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Potato field-inoculation in Ecuador with Rhizophagus irregularis: no impact on growth performance and associated arbuscular mycorrhizal fungal communities

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Abstract

A field trial was conducted in two localities of the Ecuadorian Andes to evaluate potato (Solanum tuberosum c.v. INIAP - Fripapa) response to inoculation with four commercial products containing the arbuscular mycorrhizal fungus (AMF) strain Rhizophagus irregularis DAOM 197198. In parallel, potato roots were analysed using 454 GS-FLX+ sequencing of c. 800 bp of the nuclear LSU rRNA gene to assess the associated AMF communities. To evaluate inoculation success, sequence reads of R. irregularis on the root samples were compared between inoculated and not inoculated plants by analysing the frequency of occurrence (FO) and relative read abundance (RA). None of the commercial products significantly increased potato yield. Instead, the AMF communities were dominated by an unknown Acaulospora sp. (Sp14) found at high FO and RA in both localities. Rhizophagus irregularis was found in most of the roots of both inoculated and not inoculated plants at both localities. However, its abundance was unexpectedly low indicating poor inoculum establishment. Clearly, many factors have to be taken in consideration for the successful application of AMF-based inoculants. For the Ecuadorian field trials, several causes may explain the lack or poor establishment of R. irregularis such as inoculation technique, agricultural practices, biotic and abiotic conditions and competition with native AMF species.

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References

  • APHA (1996) Standard methods for the examination of water and wastewater. American Public Health Association, Washington D.C

    Google Scholar 

  • Berger SA, Stamatakis A (2011) Aligning short reads to reference alignments and trees. Bioinformatics 27:2068–2075

    Article  PubMed  CAS  Google Scholar 

  • Berger SA, Krompass D, Stamatakis A (2011) Performance, accuracy, and web server for evolutionary placement of short sequence reads under maximum likelihood. Syst Biol 60:291–302

    Article  PubMed  PubMed Central  Google Scholar 

  • Berruti A, Borriello R, Orgiazzi A, Barbera AC, Lumini E, Bianciotto V (2014) Arbuscular mycorrhizal fungi and their value for ecosystem management. In: Grillo O (ed) Biodiversity: the dynamic balance of the planet. InTech, Rijeta, pp. 159–191

    Google Scholar 

  • Borriello R, Lumini E, Girlanda M, Bonfante P, Bianciotto V (2012) Effects of different management practices on arbuscular mycorrhizal fungal diversity in maize fields by a molecular approach. Biol Fertil Soils 48:911–922

    Article  Google Scholar 

  • Börstler B, Raab PA, Thiéry O, Morton JB, Redecker D (2008) Genetic diversity of the arbuscular mycorrhizal fungus Glomus intraradices as determined by mitochondrial large subunit rRNA gene sequences is considerably higher than previously expected. New Phytol 180:452–465

    Article  PubMed  CAS  Google Scholar 

  • Börstler B, Thiery O, Sýkorová Z, Berner A, Redecker D (2010) Diversity of mitochondrial large subunit rDNA haplotypes of Glomus intraradices in two agricultural field experiments and two semi-natural grasslands. Mol Ecol 19:1497–1511

    Article  PubMed  CAS  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Carreón-Abud Y, Vega-Fraga M, Gavito ME (2015) Interaction of arbuscular mycorrhizal inoculants and chicken manure in avocado rootstock production. J Soil Sci Plant Nutr 15:867–881

    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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cheng Y, Bai D, Sun L, Feldmann F, Feng G, Kapulnik Y, and Baar J (2008) Utilization of arbuscular mycorrhizal fungi during production of micropropagated potato Solanum tuberosum. In Mycorrhiza works: Proceedings of the International Symposium" Mycorrhiza for Plant Vitality" and the Joint Meeting for Working Groups 1–4 of COST Action 870, Hannover, Germany, 3–5 October, 2007, pp. 165–178.

