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Effect of arbuscular mycorrhizal fungi on growth and on micronutrient and macronutrient uptake and allocation in olive plantlets growing under high total Mn levels

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Abstract

The reported work was designed to increase knowledge about the role of arbuscular mycorrhizal fungi (AMF) on the phytoavailability and allocation of some of the principal macroelements and microelements in young potted olive plants growing in a soil presenting high levels of manganese (Mn), taken from an experimental olive field. A greenhouse trial was performed using self-rooted cuttings of Ascolana tenera, Nocellara del Belice and Carolea cultivars inoculated or not with two mycorrhizal inocula (commercial vs native). Molecular characterization of the indigenous AMF indicated that the species found in the experimental soil were different from those present in the commercial inoculum. The important incidence of AMF on P uptake was confirmed with generally double the concentration in mycorrhizal olive plants as compared to non-mycorrhizal controls, irrespective of genotype and inocula. Furthermore, apart from promoting plant growth (from 1.7- to 5-fold), the symbiosis reduced Mn concentrations from 43 to 83 %. The observed differences depended on the cultivar and the inoculum, with native AMF being more effective probably as a result of their adaptation to the experimental soil. No clear direct relationship was found between AMF inoculation and other elements analysed.

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References

  • Abo-Ghalia HH, Khalafallah AA (2008) Responses of wheat plants associated with arbuscular mycorrhizal fungi to short-term water stress followed by recovery at three growth stages. J Appl Sci Res 4:570–580

    CAS  Google Scholar 

  • Alam S, Akiha F, Kamei S, Huq S, Kawai S (2005) Mechanism of potassium alleviation of manganese phytotoxicity in barley. J Plant Nutr 28:889–901

    Article  CAS  Google Scholar 

  • Alam S, Kodama R, Akiha F, Kamei S, Kawai S (2006) Alleviation of manganese phytotoxicity in barley with calcium. J Plant Nutr 29:59–74

    Article  CAS  Google Scholar 

  • Allen JW, Shachar-Hill Y (2009) Sulfur transfer through an arbuscular mycorrhiza. Plant Physiol 149:549–560

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Angelone M, Bini C (1992) Trace elements concentrations in soils and plants of Western Europe. In: Adriano DC (ed) Biogeochemistry of trace metals. Lewis Publishers, Boca Raton, pp 19–60

    Google Scholar 

  • Arines J, Porto ME, Vilarino A (1992) Effect of manganese on vesicular-arbuscular mycorrhizal development in red clover plants and on soil Mn-oxidizing bacteria. Mycorrhiza 1:127–131

    Article  CAS  Google Scholar 

  • Bedini S, Pellegrino E, Argese E, Giovannetti M (2004) Miglioramento del suolo e biostabilizzazione di metalli pesanti mediati da glomalina. Atti del XIV Congresso della Società Italiana di Ecologia. Siena, 4-6 Ottobre 2004. http://www.xivcongresso.societaitalianaecologia.org/articles/

  • Bennett AE, Alers-Garcia J, Bever JD (2006) Three-way interactions among mutualistic mycorrhizal fungi, plants, and plant enemies: hypotheses and synthesis. Am Nat 167:141–152

    Article  PubMed  Google Scholar 

  • Binet MN, Lemoine MC, Martin C, Chambon C, Gianinazzi S (2007) Micropropagation of olive (Olea europaea L.) and application of mycorrhiza to improve plantlet establishment. In Vitro Cell Dev Biol-Plant 43:473–478

    Article  CAS  Google Scholar 

  • Bini C, Dall’Oglio M, Ferretti O, Gragnani R (1998) Background levels of microelements in soils of Italy. Environ Geochem Health 10:63–69

    Article  Google Scholar 

  • Bonfante P, Genre A (2008) Plants and arbuscular mycorrhizal fungi: an evolutionary-developmental perspective. Trends Plant Sci 13:492–498

    Article  CAS  PubMed  Google Scholar 

  • Briccoli Bati C, Santilli E, Varlaro ME, Alessandrino M (2009) Effects of a commercial arbuscular mycorrhizal fungi inoculum on vegetative growth of three young olive cultivars. In XXXIII CIOSTA - CIGR V Conference 2009, Reggio Calabria (Italy) Technology and management to ensure sustainable agriculture, agro-systems, forestry and safety. pp. 2015-2019

  • Buchanan BB, Gruissem W, Jones RL (2000) Biochemistry and molecular biology of plants. Am Soc Plant Physiol. Rockville, Maryland, p 1367

