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High phosphorus supply reduced zinc concentration of wheat in native soil but not in autoclaved soil or nutrient solution

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Abstract

Aims

Phosphorus (P)-induced zinc (Zn) deficiency is one of the most commonly studied antagonistic interactions in plant nutrition. However, there are many controversial reports about P–Zn interaction, possibly related to growth conditions. In this study, the effects of P supply on the root uptake and tissue concentrations of Zn as well as the development of Zn deficiency were investigated in wheat (Triticum aestivum) grown in different media.

Methods

Plants were grown under greenhouse and growth chamber conditions in native soil, autoclaved soil and nutrient solution with different P and Zn supplies. In the soil experiment, the shoot biomass and grain yield were measured whereas in the nutrient solution experiment, the root and shoot biomass were determined. Development of Zn deficiency symptoms was examined. Concentrations of Zn, P and other elements were measured in harvested tissues. Mycorrhizal colonization of roots was scored in soil-grown plants. Root uptake of stable Zn isotope (70Zn) was investigated at different P rates in a separate nutrient solution experiment.

Results

Higher P rates caused substantial decreases in shoot and grain Zn concentrations in native soil but not in autoclaved soil. Treatment of native soil with increasing P significantly reduced mycorrhizal colonization. At low Zn, P applications aggravated Zn deficiency symptoms in both soil and solution culture. In solution culture, root and shoot Zn concentrations were not lowered by higher P rates. Root uptake of 70Zn from nutrient solution was even depressed at low P.

Conclusions

The negative effect of increasing P supply on root Zn uptake and tissue Zn concentrations in wheat is mycorrhiza-dependent and may completely disappear in a mycorrhiza-free environment.

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References

  • Anuradha M, Narayanan A (1991) Promotion of root elongation by phosphorus deficiency. Plant Soil 136:273–275

    Article  CAS  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 

  • Bolan NS, Robson AD, Barrow NJ (1984) Increasing phosphorus supply can increase the infection of plant roots by vesicular-arbuscular mycorrhizal fungi. Soil Biol Biochem 16:419–420

    Article  CAS  Google Scholar 

  • Boyd HW (1971) Manganese toxicity to peanuts in autoclaved soil. Plant Soil 34:133–144

    Article  Google Scholar 

  • Broadley MR, Lochlainn SO, Hammond JP, Bowen HC, Cakmak I, Eker S, Erdem H, King GJ, White PJ (2010) Soil zinc (Zn) concentration varies widely within Brassica oleracea L. and is affected by soil Zn and phosphorus (P) levels. J Hortic Sci Biotechnol 85:375–380

    CAS  Google Scholar 

  • Cakmak I (2008) Enrichment of cereal grains with zinc: agronomic or genetic biofortification? Plant Soil 302:1–17

  • Cakmak I, Marschner H (1986) Mechanism of phosphorus-induced zinc deficiency in cotton. I. Zinc deficiency-enhanced uptake rate of phosphorus. Physiol Plant 68:483–490

    Article  CAS  Google Scholar 

  • Cakmak I, Marschner H (1987) Mechanism of phosphorus induced zinc deficiency in cotton. III. Changes in physiological availability of zinc in plants. Physiol Plant 70:13–20

    Article  CAS  Google Scholar 

  • Cakmak I, Hengeler C, Marschner H (1994) Partitioning of shoot and root dry matter and carbohydrates in bean plants suffering from phosphorus, potassium and magnesium deficiency. J Exp Bot 45:1245–1250

    Article  CAS  Google Scholar 

  • Cakmak I, Yilmaz A, Kalayci M, Ekiz H, Torun B, Erenoglu B, Braun HJ (1996) Zinc deficiency as a critical problem in wheat production in Central Anatolia. Plant Soil 180:165–172

    Article  CAS  Google Scholar 

  • Cakmak I, Ekiz H, Yilmaz A, Torun B, Koleli N, Gultekin I, Alkan Ai Eker S (1997) Differential response of rye, triticale, bread and durum wheats to zinc deficiency in calcareous soils. Plant Soil 188:1–10

