Abstract
Background and aims
Zinc (Zn) deficiency is a global problem in human nutrition due to imbalanced diets based on staple foods of low Zn contents. This study investigated the potential of using clover (Trifolium alexandrinum L.) and mustard (Sinapis alba L.) green manure crops to increase soil Zn uptake by wheat (Trifolium aestivum L.) without enhancing cadmium (Cd) accumulation.
Methods
A factorial pot experiment with wheat was performed with three green manure treatments (clover, mustard or no green manure) and three soil treatments which were a high-Zn soil (FYM), a low-Zn soil (TURK) and the TURK soil with mineral Zn fertilization (TURK+ZN). Green manure crops were grown first and then incorporated into the soils before wheat.
Results
In contrast to mustard, clover increased grain Zn concentrations in the FYM and TURK+ZN soils, but not in the TURK soil. The effect appeared to be due to high soil nitrogen inputs and concurrent pH decrease, root biomass increase, and the release of organic ligands mobilizing soil Zn and Cd. However, the high N inputs also induced Cd accumulation above critical thresholds.
Conclusions
The study suggests that on Zn sufficient soils or in combination with Zn fertilizer, leguminous green manure can increase soil Zn accumulation by wheat.
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Abbreviations
- DOC:
-
Dissolved organic carbon
- DTPA:
-
Diethylenetriamine pentaacetic acid
- FLOW:
-
Wheat flowering
- FYM:
-
Zn sufficient soil from the farmyard manure treatment of the Swiss long-term trial ZOFE
- NGM:
-
Control treatment without green manure
- PLA:
-
Wheat planting
- SIN:
-
Sinapis alba L. (white mustard)
- TFAA:
-
Total free amino acids
- TRI:
-
Trifolium alexandrinum L. (berseem clover)
- TURK:
-
Zn deficient soil from Central Anatolia in Turkey
- TURK + ZN:
-
Zn deficient soil from Central Anatolia (Turkey) fertilized with 5 mg kg−1 Zn
References
Aghili F, Gamper HA, Eikenberg J, Khoshgoftarmanesh AH, Afyuni M, Schulin R, Jansa J, Frossard E (2014) Green manure addition to soil increases grain zinc concentration in bread wheat. PLoS One 9:e101487. https://doi.org/10.1371/journal.pone.0101487
Agroscope (1998) Bestimmung der maximalen Wasserhaltekapazität. Schweizerische Referenzmethoden der Eidgenössischen landwirtschaftlichen Forschungsanstalten Band 2: Bodenuntersuchung zur Standortcharakterisierung. Eidgenössische Forschungsanstalt für Landwirtschaftlichen Pflanzenbau, Zürich-Reckenholz
Agroscope (1999) pH-Wert in Wassersuspension (1:2.5) & pH-Wert in CaCl2-Suspension (1:2.5). Schweizerische Referenzmethoden der Eidgenössischen landwirtschaftlichen Forschungsanstalten Band 2: Bodenuntersuchung zur Standortcharakterisierung
Agroscope (2008) Bestimmung der Körnung im mineralischen Anteil der Feinerde. Schweizerische Referenzmethoden der Eidgenössischen landwirtschaftlichen Forschungsanstalten Band 2: Bodenuntersuchung zur Standortcharakterisierung
Agroscope (2015) Extraktion von Abfalldüngern mit Königswasser in geschlossenen Gefässen im Mikrowellenofen. Schweizerische Referenzmethoden der Eidgenössischen landwirtschaftlichen Forschungsanstalten Band 4: Düngeruntersuchung
Alloway BJ (2009) Soil factors associated with zinc deficiency in crops and humans. Environ Geochem Hlth 31:537–548. https://doi.org/10.1007/s10653-009-9255-4
Blume H-P, Brümmer GW, Fleige H, Horn R, Kandeler E, Kögel-Knabner I, Kretzschmar R, Stahr K, Wilke B-M (2016) Scheffer/Schachtschabel Soil Science. Springer, Berlin
Bouis HE, Welch RM (2010) Biofortification-a sustainable agricultural strategy for reducing micronutrient malnutrition in the global south. Crop Sci 50:S20–S32. https://doi.org/10.2135/cropsci2009.09.0531
Brennan RF, Gartrell JW (1990) Reaction of Zinc with Soil Affecting Its Availability to Subterranean Clover .1. The Relationship between Critical Concentrations of Extractable Zinc and Properties of Australian Soils Responsive to Applied Zinc. Aust J Soil Res 28:293–302. https://doi.org/10.1071/Sr9900293
Broadley M, Brown P, Cakmak I, Rengel Z, Zhao FJ (2012) Function of nutrients: micronutrients. In: Marschner P (ed) Marschner's mineral nutrition of higher plants, 3rd edn. Elsevier, Amsterdam
Brunner J, Jäggli F, Nievergelt J, Peyer K (1997) Kartieren und Beurteilen von Landwirtschaftsböden. Schriftenreihe der FAL (Eidgenössische Forschungsanstalt für Agrarökologie und Landbau) 24. Eidgenössische Forschungsanstalt für Agrarökologie und Landbau, Zürich-Reckenholz
Cakmak I (2008) Enrichment of cereal grains with zinc: agronomic or genetic biofortification? Plant Soil 302:1–17. https://doi.org/10.1007/s11104-007-9466-3
Cakmak I, Kutman UB (2017) Agronomic biofortification of cereals with zinc: a review. Eur J Soil Sci. doi:https://doi.org/10.1111/ejss.12437.