  • Cuenca G, Cáceres A, González MG (2008) AM inoculation in tropical agriculture: field results. In: Varma A (ed) Mycorrhiza, 3rd edn. Springer, Berlin Heidelberg, pp. 403–417

    Chapter  Google Scholar 

  • Davies FT, Calderón CM, Huaman Z (2005) 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 

  • Dercon G, Govers G, Poesen J, Sánchez H, Rombaut K, Vandenbroeck E et al (2007) Animal-powered tillage erosion assessment in the southern Andes region of Ecuador. Geomorphology 87:4–15

    Article  Google Scholar 

  • Douds DD Jr, Nagahashi G, Reider C, Hepperly PR (2007) Inoculation with arbuscular mycorrhizal fungi increases the yield of potatoes in a high P soil. Biol Agric Hortic 25:67–78

    Article  Google Scholar 

  • Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461

    Article  PubMed  CAS  Google Scholar 

  • Fall F, Diouf DE, Fall D, Ndoye I, Ndlaye C, Kane A, Ba AM (2015) Effect of arbuscular mycorrhizal fungal inoculation on growth, and nutrient uptake of the two grass species, Leptochloa fusca (L.) Stapf and Sporobolus robustus Kunth, under greenhouse conditions. Afr J Biotechnol 14:2770–2776

    Article  CAS  Google Scholar 

  • Farmer MJ, Li X, Feng G, Zhao B, Chatagnier O, Gianinazzi S, Pearson V, van Tuinen D (2007) Molecular monitoring of field-inoculated AMF to evaluate persistence in sweet potato crops in China. Appl Soil Ecol 35:599–609

    Article  Google Scholar 

  • Formey D, Moles M, Haouy A, Savelli B, Bouchez O, Becard G, Roux C (2012) Comparative analysis of mitochondrial genomes of Rhizophagus Irregularis–syn. Glomus irregulare–reveals a polymorphism induced by variability generating elements. New Phytol 196:1217–1227

    Article  PubMed  CAS  Google Scholar 

  • Fox RL, Olson RA, Rhoades HF (1964) Evaluating the sulfur status of soils by plant and soil tests. Soil Sci Soc of Am. PRO 28:243–246

    Google Scholar 

  • Hawkes JG (1990) The potato. Evolution, biodiversity and genetic resources. Smithsonian Institution Press, Washington

    Google Scholar 

  • Herrera-Peraza RA, Hamel C, Fernández F, Ferrer RL, Furrazola E (2011) Soil–strain compatibility: the key to effective use of arbuscular mycorrhizal inoculants? Mycorrhiza 21:183–193

    Article  PubMed  Google Scholar 

  • Hijri M (2015) Analysis of a large dataset of mycorrhiza inoculation field trials on potato shows highly significant increases in yield. Mycorrhiza 26:209–214

    Article  PubMed  Google Scholar 

  • Hunter AH (1979) Suggested soil plant analytical techniques for tropical soils research program laboratories. Agroservices International, Orange City

    Google Scholar 

  • IJdo M, Cranenbrouck S, Declerck S (2011) Methods for large-scale production of AM fungi: past, present, and future. Mycorrhiza 21:1–16

    Article  PubMed  CAS  Google Scholar 

  • Jansa J, Erb A, Oberholzer HR, Šmilauer P, Egli S (2014) Soil and geography are more important determinants of indigenous arbuscular mycorrhizal communities than management practices in Swiss agricultural soils. Mol Ecol 23:2118–2135

    Article  PubMed  CAS  Google Scholar 

  • Kivlin SN, Hawkes CV, Treseder KK (2011) Global diversity and distribution of arbuscular mycorrhizal fungi. Soil Biol Biochem 43:2294–2303

    Article  CAS  Google Scholar 

  • Kohout P, Sudová R, Janoušková M, Čtvrtlíková M, Hejda M, Pánková H, Slvíková R, Štajerová K, Vosátka M, Sýkorová Z (2014) Comparison of commonly used primer sets for evaluating arbuscular mycorrhizal fungal communities: is there a universal solution? Soil Biol Biochem 68:482–493

    Article  CAS  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

    Article  PubMed  CAS  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 

  • Lu FC, Lee CY, and Wang CL (2015) The influence of arbuscular mycorrhizal fungi inoculation on yam (Dioscorea spp.) tuber weights and secondary metabolite content. Peer J. doi:10.7717/peerj.1266

  • Mathimaran N, Falquet L, Ineichen K, Picard C, Redecker D, Boller T, Wiemken A (2008) Microsatellites for disentangling underground networks: strain-specific identification of Glomus intraradices, an arbuscular mycorrhizal fungus. Fungal Genet Biol 45:812–817

