The aim of this paper was to test the use of dual microbial inoculation with mycorrhizal and saprotrophic fungi in onion cultivation to enhance yield while maintaining or improving the nutritional quality of onion bulbs. Treatments were two-factorial: (1) arbuscular mycorrhizal fungi (AMF): the mix corresponding to fungal part of commercial product Symbivit (Glomus etunicatum, G. microaggregatum, G. intraradices, G. claroideum, G. mosseae, and G. geosporum) (M1) or the single-fungus inoculum of G. intraradices BEG140 (M2) and (2) bark chips preinoculated with saprotrophic fungi (mix of Gymnopilus sp., Agrocybe praecox, and Marasmius androsaceus) (S). The growth response of onion was the highest for the M1 mix treatment, reaching nearly 100% increase in bulb fresh weight. The effectiveness of dual inoculation was proved by more than 50% increase. We observed a strong correlation (r = 0.83) between the growth response of onion bulbs and AM colonization. All inoculation treatments but the single-fungus one enhanced significantly the total antioxidant capacity of bulb biomass, was the highest values being found for M1, S + M1, and S + M2. We observed some induced enhancement of the contents of mineral elements in bulb tissue (Mg and K contents for the M2 and M2, S, and S + M2 treatments, resp.).

Department of Experimental Plant Biology Faculty of Science Charles University Prague 12844 Vinicna 5 Czech Republic

See more in PubMed

Roger-Estrade J, Anger C, Bertrand M, Richard G. Tillage and soil ecology: partners for sustainable agriculture. Soil and Tillage Research. 2010;111(1):33–40.

Lichtfouse E, Habib R, Meynard JM, Papy F. Agronomy for sustainable development. Agronomie. 2004;24(8):p. 445.

Lal R. Soils and sustainable agriculture. A review. Agronomy for Sustainable Development. 2008;28(1):57–64.

Gianinazzi S, Gollotte A, Binet MN, van Tuinen D, Redecker D, Wipf D. Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza. 2010;20(8):519–530. PubMed

Gianinazzi S, Vosátka M. Inoculum of arbuscular mycorrhizal fungi for production systems: science meets business. Canadian Journal of Botany. 2004;82(8):1264–1271.

Vosatka M, Albrechtova J. Theoretical aspects an practical uses of mycorrhizal technology in floriculture and horticulture. In: da Silva JAT, editor. Floriculture, Ornamental and Plant Biotechnology. Advances and Topical Issues. Vol. 5. Global Science Books Ltd; 2008. pp. 466–479.

Wang FY, Tong RJ, Shi ZY, Xu XF, He XH. Inoculations with Arbuscular mycorrhizal fungi increase vegetable yields and decrease phoxim concentrations in carrot and green onion and their soils. PLoS ONE. 2011;6(2, e16949) PubMed PMC

Oehl F, Sieverding E, Ineichen K, Mäder P, Boller T, Wiemken A. Impact of land use intensity on the species diversity of arbuscular mycorrhizal fungi in agroecosystems of Central Europe. Applied and Environmental Microbiology. 2003;69(5):2816–2824. PubMed PMC

Oehl F, Sieverding E, Mäder P, et al. Impact of long-term conventional and organic farming on the diversity of arbuscular mycorrhizal fungi. Oecologia. 2004;138(4):574–583. PubMed

Gryndler M, Vosátka M, Hršelová H, Catská V, Chvátalová I, Jansa J. Effect of dual inoculation with arbuscular mycorrhizal fungi and bacteria on growth and mineral nutrition of strawberry. Journal of Plant Nutrition. 2002;25(6):1341–1358.

Camprubi A, Calvet C, Estaun V. Growth enhancement of Citrus reshni after inoculation with Glomus intraradices and Trichoderma aureoviride and associated effects on microbial populations and enzyme activity in potting mixes. Plant and Soil. 1995;173(2):233–238.

Tchameni SN, Ngonkeu MEL, Begoude BAD, et al. Effect of Trichoderma asperellum and arbuscular mycorrhizal fungi on cacao growth and resistance against black pod disease. Crop Protection. 2011;30(10):1321–1327.

