I, Jones J, Prashar A, Taylor M, Torrance L, Toth I (2012) Crops that feed the world 8: potato: are the trends of increased global production sustainable? Food Sec 4:477–508

    Article  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

    CAS  Article  Google Scholar 

  • Brush S, Kesseli R, Ortega R, Cisneros P, Zimmerer K, Quiros C (1995) Potato diversity in the Andean center of crop domestication. Conserv Biol 9:1189–1198

    Article  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Chaurasia B, Pandey A, Palni LMS (2005) Distribution, colonization and diversity of arbuscular mycorrhizal fungi associated with central Himalayan rhododendrons. For Ecol Manage 207:315–324

    Article  Google Scholar 

  • Davies JFT, Calderón CM, Huaman Z, Gómez R (2005a) Influence of a flavonoid (formononetin) on mycorrhizal activity and potato crop productivity in the highlands of Peru. Sci Hortic 106:318–329

    CAS  Article  Google Scholar 

  • Davies TFJ, Calderón MC, Huaman Z (2005b) Influence of arbuscular mycorrhizae indigenous to Peru and a flavonoid on growth, yield, and leaf elemental concentration of “Yungay” potatoes. Hortic Sci 40:381–385

    Google Scholar 

  • 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 78:103–115

    CAS  PubMed  Article  Google Scholar 

  • Dechassa N, Schenk MK, Claassen N, Steingrobe B (2003) Phosphorus efficiency of cabbage (Brassica oleraceae L. var. capitata), carrot (Daucus carota L.), and potato (Solanum tuberosum L.). Plant Soil 250:215–224

    CAS  Article  Google Scholar 

  • R Development Core Team (2008) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org

  • Duffy EM, Cassells AC (2000) The effect of inoculation of potato (Solanum tuberosum L.) microplants with arbuscular mycorrhizal fungi on tuber yield and tuber size distribution. Appl Soil Ecol 15:137–144

    Article  Google Scholar 

  • FAO (2012) Food and Agriculture Organization of the United Nations, Land Resources. http://www.fao.org/nr/land/en/. Accessed 07 July 2013.

  • Feinstein LM, Sul WJ, Blackwood CB (2009) Assessment of bias associated with incomplete extraction of microbial DNA from soil. Appl Environ Microbiol 75:5428–5433

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Gai J, Christie P, Cai X, Fan J, Zhang J, Feng G, Li X (2009) Occurrence and distribution of arbuscular mycorrhizal fungal species in three types of grassland community of the Tibetan Plateau. Ecol Res 24:1345–1350

    Article  Google Scholar 

  • Gosling P, Proctor M, Jones J, Bending G (2013) Distribution and diversity of Paraglomus spp. in tilled agricultural soils. Mycorrhiza. doi:10.1007/s00572-013-0505-z

    PubMed  Google Scholar 

  • Hack H, Gall H, Klemke T, Klose R, Meier U, Stauss R, Witzenberger A (1993) Phänologische Entwicklungsstadien der Kartoffel (Solanum tuberosum L.). Codierung und Beschreibung nach der erweiterten BBCH-Skala mit Abbildungen. Nachrichtenbl Deut Pflanzenschutzd 45:11–19

    Google Scholar 

  • Hannula SE, De Boer W, Van Veen JA (2010) In situ dynamics of soil fungal communities under different genotypes of potato, including a genetically modified cultivar. Soil Biol Biochem 42:2211–2223

    CAS  Article  Google Scholar 

  • Hannula SE, De Boer W, Van Veen J (2012) A 3-year study reveals that plant growth stage, season and field site affect soil fungal communities while cultivar and GM-trait have minor effects. PLoS ONE 7:e33819

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • 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 9:1930–1938

    CAS  PubMed  Article  Google Scholar 

  • Husband R, Herre EA, Turner SL, Gallery R, Young JPW (2002a) Molecular diversity of arbuscular mycorrhizal fungi and patterns of host association over time and space in a tropical forest. Mol Ecol 11:2669–2678

    CAS  PubMed  Article  Google Scholar 

  • Husband R, Herre EA, Young JPW (2002b) Temporal variation in the arbuscular mycorrhizal communities colonising seedlings in a tropical forest. FEMS Microbiol Ecol 42:131–136