    Article  CAS  Google Scholar 

  • Cavagnaro TR (2008) The role of arbuscular mycorrhizas in improving plant zinc nutrition under low soil zinc concentrations: a review. Plant Soil 304:315–325

    Article  CAS  Google Scholar 

  • Dang YP, Edwards DG, Dalal RC, Tiller KG (1993) Identification of an index tissue to predict zinc status of wheat. Plant Soil 154:161–167

    Article  CAS  Google Scholar 

  • Dwivedi RS, Randhawa NS, Bansal RL (1975) Phosphorus-zinc interaction I. Sites of immobilization of zinc in maize at high level of phosphorus. Plant Soil 43:639–648

    Article  CAS  Google Scholar 

  • Endlweber K, Scheu S (2006) Establishing arbuscular mycorrhiza-free soil: a comparison of six methods and their effects on nutrient mobilization. Appl Soil Ecol 34:276–279

    Article  Google Scholar 

  • Erenoglu EB, Kutman UB, Ceylan Y, Yildiz B, Cakmak I (2011) Improved nitrogen nutrition enhances root uptake, root-to-shoot translocation and remobilization of zinc (65Zn) in wheat. New Phytol 189:438–448

    Article  CAS  PubMed  Google Scholar 

  • Genc Y, McDonald GK, Graham RD (2002) A soil-based method to screen for zinc efficiency in seedlings and its ability to predict yield responses to zinc deficiency in mature plants. Aust J Agric Res 53:409–421

    Article  CAS  Google Scholar 

  • Gianquinto G, Abu-Rayyan A, Tola LD, Piccotino D, Pezzarossa B (2000) Interaction effects of phosphorus and zinc on photosynthesis, growth and yield of dwarf bean grown in two environments. Plant Soil 220:219–228

    Article  CAS  Google Scholar 

  • Giovanetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular-arbuscular mycorrhizal infection in roots. New Phytol 84:489–500

  • Huang C, Barker SJ, Langridge P, Smith FW, Graham RD (2000) Zinc deficiency up-regulates expression of high-affinity phosphate transporter genes in both phosphate-sufficient and -deficient barley roots. Plant Physiol 124:415–422

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jackson LE, Miller D, Smith SE (2002) Arbuscular mycorrhizal colonization and growth of wild and cultivated lettuce in response to nitrogen and phosphorus. Sci Hortic 94:205–218

    Article  Google Scholar 

  • Kothari SK, Marschner H, Romheld V (1991) Contribution of the VA mycorrhizal hyphae in acquisition of phosphorus and zinc by maize grown in a calcareous soil. Plant Soil 131:177–185

    Article  CAS  Google Scholar 

  • Krebs NF (2013) Update on zinc deficiency and excess in clinical pediatric practice. Ann Nutr Metab 62:19–29

    Article  CAS  PubMed  Google Scholar 

  • Kutman UB, Yildiz B, Ozturk L, Cakmak I (2010) Biofortification of durum wheat with zinc through soil and foliar applications of nitrogen. Cereal Chem 87:1–9

    Article  CAS  Google Scholar 

  • Lambert DH, Weidensaul TC (1991) Element uptake by mycorrhizal soybean from sewage-sludge treated soil. Soil Sci Soc Am J 55:393–398

    Article  CAS  Google Scholar 

  • Lambert DH, Baker DE, Cole H (1979) The role of mycorrhizae in the interactions of phosphorus with zinc, copper, and other elements. Soil Sci Soc Am J 43:976–980

    Article  CAS  Google Scholar 

  • Lehmann A, Veresoglou SD, Leifheit EF, Rillig MC (2014) Arbuscular mycorrhizal influence on zinc nutrition in crop plants-a meta-analysis. Soil Biol Biochem 69:123–131

    Article  CAS  Google Scholar 

  • Li XL, Marschner H, George E (1991) Acquisition of phosphorus and copper by VA-mycorrhizal hyphae and root-to-shoot transport in white clover. Plant Soil 136:49–57