Bosch-Serra AD, Currah L. Agronomy of onions. In: Rabinowitch HD, Currah L, editors. Allium Crop Science: Recent Advances. Wallingford, UK: CAB International; 2002. pp. 187–232.

Galván GA, Parádi I, Burger K, et al. Molecular diversity of arbuscular mycorrhizal fungi in onion roots from organic and conventional farming systems in the Netherlands. Mycorrhiza. 2009;19(5):317–328. PubMed PMC

Phillips JM, Hayman DS. Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Transactions of the British Mycological Society. 1970;55:158–161.

Miean KH, Mohamed S. Flavonoid (myricetin, quercetin, kaempferol, luteolin, and apigenin) content of edible tropical plants. Journal of Agricultural and Food Chemistry. 2001;49(6):3106–3112. PubMed

Corzo-Martínez M, Corzo N, Villamiel M. Biological properties of onions and garlic. Trends in Food Science and Technology. 2007;18(12):609–625.

Park J, Kim J, Kim MK. Onion flesh and onion peel enhance antioxidant status in aged rats. Journal of Nutritional Science and Vitaminology. 2007;53(1):21–29. PubMed

Vazquez-Prieto MA, Miatello RM. Organosulfur compounds and cardiovascular disease. Molecular Aspects of Medicine. 2010;31(6):540–545. PubMed

Ceccarelli N, Curadi M, Martelloni L, Sbrana C, Picciarelli P, Giovannetti M. Mycorrhizal colonization impacts on phenolic content and antioxidant properties of artichoke leaves and flower heads two years after field transplant. Plant and Soil. 2010;335(1):311–323.

Montalba R, Arriagada C, Alvear M, Zúñiga GE. Effects of conventional and organic nitrogen fertilizers on soil microbial activity, mycorrhizal colonization, leaf antioxidant content, and Fusarium wilt in highbush blueberry (Vaccinium corymbosum L.) Scientia Horticulturae. 2010;125(4):775–778.

Benzie IFF, Strain JJ. The ferric reducing ability of plasma (FRAP) as a measure of ’antioxidant power’: the FRAP assay. Analytical Biochemistry. 1996;239(1):70–76. PubMed

Blatny P, Kvasnicka F, Loucka R, Safarova H. Determination of ammonium, calcium, magnesium, and potassium in silage by capillary isotachophoresis. Journal of Agricultural and Food Chemistry. 1997;45(9):3554–3558.

Arya SP, Mahajan M, Jain P. Non-spectrophotometric methods for the determination of Vitamin C. Analytica Chimica Acta. 2000;417(1):1–14.

Koske RE, Gemma JN. A modified procedure for staining roots to detect VA mycorrhizas. Mycological Research. 1989;92:486–505.

Giovannetti M, Mosse B. Evaluation of techniques for measuring vesicular-arbuscular mzcorrhiyal infection in roots. New Phytologist. 1980;84(3):489–500.

Plenchette C, Fortin JA, Furlan V. Growth responses of several plant species to mycorrhizae in a soil of moderate P-fertility—I. Mycorrhizal dependency under field conditions. Plant and Soil. 1983;70(2):199–209.

Hayman DS, Mosse B. Plant growth responses to vesicular-arbuscular mycorrhiza—I. Growth of endogone-inoculated plants in phosphate-deficient soils. New Phytologist. 1971;70(1):19–27.

Portas CAM. Development of root systems during the growth of some vegetable crops. Plant and Soil. 1973;39(3):507–518.

Charron G, Furlan V, Bernier-Cardou M, Doyon G. Response of onion plants to arbuscular mycorrhizae 1. Effects of inoculation method and phosphorus fertilization on biomass and bulb firmness. Mycorrhiza. 2001;11(4):187–197. PubMed

Galván GA, Kuyper TW, Burger K, et al. Genetic analysis of the interaction between Allium species and arbuscular mycorrhizal fungi. Theoretical and Applied Genetics. 2011;122(5):947–960. PubMed PMC

Shi Z, Wang F, Zhang C, Yang Z. Exploitation of phosphorus patches with different phosphorus enrichment by three arbuscular mycorrhizal fungi. Journal of Plant Nutrition. 2011;34(8):1096–1106.