  • Bücking H, Shachar-Hill Y (2005) Phosphate uptake, transport and transfer by the arbuscular mycorrhizal fungus Glomus intraradices is stimulated by increased carbohydrate availability. New Phytol 165:899–911

    Article  PubMed  Google Scholar 

  • Calvente R, Cano C, Ferrol N, Azcón-Aguilar C, Barea JM (2004) Analysing natural diversity of arbuscular mycorrhizal fungi in olive tree (Olea europaea L.) plantations and assessment of the effectiveness of native fungal isolates as inoculants for commercial cultivars of olive plantlets. Appl Soil Ecol 26:11–19

    Article  Google Scholar 

  • Castillo P, Nico AI, Azcón-Aguilar C et al (2006) Protection of olive planting stocks against parasitism of root-knot nematodes by arbuscular mycorrhizal fungi. Plant Pathol 55:705–713

    Article  Google Scholar 

  • Chatzistathis T, Orfanoudakis M, Alifragis D, Therios I (2013) Colonization of Greek olive cultivars’ root system by arbuscular mycorrhiza fungus: root morphology, growth, and mineral nutrition of olive plants. Sci Agric 70:185–194

    Article  CAS  Google Scholar 

  • Citernesi AS, Vitagliano C, Giovannetti M (1998) Plant growth and root systems morphology of Olea europaea L. rooted cuttings as influenced by arbuscular mycorrhizas. J Hortic Sci Biotechnol 73:647–654

    Google Scholar 

  • Cobbett CS, Goldsborough PB (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182

    Article  CAS  PubMed  Google Scholar 

  • Cozzolino V, Di Meo V, Piccolo A (2013) Impact of arbuscular mycorrhizal fungi applications on maize production and soil phosphorus availability. J Geochem Explor 129:40–44

    Article  CAS  Google Scholar 

  • Dag A, Yermiyahu U, Ben-Gal A, Zipori I, Kapulnik Y (2009) Nursery and post-transplant field response of olive trees to arbuscular mycorrhizal fungi in an arid region. Crop Pasture Sci 60:427–433

    Article  Google Scholar 

  • de Rougement M (2007) Les mycorhizes et l’olivier: Effet sur le développement des plants en pépinière et en verger. Journées méditerranéennes de l’olivier, Meknès, 22-26 octobre 2007: 2-7

  • Dučić T, Thieme J, Polle A (2012) Phosphorus compartmentalization on the cellular level of Douglas fir root as affected by Mn toxicity: a synchrotron-based FTIR approach. Spectrosc Int J 27:265–272

    Article  Google Scholar 

  • Enami I, Okumura A, Nagao R et al (2008) Structures and functions of the extrinsic proteins of photosystem II from different species. Photosynth Res 98:349–363

    Article  CAS  PubMed  Google Scholar 

  • Entry JA, Rygiewicz PT, Watrud LS, Donnelly PK (2002) Influence of adverse soil conditions on the formation and function of arbuscular mycorrhizas. Adv Environ Res 7:123–138

    Article  CAS  Google Scholar 

  • Estaún V, Camprubí A, Calvet C, Pinochet J (2003) Nursery and field response of olive trees inoculated with two arbuscular mycorrhizal fungi, Glomus intraradices and Glomus mosseae. J Am Soc Hortic Sci 28:767–775

    Google Scholar 

  • Farzaneh M, Vierheilig H, Lössl A, Kaul HP (2011) Arbuscular mycorrhiza enhances nutrient uptake in chickpea. Plant Soil Environ 57:465–470

    CAS  Google Scholar 

  • Gadd GM (1993) Interactions of fungi with toxic metals. New Phytol 124:25–60

    Article  CAS  Google Scholar 

  • Galli U, Schuepp H, Brunold C (1995) Thiol of Cu-treated maize plants inoculated with the arbuscular mycorrhizal fungus Glomus intraradices. Physiol Plant 94:247–253

    Article  CAS  Google Scholar 

  • Gemma JN, Koske RE, Habte M (2002) Mycorrhizal dependency of some endemic and endangered Hawaiian plant species. Am J Bot 89:337–345

    Article  CAS  PubMed  Google Scholar 

  • Gerdemann JW (1975) Vesicular-arbuscular mycorrhizae. In: Torrey JG, Clarkson DT (eds) The development and function of root. Academic Press, New York, pp 575–591

    Google Scholar 

  • Goss MJ, Carvalho MJ, Cosimini V, Fearnhead ML (1992) An approach to the identification of potentially toxic concentrations of manganese in soils. Soil Use Manag 8:40–44

