[en] Naranjilla (Solanum quitoense) is a perennial shrub plant mainly cultivated in Ecuador, Colombia, and Central America where it represents an important cash crop. Current cultivation practices not only cause deforestation and large-scale soil degradation but also make plants highly susceptible to pests and diseases. The use of arbuscular mycorrhizal fungi (AMF) can offer a possibility to overcome these problems. AMF can act beneficially in various ways, for example by improving plant nutrition and growth, water relations, soil structure and stability and protection against biotic and abiotic stresses. In this study, the impact of AMF inoculation on growth and nutrition parameters of naranjilla has been assessed. For inoculation three European reference AMF strains (Rhizoglomus irregulare, Claroideoglomus claroideum, and Cetraspora helvetica) and soils originating from three differently managed naranjilla plantations in Ecuador (conventional, organic, and permaculture) have been used. This allowed for a comparison of the performance of exotic AMF strains (reference strains) versus native consortia contained in the three soils used as inocula. To study fungal communities present in the three soils, trap cultures have been established using naranjilla as host plant. The community structures of AMF and other fungi inhabiting the roots of trap cultured naranjilla were assessed using next generation sequencing (NGS) methods. The growth response experiment has shown that two of the three reference AMF strains, a mixture of the three and soil from a permaculture site led to significantly better acquisition of phosphorus (up to 104%) compared to uninoculated controls. These results suggest that the use of AMF strains and local soils as inoculants represent a valid approach to improve nutrient uptake efficiency of naranjilla and consequently to reduce inputs of mineral fertilizers in the cultivation process. Improved phosphorus acquisition after inoculation with permaculture soil might have been caused by a higher abundance of AMF and the presence of Piriformospora indica as revealed by NGS. A higher frequency of AMF and enhanced root colonization rates in the trap cultures supplemented with permaculture soil highlight the importance of diverse agricultural systems for soil quality and crop production.
Symanczik, Sarah; Department of Soil Sciences, Research Institute of Organic AgricultureFrick, Switzerland
Gisler, Michelle; Department of Soil Sciences, Research Institute of Organic AgricultureFrick, Switzerland ; Department of Environmental Sciences, University of BaselBasel, Switzerland
Thonar, Cécile ; Université de Liège - ULiège > Département GxABT > Plant Sciences ; Department of Soil Sciences, Research Institute of Organic AgricultureFrick, Switzerland
Schlaeppi, Klaus; Department of Agroecology and Environment, AgroscopeZürich, Switzerland
Van der Heijden, Marcel; Department of Agroecology and Environment, AgroscopeZürich, Switzerland
Kahmen, Ansgar; Department of Environmental Sciences, University of BaselBasel, Switzerland
Boller, Thomas; Department of Environmental Sciences, University of BaselBasel, Switzerland
Mäder, Paul; Department of Soil Sciences, Research Institute of Organic AgricultureFrick, Switzerland
Language :
English
Title :
Application of Mycorrhiza and Soil from a Permaculture System Improved Phosphorus Acquisition in Naranjilla.
SNF - Schweizerischer Nationalfonds zur Förderung der wissenschaftlichen Forschung [CH] Staatssekretariat für Bildung, Forschung und Innovation Horizon 2020 Framework Programme
Funding text :
We thank Hannes Gamper from ETH Z?rich for providing the two inocula of Ce. helvetica and Cl. claroideum for our experiments. We acknowledge Alain Held (Agroscope) and Giancarlo Russo and Andrea Patrignani (Functional Genomic Centre Zurich) for excellent support in library preparation and sequencing. We also thank Pepe Proa?io and David Sanchez (Ministerio de Agricultura Ganader?a Acuacultura y Pesca) for providing us with naranjilla seeds and soil samples, respectively, as well as Jesus und Victor Tepud from La Esperanza and naranjilla farmers from Carchi for sharing seeds, soils samples and valuable information.Projects of KS are supported by the Swiss State Secretariat for Education, Research and Innovation (Projects C14.0132, C15.0111), and the Swiss National Science Foundation (Nr. 31003A_165891). SS partially received funding from the European Community?s Seventh Framework Program 662 (FP7/2007?2013) under Grant Agreement No. 312117 (BIOFECTOR), the European Union?s Horizon 2020 research and innovation programme under grant agreement No. 635750 and from the Swiss State Secretary for Education, Research and Innovation (SERI) under contact number 635750.