    Article  PubMed  CAS  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 

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, et al. (2013) Vegan: Community Ecology Package. R package version 2.15–1.2013. http://cran.r-project.org/package=vegan. Accessed 10 May 2013

  • Olsen SR (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. USDA Circular Nr 939, US Gov. Print. Office, Washington

    Google Scholar 

  • Pellegrini F (2013) Evaluation of Integrated Pest Management (IPM) adoption in potato production using the Sustainable Livelihoods Approach. Dissertation, Swedish University of Agricultural Sciences

  • Pellegrino E, Turrini A, Gamper HA, Cafa G, Bonari E, Young JPW, Giovannetti M (2012) Establishment, persistence and effectiveness of arbuscular mycorrhizal fungal inoculants in the field revealed using molecular genetic tracing and measurement of yield components. New Phytol 194:810–822

    Article  PubMed  CAS  Google Scholar 

  • Peyret-Guzzon M, Stockinger H, Bouffaud ML, Farcy P, Wipf D, Redecker D (2016) Arbuscular mycorrhizal fungal communities and Rhizophagus Irregularis populations shift in response to short-term ploughing and fertilisation in a buffer strip. Mycorrhiza 26:33–46

    Article  PubMed  CAS  Google Scholar 

  • R Development Core Team (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3–900051–07-0. http://www.r-project.org

  • Rodriguez A, Sanders IR (2015) The role of community and population ecology in applying mycorrhizal fungi for improved food security. The ISME journal 9:1053–1061

    Article  PubMed  Google Scholar 

  • Sasvári Z, Hornok L, Posta K (2011) The community structure of arbuscular mycorrhizal fungi in roots of maize grown in a 50-year monoculture. Biol Fertil Soils 47:167–176

    Article  Google Scholar 

  • Schlaeppi K, Bender SF, Mascher F, Russo G, Patrignani A, Camenzind T et al (2016) High-resolution community profiling of arbuscular mycorrhizal fungi. New Phytol. doi:10.1111/nph.14070

    PubMed  Google Scholar 

  • Schüßler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeroomycota: phylogeny and evolution. Mycol Res 105:1413–1421

    Article  Google Scholar 

  • Schüßler A, Krüger C, Urgiles N (2016) Phylogenetically diverse AM fungi from Ecuador strongly improve seedling growth of native potential crop trees. Mycorrhiza 26:199–207

    Article  PubMed  Google Scholar 

  • Senés-Guerrero C, Schüßler A (2016) A conserved arbuscular mycorrhizal fungal core-species community colonizes potato roots in the Andes. Fungal Divers 77:317–333

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Sherwood S, Crissman C, and Cole D (2002) Pesticide exposure and poisonings in Ecuador: a call for action. Pesticides News-London-Pesticides Trust then Pesticide Action Network UK, 3–6

  • SINAGAP (2014) Sistema Nacional de Información del Ministerio de Agricultura, Ganadería, Acuacultura y Pesca del Ecuador. Boletín Situacional Papa. http://sinagap.agricultura.gob.ec/phocadownloadpap/cultivo/2014/kboletin-situacional-de-papa-2014-actualizado.pdf. Accessed 10 Oct 2016

  • Smith EE, Read JD (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, London

    Google Scholar 

  • Stockinger H, Walker C, Schüßler A (2009) Glomus intraradices DAOM 197198’, a model fungus in arbuscular mycorrhiza research, is not Glomus intraradices. New Phytol 183:1176–1187

    Article  PubMed  Google Scholar 

  • Struik PC (2007) Above-ground and below-ground plant development. In: Vreugdenhil D (ed) Potato biology and biotechnology: advances and perspectives, 1st edn. Elsevier, UK, pp. 219–236

    Chapter  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

    Article  PubMed  CAS  Google Scholar 

  • Sýkorová Z, Börstler B, Zvolenská S, Fehrer J, Gryndler M, Vosátka M, Redecker D (2012) Long-term tracing of Rhizophagus irregularis isolate BEG140 inoculated on Phalaris arundinacea in a coal mine spoil bank, using mitochondrial large subunit rDNA markers. Mycorrhiza 22:69–80

    Article  PubMed  CAS  Google Scholar 

  • Tambascio C, Covacevich F, Lobato MC, de Lasa C, Caldiz D, Dosio G, Andreu A (2014) The application of K phosphites to seed tubers enhanced emergence, early growth and mycorrhizal colonization in potato (Solanum tuberosum). AJPS 5:132–137