    Article  CAS  Google Scholar 

  • Li HY, Zhu YG, Smith SE, Smith FA (2003) Phosphorus–zinc interactions in two barley cultivars differing in phosphorus and zinc efficiencies. J Plant Nutr 26:1085–1099

    Article  CAS  Google Scholar 

  • Lindsay WL, Norvell WA (1978) Development of a DTPA soil test for zinc, iron, manganese and copper. Soil Sci Soc Am 42:421–428

  • Loneragan JF, Webb MJ (1993) Interactions between zinc and other nutrients affecting the growth of plants. In: Robson AD (ed) Zinc in soils and plants. Springer, the Netherlands, pp 119–134

    Chapter  Google Scholar 

  • Loneragan JF, Grove TS, Robson AD, Snowball K (1979) Phosphorus toxicity as a factor in zinc-phosphorus interactions in plants. Soil Sci Soc Am J 43:966–972

    Article  CAS  Google Scholar 

  • Loneragan JF, Grunes DL, Welch RM, Aduayi A, Tengah A, Lazar VA, Cary EE (1982) Phosphorus accumulation and toxicity in leaves in relation to zinc supply. Soil Sci Soc Am J 46:345–352

    Article  CAS  Google Scholar 

  • Lu Z, Grewal HS, Graham RD (1998) Dry matter production and uptake of zinc and phosphorus in two oilseed rape genotypes under differential rates of zinc and phosphorus supply. J Plant Nutr 21:25–38

    Article  CAS  Google Scholar 

  • Mahmood T, Mehnaz S, Fleischmann F, Ali R, Hashmi ZH, Iqbal Z (2014) Soil sterilization effects on root growth and formation of rhizosheaths in wheat seedlings. Pedobiologia 57:123–130

    Article  Google Scholar 

  • Marschner P (2012) Marschner’s mineral nutrition of higher plants, 3rd edn. Academic Press, Elsevier, USA

    Google Scholar 

  • Marschner H, Cakmak I (1986) Mechanism of phosphorus-induced zinc deficiency in cotton. II. Evidence for impaired shoot control of phosphorus uptake and translocation under zinc deficiency. Physiol Plant 68:491–496

    Article  CAS  Google Scholar 

  • Marschner H, Schropp A (1977) Vergleichende Untersuchungen über die Empfindlichkeit von 6 Unterlagensorten der Weinrebe gegenüber Phosphat-induziertem Zink-Mangel. Vitis 16:79–88

    CAS  Google Scholar 

  • McIlveen WD, Cole H (1979) Influence of zinc on development of the endomycorrhizal fungus Glomus mosseae and its mediation of phosphorus uptake by Glycine max ‘Amsot 71’. Agric Environ 4:245–256

    Article  CAS  Google Scholar 

  • Meredith JA, Anderson RC (1992) The influence of varied microbial substrate conditiond on the growth and mycorrhizal colonization of little bluestem [Schizachyrium scoparium (Michx.) Nash]. New Phytol 121:235–242

    Article  Google Scholar 

  • Nagy R, Drissner D, Amrhein N, Jakobsen I, Bucher M (2009) Mycorrhizal phosphate uptake pathway in tomato is phosphorus-repressible and transcriptionally regulated. New Phytol 181:950–959

    Article  CAS  PubMed  Google Scholar 

  • Neue HU, Quijano C, Senadhira D, Setter T (1998) Strategies for dealing with micronutrient disorders and salinity in lowland rice systems. Field Crop Res 56:139–155

    Article  Google Scholar 

  • Nichols BJRA, Hopkins GB, Jolley VD, Webb BL, Greenwood BG, Buck R (2012) Phosphorus and zinc interactions and their relationships with other nutrients in maize grown in chelator-buffered nutrient solution. J Plant Nutr 35:123–141