    CAS  PubMed  Article  Google Scholar 

  • Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucl Acids Res 30:3059–3066

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Kõljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram M, Bates ST, Bruns TD, Bengtsson-Palme J, Callaghan TM, Douglas B, Drenkhan T, Eberhardt U, Dueñas M, Grebenc T, Griffith GW, Hartmann M, Kirk PM, Kohout P, Larsson E, Lindahl BD, Lücking R, Martín MP, Matheny PB, Nguyen NH, Niskanen T, Oja J, Peay KG, Peintner U, Peterson M, Põldmaa K, Saag L, Saar I, Schüßler A, Scott JA, Senés C, Smith ME, Suija A, Taylor DL, Teresa Telleria M, Weiß M, Larsson K-H (2013) Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol 22:5271–5277

    Google Scholar 

  • Krüger M, Stockinger H, Krüger C, Schüßler A (2009) DNA-based species level detection of Glomeromycota: one PCR primer set for all arbuscular mycorrhizal fungi. New Phytol 183:212–223

    PubMed  Article  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

    PubMed  Article  Google Scholar 

  • Liu Y, He J, Shi G, An L, Öpik M, Feng H (2011) Diverse communities of arbuscular mycorrhizal fungi inhabit sites with very high altitude in Tibet Plateau. FEMS Microbiol Ecol 78:355–365

    CAS  PubMed  Article  Google Scholar 

  • Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Lozupone C, Hamady M, Knight R (2006) UniFrac—an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinformatics 7:371

    PubMed Central  PubMed  Article  Google Scholar 

  • Lugo MA, Ferrero M, Menoyo E, Estévez MC, Siñeriz F, Anton A (2008) Arbuscular mycorrhizal fungi and rhizospheric bacteria diversity along an altitudinal gradient in South American Puna grassland. Microb Ecol 55:705–713

    CAS  PubMed  Article  Google Scholar 

  • Lugo MA, Negritto MA, Jofré M, Anton A, Galetto L (2012) Colonization of native Andean grasses by arbuscular mycorrhizal fungi in Puna: a matter of altitude, host photosynthetic pathway and host life cycles. FEMS Microbiol Ecol 81:455–466

    CAS  PubMed  Article  Google Scholar 

  • McArthur DAJ, Knowles NR (1993) Influence of species of vesicular–arbuscular mycorrhizal fungi and phosphorous nutrition on growth, development, and mineral nutrition of potato (Solanum tuberosum L.). Plant Physiol 101:771–782

    Google Scholar 

  • Ngakou A, Megueni C, Nwaga D, Mabong MR, Djamba FE, Gandebe M (2006) Solanum tuberosum (L.) responses to soil solarization and arbuscular mycorrhizal fungi inoculation under field conditions: growth, yield, health status of plants and tubers. Middle-East J Sci Res 1:23–30

    Google Scholar 

  • Oehl F, Sýkorová Z, Redecker D, Wiemken A, Sieverding E (2006) Acaulospora alpina, a new arbuscular mycorrhizal fungal species characteristic for high mountainous and alpine regions of the Swiss Alps. Mycologia 98:286–294

    PubMed  Article  Google Scholar 

  • Oehl F, Laczko E, Bogenrieder A, Stahr K, Bösch R, van der Heijden M, Sieverding E (2010) Soil type and land use intensity determine the composition of arbuscular mycorrhizal fungal communities. Soil Biol Biochem 42:724–738

    CAS  Article  Google Scholar 

  • Öpik M, Moora M (2012) Missing nodes and links in mycorrhizal networks. New Phytol 194:304–306

    PubMed  Article  Google Scholar 

  • Öpik M, Zobel M, Cantero J, Davison J, Facelli J, Hiiesalu I, Jairus T et al (2013) Global sampling of plant roots expands the described molecular diversity of arbuscular mycorrhizal fungi. Mycorrhiza 23:411–430

    PubMed  Article  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 

  • Rahbek C (1995) The elevational gradient of species richness: a uniform pattern? Ecography 18:200–205