Abd-Alla, M. H., Omar, S. A., and Karanxha, S. (2000). The impact of pesticides on arbuscular mycorrhizal and nitrogen-fixing symbioses in legumes. Appl. Soil Ecol. 14, 191–200. doi: 10.1016/S0929-1393(00)00056-1
Achatz, B., von Rüden, S., Andrade, D., Neumann, E., Pons-Kühnemann, J., Kogel, K.-H., et al. (2010). Root colonization by Piriformospora indica enhances grain yield in barley under diverse nutrient regimes by accelerating plant development. Plant Soil 333, 59–70. doi: 10.1007/s11104-010-0319-0
Acosta, Ó, Pérez, A. M., and Vaillant, F. (2009). Chemical characterization, antioxidant properties, and volatile constituents of naranjilla (Solanum quitoense Lam.) cultivated in Costa Rica. Arch. Latinoam. Nutr. 59, 88–94.
Amend, A. (2014). From dandruff to deep-sea vents: Malassezia-like fungi are ecologically hyper-diverse. PLoS Pathog. 10:e1004277. doi: 10.1371/journal. ppat.1004277
Antunes, P. M., Koch, A. M., Dunfield, K. E., Hart, M. M., Downing, A., Rillig, M. C., et al. (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. doi: 10.1007/s11104-008-9806-y
Augé, R. M. (2001). Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11, 3–42. doi: 10.1007/s005720100097
Azcón-Aguilar, C., and Barea, J. (1997). Arbuscular mycorrhizas and biological control of soil-borne plant pathogens–an overview of the mechanisms involved. Mycorrhiza 6, 457–464. doi: 10.1007/s005720050147
Bossuyt, H., Denef, K., Six, J., Frey, S., Merckx, R., and Paustian, K. (2001). Influence of microbial populations and residue quality on aggregate stability. Appl. Soil Ecol. 16, 195–208. doi: 10.1016/S0929-1393(00)00116-5
Brummitt, N., and Lughadha, E. N. (2003). Biodiversity: where’s hot and where’s not. Conserv. Biol. 17, 1442–1448. doi: 10.1046/j.1523-1739.2003.02344.x
Brussaard, L., De Ruiter, P. C., and Brown, G. G. (2007). Soil biodiversity for agricultural sustainability. Agric. Ecosyst. Environ. 121, 233–244. doi: 10.1016/j. agee.2006.12.013
Bünemann, E., Schwenke, G., and Van Zwieten, L. (2006). Impact of agricultural inputs on soil organisms—a review. Soil Res. 44, 379–406. doi: 10.1071/SR05125
Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., et al. (2010). QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335–336. doi: 10.1038/nmeth. f.303
Casierra-Posada, F., Peña-Olmos, J., Peñaloza, J., and Roveda, G. (2013). Influence of shading and mycorrhizae on growth of lulo plants (Solanum quitoense Lam.). Rev. UDCA Actual. Divulg. Cien. 16, 61–70.
Chiocchio, V., Venedikian, N., Martinez, A. E., Ana Menendez, A. M., Ocampo, J. A., and Godeas, A. (2010). Effect of the fungicide benomyl on spore germination and hyphal length of the arbuscular mycorrhizal fungus Glomus mosseae. Int. Microbiol. 3, 173–175.
Collazos, H. H., Figueroa, P., Jordan, A., Patiño, H., and Sieverding, E. (1986). Estudio preliminar sobre micorriza versículo–Arbuscular (MVA) en lulo (Solanum quitoense Lam). Acta Agron. 36, 34–46.
Corkidi, L., Allen, E. B., Merhaut, D., Allen, M. F., Downer, J., Bohn, J., et al. (2004). Assessing the infectivity of commercial mycorrhizal inoculants in plant nursery conditions. J. Environ. Hortic. 22, 149–154.
De Vries, F. T., Thébault, E., Liiri, M., Birkhofer, K., Tsiafouli, M. A., Bjørnlund, L., et al. (2013). Soil food web properties explain ecosystem services across European land use systems. Proc. Natl. Acad. Sci. U.S.A. 110, 14296–14301. doi: 10.1073/pnas.1305198110
Edgar, R. C. (2013). UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10, 996–998. doi: 10.1038/nmeth.2604
Fakhro, A., Andrade-Linares, D. R., von Bargen, S., Bandte, M., Büttner, C., Grosch, R., et al. (2010). Impact of Piriformospora indica on tomato growth and on interaction with fungal and viral pathogens. Mycorrhiza 20, 191–200. doi: 10.1007/s00572-009-0279-5
Gamborg, O. L., and Wetter, L. (1975). Plant Tissue Culture Methods. Saskatoon, SK: National Research Council of Canada, Prairie Regional Laboratory.