    Article  CAS  Google Scholar 

  • Nogueira MA, Magalhaes GC, Cardoso EJBN (2004) Manganese toxicity in mycorrhizal and phosphorus-fertilized soybean plants. J Plant Nutr 27:141–156

    Article  CAS  Google Scholar 

  • Ortas I (2012) The effect of mycorrhizal fungal inoculation on plant yield, nutrient uptake and inoculation effectiveness under long-term field conditions. Field Crop Res 125:35–48

    Article  Google Scholar 

  • Ortas I, Ortakci D, Kaya Z, Cinar A, Onelge N (2002) Mycorrhizal dependency of sour orange in relation to phosphorus and zinc nutrition. J Plant Nutr 25:1263–1279

    Article  CAS  Google Scholar 

  • Perez-Novo C, Bermudez-Couso A, Lopez-Periago E, Fernandez-Calvino D, Arias-Estevez M (2011) Zinc adsorption in acid soils influence of phosphate. Geoderma 162:358–364

    Article  CAS  Google Scholar 

  • Rahimi A, Schropp A (1984) Carboanhydraseaktivität und extrahierbares Zink als Masstab fur die Zink-Versorgung von Pflanzen. Z Pflanzenernähr Bodenkd 147:572–583

    Article  CAS  Google Scholar 

  • Reinbott EM, Blevins DG (1999) Phosphorus nutritional effects on root hydraulic conductance, xylem water flow and flux of magnesium and calcium in squash plants. Plant Soil 209:263–273

    Article  CAS  Google Scholar 

  • Reinbott EM, Blevis DG (1994) Phosphorus and temperature effects on magnesium, calcium, and potassium in wheat and tall fescue leaves. Agron J 86:523–529

    Article  CAS  Google Scholar 

  • Rengel Z, Romheld V, Marschner H (1998) Uptake of zinc and iron by wheat genotypes differing in tolerance to zinc deficiency. J Plant Physiol 152:433–438

    Article  CAS  Google Scholar 

  • Reuter DJ, Robinson JB (1997) Plant analysis: an interpretation manual, 2nd edn. CSIRO Publishing, Australia

    Google Scholar 

  • Rodrigues-Filho UP, Vaz S, Felicissimo MP, Scarpellini M, Cardoso DR, Vinhas RCJ, Landers R, Schneider JF, McGarvey BR, Andersen ML, Skibsted LH (2005) Heterometallic manganese/zinc-phytate complex as a model compound for metal storage in wheat grains. J Inorg Biochem 99:1973–1982

    Article  CAS  PubMed  Google Scholar 

  • Ryan MH, Angus JF (2003) Arbuscular mycorrhizae in wheat and field pea crops on a low P soil: increased Zn-uptake but no increase in P-uptake or yield. Plant Soil 250:225–239

    Article  CAS  Google Scholar 

  • Ryan MH, McInerney JK, Record IR, Angus JF (2008) Zinc bioavailability in wheat grain in relation to phosphorus fertilizer, crop sequence and mycorrhizal fungi. J Sci Food Agric 88:1208–1216

    Article  CAS  Google Scholar 

  • Sharma PN, Kumar P, Tewari RK (2004) Early signs of oxidative stress in wheat plants subjected to zinc deficiency. J Plant Nutr 27:451–463

    Article  CAS  Google Scholar 

  • Singh JP, Karamanos RE, Stewart JWB (1988) The mechanism of phosphorus-induced zinc deficiency in bean (Phaseolus vulgaris L.). Can J Soil Sci 68:345–358

    Article  CAS  Google Scholar 

  • Skinner PW, Matthews MA (1990) A novel interaction of magnesium translocation with the supply of phosphorus to roots of grapevine (Vitis vinifera L.). Plant Cell Environ 13:821–826

    Article  CAS  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic, Amsterdam

    Google Scholar 

  • Smith FA, Smith SE (1981) Mycorrhizal colonization and growth of Trifolium subterraneum: use of sterilized soil as a control treatment. New Phytol 88:299–309