    Article  Google Scholar 

  • Redecker D, Schüßler A, Stockinger H, Stürmer SL, Morton JB, Walker C (2013) An evidence-based consensus for the classification of arbuscular mycorrhizal fungi (Glomeromycota). Mycorrhiza 23:515–531

    Google Scholar 

  • Renker C, Blanke V, Buscot F (2005) Diversity of arbuscular mycorrhizal fungi in grassland spontaneously developed on area polluted by a fertilizer plant. Environ Pollut 135:255–266

    Google Scholar 

  • Sambrook J, Russell DW (2006) Purification of nucleic acids by extraction with phenol:chloroform. Cold Spring Harbor Protoc 2006: pdb.prot4455

  • Sánchez-Castro I, Ferrol N, Cornejo P, Barea JM (2012) Temporal dynamics of arbuscular mycorrhizal fungi colonizing roots of representative shrub species in a semi-arid Mediterranean ecosystem. Mycorrhiza 22:449–460

    PubMed  Article  Google Scholar 

  • Sanders NJ, Rahbek C (2012) The patterns and causes of elevational diversity gradients. Ecography 35:1–3

    Article  Google Scholar 

  • Schmidt SK, Sobieniak-Wiseman LC, Kageyama SA, Halloy SRP, Schadt CW (2008) Mycorrhizal and dark-septate fungi in plant roots above 4270 meters elevation in the Andes and rocky mountains. Arct Antarct Alp Res 40:576–583

    Article  Google Scholar 

  • Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, Chen W, Bolchacova E, Voigt K, Crous PW et al (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc Natl Acad Sci U S A 109:6241–6246

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Sikes BA, Maherali H, Klironomos JN (2012) Arbuscular mycorrhizal fungal communities change among three stages of primary sand dune succession but do not alter plant growth. Oikos 121:1791–1800

    Article  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, London

    Google Scholar 

  • Spooner DM, McLean K, Ramsay G, Waugh R, Bryan GJ (2005) A single domestication for potato based on multilocus amplified fragment length polymorphism genotyping. Proc Natl Acad Sci U S A 102:14694–14699

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 57:758–771

    PubMed  Article  Google Scholar 

  • Stockinger H, Walker C, Schüßler A (2009) “Glomus intraradices DAOM197198”, a model fungus in arbuscular mycorrhiza research, is not Glomus intraradices. New Phytol 183:1176–1187

    PubMed  Article  Google Scholar 

  • Stockinger H, Krüger M, Schüßler A (2010) DNA barcoding of arbuscular mycorrhizal fungi. New Phytol 187:461–474

    CAS  PubMed  Article  Google Scholar 

  • 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 18:1–14

    PubMed  Article  Google Scholar 

  • Urcelay C, Acho J, Joffre R (2011) Fungal root symbionts and their relationship with fine root proportion in native plants from the Bolivian Andean highlands above 3,700 m elevation. Mycorrhiza 21:323–330

    PubMed  Article  Google Scholar 

  • Verbruggen E, Van der Heijden MGA, Rillig MC, Kiers ET (2013) Mycorrhizal fungal establishment in agricultural soils: factors determining inoculation success. New Phytol 197:1104–1109

    PubMed  Article  Google Scholar 

Download references

Acknowledgments

The research leading to these results has received funding from the European Community's Seventh Framework Programme FP7/2007-2013 under grant agreement no. 227522.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Arthur Schüßler.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Fig. 1

Full phylogenetic analysis showing the species detected in the Peruvian potato fields and AMF representatives from all orders of the Glomeromycota. Sequences obtained by Cesaro et al. (2008) from two Italian potato fields are included. Red = Peruvian rhizosphere soil-derived sequences; blue = Peruvian root-derived sequences; green = Italian root-derived sequences; purple = Italian soil-derived sequences (PDF 255 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Senés-Guerrero, C., Torres-Cortés, G., Pfeiffer, S. et al. Potato-associated arbuscular mycorrhizal fungal communities in the Peruvian Andes. Mycorrhiza 24, 405–417 (2014). https://doi.org/10.1007/s00572-013-0549-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-013-0549-0

Keywords

  • Andes
  • Arbuscular mycorrhizal fungi
  • Community analysis
  • Roots and rhizosphere
  • Nuclear rDNA
  • Solanum tuberosum