Gianinazzi, S., Schüepp, H., Barea, J. M., and Haselwandter, K. (2012). Mycorrhizal Technology in Agriculture: from Genes to Bioproducts. Basel: Birkhäuser.
Gonzalez, O., and Osorio, W. (2015). Determination of mycorrhizal dependency of lulo [Determinación de la dependencia micorrizal del lulo]. Acta Biol. Colomb. 13, 163–174.
Gosling, P., Hodge, A., Goodlass, G., and Bending, G. D. (2006). Arbuscular mycorrhizal fungi and organic farming. Agric. Ecosyst. Environ. 113, 17–35. doi: 10.1016/j.agee.2005.09.009
Green, M. J., Thompson, D. A., and MacKenzie, D. J. (1999). Easy and efficient DNA extraction from woody plants for the detection of phytoplasmas by polymerase chain reaction. Plant Dis. 83, 482–485. doi: 10.1094/PDIS.1999.83. 5.482
Heiser, C. B. (1985). Ethnobotany of the naranjilla (Solanum quitoense) and its relatives. Econ. Bot. 39, 4–11. doi: 10.1007/BF02861168
Hildebrandt, U., Regvar, M., and Bothe, H. (2007). Arbuscular mycorrhiza and heavy metal tolerance. Phytochemistry 68, 139–146. doi: 10.1016/j.phytochem. 2006.09.023
Jansa, J., Wiemken, A., and Frossard, E. (2006). The effects of agricultural practices on arbuscular mycorrhizal fungi. Geol. Soc. 266, 89–115. doi: 10.1144/GSL.SP. 2006.266.01.08
Johnson, D., Vandenkoornhuyse, P. J., Leake, J. R., Gilbert, L., Booth, R. E., Grime, J. P., et al. (2004). Plant communities affect arbuscular mycorrhizal fungal diversity and community composition in grassland microcosms. New Phytol. 161, 503–515. doi: 10.1046/j.1469-8137.2003.00938.x
Kalia, A., and Gosal, S. (2011). Effect of pesticide application on soil microorganisms. Arch. Agron. Soil Sci. 57, 569–596. doi: 10.1080/0365034 1003787582
Koch, A. M., Antunes, P. M., Barto, E. K., Cipollini, D., Mummey, D. L., and Klironomos, J. N. (2011). The effects of arbuscular mycorrhizal (AM) fungal and garlic mustard introductions on native AM fungal diversity. Biol. Invasions 13, 1627–1639. doi: 10.1007/s10530-010-9920-7
Köhl, L., Oehl, F., and van der Heijden, M. G. (2014). Agricultural practices indirectly influence plant productivity and ecosystem services through effects on soil biota. Ecol. Appl. 24, 1842–1853. doi: 10.1890/13-1821.1
Koide, R., and Elliott, G. (1989). Cost, benefit and efficiency of the vesicular-arbuscular mycorrhizal symbiosis. Funct. Ecol. 3, 252–255.
Kõljalg, U., Nilsson, R. H., Abarenkov, K., Tedersoo, L., Taylor, A. F., Bahram, M., et al. (2013). Towards a unified paradigm for sequence-based identification of fungi. Mol. Ecol. 22, 5271–5277. doi: 10.1111/mec.12481
Krüger, C., Kohout, P., Janouskova, M., Püschel, D., Frouz, J., and Rydlova, J. (2017). Plant communities rather than soil properties structure arbuscular mycorrhizal fungal communities along primary succession on a mine spoil. Front. Microbiol. 8:719. doi: 10.3389/fmicb.2017.00719
Kumar, M., Sharma, R., Jogawat, A., Singh, P., Dua, M., Gill, S. S., et al. (2012). “Piriformospora indica, a root endophytic fungus, enhances abiotic stress tolerance of the host plant,” in Improving Crop Resistance to Abiotic Stress, Vol. 1 and 2, eds N. Tuteja, S. S. Gill, A. F. Tiburcio, and R. Tuteja (Weinheim: Wiley), 543–558. doi: 10.1016/j.jprot.2013.09.017
Kurle, J. E., and Pfleger, F. (1994). “The effects of cultural practices and pesticides on VAM fungi,” in Mycorrhizae and Plant Health, eds F. L. Pfleger and R. G. Linderman (Saint Paul, MN: APS Press), 101–131.