    Article  CAS  Google Scholar 

  • Tawaraya K, Hirose R, Wagatsuma T (2012) Inoculation of arbuscular mycorrhizal fungi can substantially reduce phosphate fertilizer application to Allium fistulosum L. and achieve marketable yield under field condition. Biol Fert. Soil 48:839–843

    Google Scholar 

  • Thiéry O (2010) Molecular markers from the mitochondrial genome of arbuscular mycorrhizal fungi (Glomeromycota): evolutionary dynamics and application. Dissertation, University of Basel

  • Trouvelot A, Kough JL, Gianinazzi-Pearson V (1986) Mesure du taux de mycorhization VA d’un système radiculaire. Recherche de méthodes d’estimation ayant une signification fonctionnelle. In Gianinazzi-Pearson V, Gianinazzi S (eds) Physiological and Genetical Aspects of Mycorrhizae. INRA Press, Paris, pp 217–221

  • Urgiles N, Loján P, Aguirre N, Blaschke H, Günter S, Stimm B, Kottke I (2009) Application of mycorrhizal roots improves growth of tropical tree seedlings in the nursery: a step towards reforestation with native species in the Andes of Ecuador. New Forest 38:229–239

    Article  Google Scholar 

  • Vályi K, Rillig MC, Hempel S (2015) Land-use intensity and host plant identity interactively shape communities of arbuscular mycorrhizal fungi in roots of grassland plants. New Phytol 205:1577–1586

    Article  PubMed  Google Scholar 

  • Velivelli SLS, Kromann P, Loján P, Rojas M, Franco J, Suarez JP, Prestwich BD (2015) Identification of mVOCs from Andean Rhizobacteria and field evaluation of bacterial and mycorrhizal inoculants on growth of potato in its Center of Origin. Microb Ecol 69:652–667

    Article  PubMed  CAS  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

    Article  PubMed  Google Scholar 

  • Vosátka M, Látr A, Gianinazzi S, Albrechtová J (2012) Development of arbuscular mycorrhizal biotechnology and industry: current achievements and bottlenecks. Symbiosis 58:29–37

    Article  CAS  Google Scholar 

  • Wang YY, Vestberg M, Walker C, Hurme T, Zhang X, Lindström K (2008) Diversity and infectivity of arbuscular mycorrhizal fungi in agricultural soils of the Sichuan Province of mainland China. Mycorrhiza 18:59–68

    Article  PubMed  Google Scholar 

  • Wehner J, Antunes PM, Powell JR, Caruso T, Rillig MC (2011) Indigenous arbuscular mycorrhizal fungal assemblages protect grassland host plants from pathogens. PLoS One 6(11):e27381

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • White PJ, Wheatley RE, Hammond JP, Zhang K (2007) Minerals, soils and roots. In: Vreugdenhil D (ed) Potato biology and biotechnology: advances and perspectives, 1st edn. Elsevier, UK, pp. 739–752

    Chapter  Google Scholar 

  • White JA, Tallaksen J, Charvat I (2008) The effects of arbuscular mycorrhizal fungal inoculation at a roadside prairie restoration site. Mycologia 100:6–11

    Article  PubMed  Google Scholar 

  • Wolfe BE, Mummey DL, Rillig MC, Klironomos JN (2007) Small-scale spatial heterogeneity of arbuscular mycorrhizal fungal abundance and community composition in a wetland plant community. Mycorrhiza 17:175–183

    Article  PubMed  Google Scholar 

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Acknowledgements

This work was supported by the European Community’s Seventh Framework Programme FP7/2007-2013 under grant agreement N° 227522, entitled “Valorizing Andean microbial diversity through sustainable intensification of potato-based farming systems”. Paul Loján was funded by SENESCYT (Secretaría Nacional de Educación Ciencia y Tecnología del Ecuador).

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Correspondence to Stéphane Declerck.

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Paul Loján and Carolina Senés-Guerrero equally contributed to the work

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Loján, P., Senés-Guerrero, C., Suárez, J.P. et al. Potato field-inoculation in Ecuador with Rhizophagus irregularis: no impact on growth performance and associated arbuscular mycorrhizal fungal communities. Symbiosis 73, 45–56 (2017). https://doi.org/10.1007/s13199-016-0471-2

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