Tu C, Booker FL, Watson DM, et al. Mycorrhizal mediation of plant N acquisition and residue decomposition: impact of mineral N inputs. Global Change Biology. 2006;12(5):793–803.

Nell M, Wawrosch C, Steinkellner S, et al. Root colonization by symbiotic arbuscular mycorrhizal fungi increases sesquiterpenic acid concentrations in Valeriana officinalis L. Planta Medica. 2010;76(4):393–398. PubMed

Hodge A, Campbell CD, Fitter AH. An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature. 2001;413(6853):297–299. PubMed

Leigh J, Fitter AH, Hodge A. Growth and symbiotic effectiveness of an arbuscular mycorrhizal fungus in organic matter in competition with soil bacteria. FEMS Microbiology Ecology. 2011;76(3):428–438. PubMed

Tiunov AV, Scheu S. Arbuscular mycorrhiza and Collembola interact in affecting community composition of saprotrophic microfungi. Oecologia. 2005;142(4):636–642. PubMed

Allison SD, LeBauer DS, Ofrecio MR, Reyes R, Ta AM, Tran TM. Low levels of nitrogen addition stimulate decomposition by boreal forest fungi. Soil Biology and Biochemistry. 2009;41(2):293–302.

Albertsen A, Ravnskov S, Green H, Jensen DF, Larsen J. Interactions between the external mycelium of the mycorrhizal fungus Glomus intraradices and other soil microorganisms as affected by organic matter. Soil Biology and Biochemistry. 2006;38(5):1008–1014.

Boddington CL, Dodd JC. The effect of agricultural practices on the development of indigenous arbuscular mycorrhizal fungi. II. Studies in experimental microcosms. Plant and Soil. 2000;218(1-2):145–157.

Ravnskov S, Jensen B, Knudsen IMB, et al. Soil inoculation with the biocontrol agent Clonostachys rosea and the mycorrhizal fungus Glomus intraradices results in mutual inhibition, plant growth promotion and alteration of soil microbial communities. Soil Biology and Biochemistry. 2006;38(12):3453–3462.

Johnson NC. Can fertilization of soil select less mutualistic mycorrhizae? Ecological Applications. 1993;3(4):749–757. PubMed

Sawers RJH, Gutjahr C, Paszkowski U. Cereal mycorrhiza: an ancient symbiosis in modern agriculture. Trends in Plant Science. 2008;13(2):93–97. PubMed

Wu QS, Zou YN. The effect of dual application of arbuscular mycorrhizal fungi and polyamines upon growth and nutrient uptake on trifoliate orange (Poncirus trifoliata) seedlings. Notulae Botanicae Horti Agrobotanici Cluj-Napoca. 2009;37(2):95–98.

Baslam M, Garmendia I, Goicoechea N. Arbuscular mycorrhizal fungi (AMF) improved growth and nutritional quality of greenhouse-grown Lettuce. Journal of Agricultural and Food Chemistry. 2011;59(10):5504–5515. PubMed

Arriagada C, Sampedro I, Garcia-Romera I, Ocampo J. Improvement of growth of Eucalyptus globulus and soil biological parameters by amendment with sewage sludge and inoculation with arbuscular mycorrhizal and saprobe fungi. Science of the Total Environment. 2009;407(17):4799–4806. PubMed

Perner H, Rohn S, Driemel G, et al. Effect of nitrogen species supply and mycorrhizal colonization on organosulfur and phenolic compounds in onions. Journal of Agricultural and Food Chemistry. 2008;56(10):3538–3545. PubMed

Pellegrino E, Bedini S, Avio L, Bonari E, Giovannetti M. Field inoculation effectiveness of native and exotic arbuscular mycorrhizal fungi in a Mediterranean agricultural soil. Soil Biology and Biochemistry. 2011;43(2):367–376.

Vosatka M. Influence of inoculation with arbuscular mycorrhizal fungi on the growth and mycorrhizal infection of transplanted onion. Agriculture, Ecosystems and Environment. 1995;53(2):151–159.

Vosatka M, Albrechtova J, Patten R. The international market development for mycorrhizal technology. In: Varma A, editor. Mycorrhiza. chapter 21. Springer; 2008. pp. 438–419.

The shaping of onion seedlings performance through substrate formulation and co-inoculation with beneficial microorganism consortia