    Article  Google Scholar 

  • Govindarajulu M, Pfeffer PE, Jin HR et al (2005) Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435:819–823

    Article  CAS  PubMed  Google Scholar 

  • Graham JH (2001) What do root pathogens see in mycorrhizas? New Phytol 149:357–359

    Article  Google Scholar 

  • Graham RD, Reed ML (1991) Carbonic anhydrase and the regulation of photosynthesis. Nat New Biol 231:81–83

    Article  Google Scholar 

  • Hayman DS, Barea JM, Azcon-Aguilar R (1976) Vesicular-arbuscular mycorrhiza in Southern Spain: its distribution in crops growing in soil of different fertility. Phytopathol Mediterr 15:1–6

    Google Scholar 

  • Horst WJ (1988) The physiology of manganese toxicity. In: Graham RD, Hannam RJ, Uren NC (eds) Manganese in soils and plants. Kluwer Academic Publishers, Dordrecht, pp 175–188

    Chapter  Google Scholar 

  • Jamal A, Ayub N, Usman M, Khan AG (2002) Arbuscular mycorrhizal fungi enhance zinc and nickel uptake from contaminated soil by soybean and lentil. Int J Phytoremediat 4:205–221

    Article  CAS  Google Scholar 

  • Jentschke G, Godbold DL (2000) Metal toxicity and ectomycorrhizas. Physiol Plant 109:107–116

    Article  CAS  Google Scholar 

  • Jin H, Pfeffer PE, Douds DD et al (2005) The uptake, metabolism, transport and transfer of nitrogen in an arbuscular mycorrhizal symbiosis. New Phytol 168:687–696

    Article  CAS  PubMed  Google Scholar 

  • Kabata-Pendias A (2001) Trace elements in soils and plants, 3rd edn. CRC Press, Boca Raton, FL, pp 413

  • Kapoor A, Viraraghavan T (1995) Fungal biosorption—an alternative treatment option for heavy metal bearing waste water: a review. Bioresourc Technol 53:195–206

    CAS  Google Scholar 

  • Khan AG (2005) Role of soil microbes in the rhizospheres of plants growing on trace element contaminated soils in phytoremediation. J Trace Elem Med Biol 18:355–364

    Article  CAS  PubMed  Google Scholar 

  • Khan HR, McDonald GK, Rengel Z (2004) Zinc fertilization and water stress affects plant water relations, stomatal conductance and osmotic adjustment in chickpea (Cicer arientinum L.). Plant Soil 267:271–284

    Article  CAS  Google Scholar 

  • Kiers ET, Duhamel M, Beesetty Y et al (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880–882

    Article  CAS  PubMed  Google Scholar 

  • Kothari SK, Marschner H, Römheld V (1991) Effect of a vesicular-arbuscular mycorrhizal fungus and rhizosphere micro-organisms on manganese reduction in the rhizosphere and manganese concentrations in maize (Zea mays L.). New Phytol 117:649–655

    Article  CAS  Google Scholar 

  • LeBot J, Goss MJ, Carvalho GPR, van Beusichem ML, Kirby EA (1990) The significance of magnesium to manganese ratio in plant tissues for growth and alleviation of manganese toxicity in tomato (Lycopersicon esculentum) and wheat (Triticum sativum) plants. Plant Soil 124:205–210

    Article  CAS  Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382

    Article  CAS  Google Scholar 

  • Lichtenthaler HK, Buschmann C (2001) Chlorophylls and carotenoids—measurement and characterisation by UV-VIS. In: Current protocols in food analytical chemistry, J Wiley & Sons, Madison F4.3.1-F4.3.8

  • Linderman RG (1988) Mycorrhizal interactions with the rhizosphere microflora—the mycorrhizosphere effect. Phytopathology 78:366–371

    Google Scholar 

  • Mathur N, Vyas A (1995) Influence of VA mycorrhizae on net photosynthesis and transpiration on Ziziphus mauritiana. J Plant Physiol 147:328–330

    Article  CAS  Google Scholar 

  • McBride MB (1994) Environmental chemistry of soils, 1st edn. Oxford University Press, New York, p 406

  • Meddad-Hamza A, Beddiar A, Gollotte A et al (2010) Arbuscular mycorrhizal fungi improve the growth of olive trees and their resistance to transplantation stress. Afr J Biotechnol 9:1159–1167

    Google Scholar 

  • Mekahlia MN, Beddiar A, Chenchouni H (2013) Mycorrhizal dependency in the olive tree (Olea europaea) across a xeric climatic gradient. Adv Environ Biol 7:2166–2174