Leifheit, E. F., Veresoglou, S. D., Lehmann, A., Morris, E. K., and Rillig, M. C. (2014). Multiple factors influence the role of arbuscular mycorrhizal fungi in soil aggregation—a meta-analysis. Plant Soil 374, 523–537. doi: 10.1007/s11104-013-1899-2
Lovelock, C. E., and Ewel, J. J. (2005). Links between tree species, symbiotic fungal diversity and ecosystem functioning in simplified tropical ecosystems. New Phytol. 167, 219–228. doi: 10.1111/j.1469-8137.2005.01402.x
Mäder, P., Edenhofer, S., Boller, T., Wiemken, A., and Niggli, U. (2000). Arbuscular mycorrhizae in a long-term field trial comparing low-input (organic, biological) and high-input (conventional) farming systems in a crop rotation. Biol. Fertil. Soils 31, 150–156. doi: 10.1007/s003740050638
Mainville, N., Webb, J., Lucotte, M., Davidson, R., Betancourt, O., Cueva, E., et al. (2006). Decrease of soil fertility and release of mercury following deforestation in the Andean Amazon, Napo River Valley, Ecuador. Sci. Total Environ. 368, 88–98. doi: 10.1016/j.scitotenv.2005.09.064
Maltz, M. R., and Treseder, K. K. (2015). Sources of inocula influence mycorrhizal colonization of plants in restoration projects: a meta-analysis. Restor. Ecol. 23, 625–634. doi: 10.1111/rec.12231
McGonigle, T., Miller, M., Evans, D., Fairchild, G., and Swan, J. (1990). A new method which gives an objective measure of colonization of roots by vesicular— arbuscular mycorrhizal fungi. New Phytol. 115, 495–501. doi: 10.1111/j.1469-8137.1990.tb00476.x
McMurdie, P. J., and Holmes, S. (2013). Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8:e61217. doi: 10.1371/journal.pone.0061217
Mummey, D. L., Antunes, P. M., and Rillig, M. C. (2009). Arbuscular mycorrhizal fungi pre-inoculant identity determines community composition in roots. Soil Biol. Biochem. 41, 1173–1179. doi: 10.1016/j.soilbio.2009.02.027
Murphy, J., and Riley, J. P. (1962). A modified single solution method for the determination of phosphate in natural waters. Anal. Chim. Acta 27, 31–36. doi: 10.1016/S0003-2670(00)88444-5
Oehl, F., Sieverding, E., Ineichen, K., Mäder, P., Boller, T., and Wiemken, A. (2003). Impact of land use intensity on the species diversity of arbuscular mycorrhizal fungi in agroecosystems of Central Europe. Appl. Environ. Microbiol. 69, 2816–2824. doi: 10.1128/AEM.69.5.2816-2824.2003
Oehl, F., Sieverding, E., Mäder, P., Dubois, D., Ineichen, K., Boller, T., et al. (2004). Impact of long-term conventional and organic farming on the diversity of arbuscular mycorrhizal fungi. Oecologia 138, 574–583. doi: 10.1007/s00442-003-1458-2
Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., O’Hara, R. B., et al. (2015). vegan: Community Ecology Package Version 2.4-3. Available at: https://CRAN.R-project.org/package=vegan
Parniske, M. (2008). Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat. Rev. Microbiol. 6, 763–775. doi: 10.1038/nrmicro1987
Phillips, J. M., and Hayman, D. (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. doi: 10.1016/S0007-1536(70)80110-3
Porcel, R., Aroca, R., and Ruiz-Lozano, J. M. (2012). Salinity stress alleviation using arbuscular mycorrhizal fungi. A review. Agron. Sustain. Dev. 32, 181–200. doi: 10.1007/s13593-011-0029-x
Pozo, M. J., Jung, S. C., López-Ráez, J. A., and Azcón-Aguilar, C. (2010). “Impact of arbuscular mycorrhizal symbiosis on plant response to biotic stress: the role of plant defence mechanisms,” in Arbuscular Mycorrhizas: Physiology and Function, eds H. Koltai and Y. Kapulnik (Berlin: Springer), 193–207.
R Core Team (2014). R: A Language and Environment for Statistical Computing (Version 3.0.2). Vienna: R Foundation for Statistical Computing.
Requena, N., Perez-Solis, E., Azcón-Aguilar, C., Jeffries, P., and Barea, J.-M. (2001). Management of indigenous plant-microbe symbioses aids restoration of desertified ecosystems. Appl. Environ. Microbiol. 67, 495–498. doi: 10.1128/AEM.67.2.495-498.2001
Revelo, J., Viteri, P., Vásquez, W., León, J., and Gallegos, P. (2010). Manual del Cultivo Ecológico de la Naranjilla. Quito: INIAP.
