, Volume 24, Issue 6, pp 405–417 | Cite as

Potato-associated arbuscular mycorrhizal fungal communities in the Peruvian Andes

  • Carolina Senés-Guerrero
  • Gloria Torres-Cortés
  • Stefan Pfeiffer
  • Mercy Rojas
  • Arthur SchüßlerEmail author
Original Paper


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.


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



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.

Supplementary material

572_2013_549_MOESM1_ESM.pdf (256 kb)
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)


  1. 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 75:4254–4263CrossRefGoogle Scholar
  2. 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 35:213–225CrossRefGoogle Scholar
  3. Bhattarai I, Mishra R (1984) Study on the vesicular–arbuscular mycorrhiza of three cultivars of potato (Solanum tuberosum). Plant Soil 79:299–303CrossRefGoogle Scholar
  4. 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 4:477–508CrossRefGoogle Scholar
  5. 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 320:37–77CrossRefGoogle Scholar
  6. Brush S, Kesseli R, Ortega R, Cisneros P, Zimmerer K, Quiros C (1995) Potato diversity in the Andean center of crop domestication. Conserv Biol 9:1189–1198CrossRefGoogle Scholar
  7. 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 74:5776–5783PubMedCentralPubMedCrossRefGoogle Scholar
  8. Chaurasia B, Pandey A, Palni LMS (2005) Distribution, colonization and diversity of arbuscular mycorrhizal fungi associated with central Himalayan rhododendrons. For Ecol Manage 207:315–324CrossRefGoogle Scholar
  9. 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 106:318–329CrossRefGoogle Scholar
  10. 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 40:381–385Google Scholar
  11. 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 78:103–115PubMedCrossRefGoogle Scholar
  12. 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 250:215–224CrossRefGoogle Scholar
  13. 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
  14. 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 15:137–144CrossRefGoogle Scholar
  15. FAO (2012) Food and Agriculture Organization of the United Nations, Land Resources. Accessed 07 July 2013.
  16. Feinstein LM, Sul WJ, Blackwood CB (2009) Assessment of bias associated with incomplete extraction of microbial DNA from soil. Appl Environ Microbiol 75:5428–5433PubMedCentralPubMedCrossRefGoogle Scholar
  17. 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 24:1345–1350CrossRefGoogle Scholar
  18. 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 PubMedGoogle Scholar
  19. 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 45:11–19Google Scholar
  20. 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 42:2211–2223CrossRefGoogle Scholar
  21. 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:e33819PubMedCentralPubMedCrossRefGoogle 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. 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 11:2669–2678PubMedCrossRefGoogle Scholar
  24. Husband R, Herre EA, Young JPW (2002b) Temporal variation in the arbuscular mycorrhizal communities colonising seedlings in a tropical forest. FEMS Microbiol Ecol 42:131–136PubMedCrossRefGoogle Scholar
  25. 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 30:3059–3066PubMedCentralPubMedCrossRefGoogle Scholar
  26. 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 22:5271–5277Google Scholar
  27. 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 183:212–223PubMedCrossRefGoogle Scholar
  28. 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
  29. 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 78:355–365PubMedCrossRefGoogle Scholar
  30. Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235PubMedCentralPubMedCrossRefGoogle Scholar
  31. Lozupone C, Hamady M, Knight R (2006) UniFrac—an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinformatics 7:371PubMedCentralPubMedCrossRefGoogle Scholar
  32. 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 55:705–713PubMedCrossRefGoogle Scholar
  33. 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 81:455–466PubMedCrossRefGoogle Scholar
  34. 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 101:771–782Google Scholar
  35. 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 1:23–30Google Scholar
  36. 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 98:286–294PubMedCrossRefGoogle Scholar
  37. 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 42:724–738CrossRefGoogle Scholar
  38. Öpik M, Moora M (2012) Missing nodes and links in mycorrhizal networks. New Phytol 194:304–306PubMedCrossRefGoogle Scholar
  39. 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 23:411–430PubMedCrossRefGoogle Scholar
  40. 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 276:4237–4245CrossRefGoogle Scholar
  41. Rahbek C (1995) The elevational gradient of species richness: a uniform pattern? Ecography 18:200–205CrossRefGoogle Scholar
  42. 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 23:515–531Google Scholar
  43. 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 135:255–266Google Scholar
  44. Sambrook J, Russell DW (2006) Purification of nucleic acids by extraction with phenol:chloroform. Cold Spring Harbor Protoc 2006: pdb.prot4455Google Scholar
  45. 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 22:449–460PubMedCrossRefGoogle Scholar
  46. Sanders NJ, Rahbek C (2012) The patterns and causes of elevational diversity gradients. Ecography 35:1–3CrossRefGoogle Scholar
  47. 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 40:576–583CrossRefGoogle Scholar
  48. 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 109:6241–6246PubMedCentralPubMedCrossRefGoogle Scholar
  49. 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 121:1791–1800CrossRefGoogle Scholar
  50. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, LondonGoogle Scholar
  51. 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 102:14694–14699PubMedCentralPubMedCrossRefGoogle Scholar
  52. Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 57:758–771PubMedCrossRefGoogle Scholar
  53. Stockinger H, Walker C, Schüßler A (2009) “Glomus intraradices DAOM197198”, a model fungus in arbuscular mycorrhiza research, is not Glomus intraradices. New Phytol 183:1176–1187PubMedCrossRefGoogle Scholar
  54. Stockinger H, Krüger M, Schüßler A (2010) DNA barcoding of arbuscular mycorrhizal fungi. New Phytol 187:461–474PubMedCrossRefGoogle 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. 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 21:323–330PubMedCrossRefGoogle Scholar
  57. Verbruggen E, Van der Heijden MGA, Rillig MC, Kiers ET (2013) Mycorrhizal fungal establishment in agricultural soils: factors determining inoculation success. New Phytol 197:1104–1109PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Carolina Senés-Guerrero
    • 1
  • Gloria Torres-Cortés
    • 1
  • Stefan Pfeiffer
    • 2
  • Mercy Rojas
    • 3
  • Arthur Schüßler
    • 1
    Email author
  1. 1.Department of Biology, GeneticsLudwig-Maximilians UniversityPlanegg-MartinsriedGermany
  2. 2.Department of Health and Environment, Bioresources UnitAIT Austrian Institute of Technology GmbHTullnAustria
  3. 3.International Potato Center (CIP)LimaPeru

Personalised recommendations