    Google Scholar 

  • Newman SE, Davies FT Jr (1988) High root-zone temperatures, mycorrhizal fungi, and water relations and root hydraulic conductivity of selected container grown woody plants. J Am Soc Hortic Sci 113:138–145

    Google Scholar 

  • Nogueira MA, Cardoso EJBN (2003) Mycorrhizal effectiveness and manganese toxicity in soybean as affected by soil type and endophyte. Sci Agric 60:329–335

    Article  CAS  Google Scholar 

  • Nogueira MA, Nehls U, Hampp R, Poralla K, Cardoso EJBN (2007) Mycorrhiza and soil bacteria influence extractable iron and manganese in soil and uptake by soybean. Plant Soil 298:273–284

    Article  CAS  Google Scholar 

  • Olsen SR, Cole V, Watanabe FS, Dean LA (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. USDA Circ. 939. US Government Printing Office, Washinghton DC, 1–19

  • Pedas P, Husted S, Skytte K, Schjoerring JK (2011) Elevated phosphorus impedes manganese acquisition by barley plants. Front Plant Sci 2:37

    Article  PubMed Central  PubMed  Google Scholar 

  • Phillips JM, Hayman DS (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

    Article  Google Scholar 

  • Plenchette C, Fortin JA, Furlan V (1983) Growth responses of several plant species to mycorrhizae in a soil of moderate P-fertility. Mycorrhizal dependency under field conditions. Plant Soil 70:191–209

    Article  Google Scholar 

  • Porras-Piedra A, Soriano-Martín ML, Porras-Soriano A, Izquierdo GF (2005) Influence of arbuscular mycorrhizas on the growth rate of mist-propagated olive plantlets. Span J Agric Res 3:98–105

    Article  Google Scholar 

  • Porras-Soriano A, Soriano-Martín ML, Porras-Piedra A, Azcón R (2009) Arbuscular mycorrhizal fungi increate growth, nutrient uptake and tolerance to salinity in olive trees under nursery conditions. J Plant Physiol 166:1350–1359

    Article  CAS  PubMed  Google Scholar 

  • Posta K, Marschner H, Römheld V (1994) Manganese reduction in the rhizosphere of mycorrhizal and nonmycorrhizal maize. Mycorrhiza 5:119–124

    Article  CAS  Google Scholar 

  • Pozo MJ, Azcón-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398

    Article  CAS  PubMed  Google Scholar 

  • Rillig MC (2004) Arbuscular mycorrhizae, glomalin, and soil aggregation. Can J Soil Sci 84:355–363

    Article  Google Scholar 

  • Roldán-Fajardo BE, Barea JM (1986) Mycorrhizal dependency in the olive tree (Olea europaea L.). In: Gianninazzi-Pearson V, Gianninazzi S (eds) Les mycorhizes: physiologie et gènètique, Proc. of the 1st Europ. Symp. on Mycorrhizae. Dijon 1-5 July 1985. INRA, Paris, pp 323–326

  • Salama AZ, Lazova GN, Stoinova ZG, Popova LP, El-Fouly MM (2002) Effect of zinc deficiency on photosynthesis in chick-pea and maize plants. C R Acad Bulg Sci 55:65–68

    CAS  Google Scholar 

  • Schausberger P, Peneder S, Jürschirk S, Hoffmann D (2012) Mychorriza changes plant volatiles to attract spider mite enemiers. Funct Ecol 26:441–449

    Article  Google Scholar 

  • Seeman JR, Sharkey TD, Wang J, Osmond CB (1987) Environmental effects on photosynthesis, nitrogen use efficiency, and metabolic pools in leaves of sun and shade plants. Plant Physiol 84:796–802

    Article  Google Scholar 

  • Shane MW, Lambers H (2005) Manganese accumulation in leaves of Hakea prostrata (Proteaceae) and the significance of cluster roots for micronutrient uptake as dependent on phosphorus supply. Physiol Plant 124:441–445

    Article  CAS  Google Scholar 

  • Sharma PN, Tripathi A, Bisht SS (1995) Zinc requirement for stomatal opening in cauliflower. Plant Physiol 107:751–756

    Article  PubMed Central  PubMed  Google Scholar 

  • Sidhoum W, Fortas Z (2013) Effect of arbuscular mycorrhizal fungi on growth of semi-woody olive cuttings of the variety “Sigoise” in Algeria. Am J Res Com 1:244–257

    Google Scholar 

  • Singh NV, Singh SK, Singh AK (2011) Standardization of embryo rescue technique and bio-hardening of grape hybrids (Vitis vinifera L.) using arbuscular mycorrhizal fungi (AMF) under sub-tropical conditions. Vitis 50:115–118