Rowe, H. I., Brown, C. S., and Claassen, V. P. (2007). Comparisons of mycorrhizal responsiveness with field soil and commercial inoculum for six native montane species and Bromus tectorum. Restor. Ecol. 15, 44–52. doi: 10.1111/j.1526-100X. 2006.00188.x
Roy, M., Watthana, S., Stier, A., Richard, F., Vessabutr, S., and Selosse, M.-A. (2009). Two mycoheterotrophic orchids from Thailand tropical dipterocarpacean forests associate with a broad diversity of ectomycorrhizal fungi. BMC Biol. 7:51. doi: 10.1186/1741-7007-7-51
Schlaeppi, K., Bender, S. F., Mascher, F., Russo, G., Patrignani, A., Camenzind, T., et al. (2016). High-resolution community profiling of arbuscular mycorrhizal fungi. New Phytol. 212, 780–791. doi: 10.1111/nph.14070
Schwartz, M. W., Hoeksema, J. D., Gehring, C. A., Johnson, N. C., Klironomos, J. N., Abbott, L. K., et al. (2006). The promise and the potential consequences of the global transport of mycorrhizal fungal inoculum. Ecol. Lett. 9, 501–515. doi: 10.1111/j.1461-0248.2006.00910.x
Smith, S. E., and Read, D. J. (2010). Mycorrhizal Symbiosis. San Diego, CA: Academic press.
Sowell, A., and Shively, G. (2012). Economic and environmental impacts of grafted naranjilla. For. Trees Livelihoods 21, 30–43. doi: 10.1080/14728028.2012.669133
Sukarno, N., Smith, S., and Scott, E. (1993). The effect of fungicides on vesicular– arbuscular mycorrhizal symbiosis. New Phytol. 125, 139–147. doi: 10.1111/j. 1469-8137.1993.tb03872.x
Sun, C., Johnson, J. M., Cai, D., Sherameti, I., Oelmüller, R., and Lou, B. (2010). Piriformospora indica confers drought tolerance in Chinese cabbage leaves by stimulating antioxidant enzymes, the expression of drought-related genes and the plastid-localized CAS protein. J. Plant Physiol. 167, 1009–1017. doi: 10.1016/j.jplph.2010.02.013
Symanczik, S., Courty, P.-E., Boller, T., Wiemken, A., and Al-Yahya’ei, M. N. (2015). Impact of water regimes on an experimental community of four desert arbuscular mycorrhizal fungal (AMF) species, as affected by the introduction of a non-native AMF species. Mycorrhiza 25, 639–647. doi: 10.1007/s00572-015-0638-3
Urgiles, N., Strauß, A., Loján, P., and Schüßler, A. (2014). Cultured arbuscular mycorrhizal fungi and native soil inocula improve seedling development of two pioneer trees in the Andean region. New For. 45, 859–874. doi: 10.1007/s11056-014-9442-8
Van der Heijden, M. G., Klironomos, J. N., Ursic, M., and Moutoglis, P. (1998). Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396, 69–72. doi: 10.1038/23932
Van der Heijden, M. G. A., Bardgett, R. D., and Van Straalen, N. M. (2008). The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol. Lett. 11, 296–310. doi: 10.1111/j.1461-0248.2007. 01139.x
Varma, A., Bakshi, M., Lou, B., Hartmann, A., and Oelmueller, R. (2012). Piriformospora indica: a novel plant growth-promoting mycorrhizal fungus. Agric. Res. 1, 117–131. doi: 10.1007/s40003-012-0019-5
Verbruggen, E., Röling, W. F., Gamper, H. A., Kowalchuk, G. A., Verhoef, H. A., and van der Heijden, M. G. (2010). Positive effects of organic farming on belowground mutualists: large-scale comparison of mycorrhizal fungal communities in agricultural soils. New Phytol. 186, 968–979. doi: 10.1111/j.1469-8137.2010. 03230.x
Wagg, C., Bender, S. F., Widmer, F., and van der Heijden, M. G. (2014). Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proc. Natl. Acad. Sci. U.S.A. 111, 5266–5270. doi: 10.1073/pnas.1320054111
Yadav, V., Kumar, M., Deep, D. K., Kumar, H., Sharma, R., Tripathi, T., et al. (2010). A phosphate transporter from the root endophytic fungus Piriformospora indica plays a role in phosphate transport to the host plant. J. Biol. Chem. 285, 26532–26544. doi: 10.1074/jbc.M110.111021