    Article  CAS  Google Scholar 

  • Subramanian KS, Tenshia V, Jayalakshmi K, Ramachandran V (2009) Role of arbuscular mycorrhizal fungus (Glomus intraradices)—(fungus aided) in zinc nutrition of maize. J Agric Biotechnol Sustain Dev 1:029–038

    CAS  Google Scholar 

  • Thompson JP (1990) Soil sterilization methods to show VA-mycorrhizae aid P and Zn nutrition of wheat in vertisols. Soil Biol Biochem 22:229–240

    Article  CAS  Google Scholar 

  • Tinker PB, Jones MD, Durall DM (1992) A functional comparison of ecto- and endomycorrhizas. In: Read DJ, Lewis DH, Fitter AH, Alexander IJ (eds) Mycorrhizas in ecosystems. C.A.B... International, Wellingford, pp 303–310

    Google Scholar 

  • Verma TS, Minhas RS (1987) Zinc and phosphorus interaction in a wheat-maize cropping system. Fertil Res 13:77–86

    Article  CAS  Google Scholar 

  • Warnock RE (1970) Micronutrient uptake and mobility within corn plants (Zea mays L.) in relation to phosphorus-induced zinc deficiency. Soil Sci Soc Am J 34:765–769

    Article  CAS  Google Scholar 

  • Watts-Williams SJ, Patti AF, Cavagnaro TR (2013) Arbuscular mycrorrhizas are beneficial under both deficient and toxic soil zinc conditions. Plant Soil 371:299–312

    Article  CAS  Google Scholar 

  • Webb MJ, Loneragan JF (1988) Effect of zinc deficiency on growth, phosphorus concentration, and phosphorus toxicity of wheat plants. Soil Sci Soc Am J 52:1676–1680

    Article  CAS  Google Scholar 

  • Williams-Linera G, Ewel JJ (1984) Effect of acutoclave sterilization of a tropical andept on seed germination and seedling growth. Plant Soil 82:263–268

    Article  CAS  Google Scholar 

  • Youngdahl LJ, Svec LV, Liebhardt WC, Teel MR (1977) Changes in the zinc-65 distribution in corn root tissue with a phosphorus variable. Crop Sci 17:66–69

    Article  CAS  Google Scholar 

  • Zhang YQ, Deng Y, Chen RY, Cui ZL, Chen XP, Yost R, Zhang FS, Zou CQ (2012) The reduction in zinc concentration of wheat grain upon increased phosphorus-fertilization and its mitigation by foliar zinc application. Plant Soil 361:143–152

    Article  CAS  Google Scholar 

  • Zhu YG, Smith SE, Smith FA (2001) Zinc (Zn)-phosphorus (P) interactions in two cultivars of spring wheat (Triticum aestivum L.) differing in P uptake efficiency. Ann Bot 88:941–945

    Article  CAS  Google Scholar 

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Acknowledgments

This study was financially supported by the HarvestPlus Program (www.harvestplus.org) and the sponsors of the HarvestPlus Global Zinc Fertilizer Project (www.harvestzinc.org) including Mosaic Company, K + S Kali GmbH, International Zinc Association, Omex Agrifluids, International Fertilizer Industry Association and International Plant Nutrition Institute. We would like also to thank Prof. Dr. Ibrahim Ortas and his team at the Cukurova University in Adana, Turkey, for the advice and contribution to measurement of mycorrhizal colonization of roots.

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  1. Faculty of Engineering and Natural Sciences, Sabanci University, 34956, Istanbul, Turkey

    Emir Ali Ova, Umit Baris Kutman, Levent Ozturk & Ismail Cakmak

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  1. Emir Ali Ova
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  2. Umit Baris Kutman
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Correspondence to Ismail Cakmak.

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Ova, E.A., Kutman, U.B., Ozturk, L. et al. High phosphorus supply reduced zinc concentration of wheat in native soil but not in autoclaved soil or nutrient solution. Plant Soil 393, 147–162 (2015). https://doi.org/10.1007/s11104-015-2483-8

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