    Google Scholar 

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

    Google Scholar 

  • Smith SE, Facelli E, Pope S, Smith FA (2010) Plant performance in stressful environments: interpreting new and established knowledge of the roles of arbuscular mycorrhizas. Plant Soil 326:3–20

    Article  CAS  Google Scholar 

  • Soil Survey Staff (1996) Soil survey laboratory methods manual. USDA Natural Resources Conservation Service, Soil survey Investigations Report No 42, Version 3.0. National Soil Survey Center, Lincoln

    Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Treseder KK, Cross A (2006) Global distributions of arbuscular mycorrhizal fungi. Ecosystems 9:305–316

    Article  Google Scholar 

  • Trouvelot A, Kough JL, Gianinazzi-Pearson V (1986) Mesure du taux de mycorhization VA d’un système radiculaire. Recherche des méthodes d’estimation ayant une signification fonctionnelle. In: Gianinazzi-Pearson V, Gianinazzi S (eds) The mycorrhizae: physiology and genetics. INRA Presse, Paris, France, pp 217–221

    Google Scholar 

  • Turnau K (1998) Heavy metal content and localization in mycorrhizal Euphorbia cyparissias from zinc wastes in Southern Poland. Acta Soc Bot Pol 67:105–113

    Article  CAS  Google Scholar 

  • Turnau K, Dexheimer J (1996) Acid phosphatase activity in Pisolithus arrhizus. Mycelium treated with cadmium dust. Mycorrhiza 5:205–211

    Article  Google Scholar 

  • Van Tuinen D, Jacquot E, Zhao B, Gollotte A, Gianinazzi-Pearson V (1998) Characterization of root colonization profiles by a microcosm community of arbuscular mycorrhizal fungi using 25 rDNA-targeted nested PCR. Mol Ecol 7:879–887

    Article  PubMed  Google Scholar 

  • Walkley A, Black IA (1934) An examination of the Degtjareff method for determining organic carbon in soils: Effect of variations in digestion conditions and of inorganic soil constituents. Soil Sci 63:251–263

    Article  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, Inc, New York, pp 315–322

    Chapter  Google Scholar 

  • Williams A, Norton DA, Ridgway HJ (2012) Different arbuscular mycorrhizal inoculants affect the growth and survival of Podocarpus cunninghamii restoration plantings in the Mackenzie Basin, New Zealand. N Z J Bot 50:473–479

    Article  Google Scholar 

  • Wood CW, Reeves DW, Himelrick DG (1993) Relationships between chlorophyllmeter readings and leaf chlorophyll concentration, n status, and crop yield: a review. Proc Agron Soc NZ 23:1–9

  • Wu QS, Li GH, Zou YN (2011) Roles of arbuscular mycorrhizal fungi on growth and nutrient acquisition of peach (Prunus persica l. Batsch) seedlings. J Anim Plant Sci 21:746–750

    CAS  Google Scholar 

  • Yavitt JB, Harms KE, Garcia MN et al (2009) Spatial heterogeneity of soil chemical properties in a lowland tropical moist forest, Panama. Aust J Soil Res 47:674–687

    Article  CAS  Google Scholar 

  • Yoder BJ, Pettigrew-Crosby RE (1995) Predicting nitrogen and chlorophyll content and concentrations from reflectance spectra (400–2500 nm) at leaf and canopy scales. Remote Sens Environ 53:199–211

    Article  Google Scholar 

  • Zhu YG, Smith FA, Smith SE (2002) Phosphorus efficiencies and their effects on Zn, Cu, and Mn nutrition of different barley (Hordeum vulgare) cultivars grown in sand culture. Aust J Agric Res 53:211–216

    Article  CAS  Google Scholar 

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  1. Consiglio per la Ricerca e la Sperimentazione in Agricoltura, Research Centre for Oliviculture and Olive Oil Industry, Rende, Italy

    Caterina Briccoli Bati & Elena Santilli

  2. Department of Crop Systems, Forestry and Environmental Sciences, University of Basilicata, Potenza, Italy

    Luca Lombardo

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  1. Caterina Briccoli Bati
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Briccoli Bati, C., Santilli, E. & Lombardo, L. Effect of arbuscular mycorrhizal fungi on growth and on micronutrient and macronutrient uptake and allocation in olive plantlets growing under high total Mn levels. Mycorrhiza 25, 97–108 (2015). https://doi.org/10.1007/s00572-014-0589-0

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