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. https://doi.org/10.1007/Bf00015299
Cakmak I, Pfeiffer WH, McClafferty B (2010) Biofortification of durum wheat with zinc and iron. Cereal Chem 87:10–20. https://doi.org/10.1094/Cchem-87-1-0010
Clemens S, Persoh D (2009) Multi-tasking phytochelatin synthases. Plant Sci 177:266–271. https://doi.org/10.1016/j.plantsci.2009.06.008
Clemens S, Aarts MGM, Thomine S, Verbruggen N (2013) Plant science: the key to preventing slow cadmium poisoning. Trends Plant Sci 18:92–99. https://doi.org/10.1016/j.tplants.2012.08.003
Delogu G, Cattivelli L, Pecchioni N, De Falcis D, Maggiore T, Stanca AM (1998) Uptake and agronomic efficiency of nitrogen in winter barley and winter wheat. Eur J Agron 9:11–20. https://doi.org/10.1016/S1161-0301(98)00019-7
EDI (1995) Verordnung des EDI über Fremd- und Inhaltsstoffe in Lebensmitteln (817.021.23). Eidgenössisches Departement des Innern, Bern
EFSA (2012) Cadmium dietary exposure in the European population. European Food Safety Authority. EFSA Journal 10. doi:https://doi.org/10.2903/j.efsa.2012.2551.
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 ((65) Zn) in wheat. New Phytol 189:438–448. https://doi.org/10.1111/j.1469-8137.2010.03488.x
Evans A (1991) Influence of low-molecular-weight organic-acids on zinc distribution within micronutrient pools and zinc uptake by wheat. J Plant Nutr 14:1307–1318. https://doi.org/10.1080/01904169109364287
Fageria NK (2007) Green manuring in crop production. J Plant Nutr 30:691–719. https://doi.org/10.1080/01904160701289529
FAO/WHO (1995) Codex Alimentarius: general standard for contaminants and toxins in food and feed (CODEX STAN 193). Food and Agriculture Organization of the United Nations & World Health Organization, Rome
Fischer H, Meyer A, Fischer K, Kuzyakov Y (2007) Carbohydrate and amino acid composition of dissolved organic matter leached from soil. Soil Biol Biochem 39:2926–2935. https://doi.org/10.1016/j.soilbio.2007.06.014
Franchini JC, Gonzalez-Vila FJ, Cabrera F, Miyazawa M, Pavan MA (2001) Rapid transformations of plant water-soluble organic compounds in relation to cation mobilization in an acid Oxisol. Plant Soil 231:55–63. https://doi.org/10.1023/A:1010338917775
Frossard E, Julien P, Neyroud J-A, Sinaj S (2004) Phosphor in Böden- Standortbestimmung Schweiz. Schriftenreihe Umwelt Nr. 368, Bern
Gibson RS (2012) Zinc deficiency and human health: etiology, health consequences, and future solutions. Plant Soil 361:291–299. https://doi.org/10.1007/s11104-012-1209-4
Graham RD, Ascher JS, Hynes SC (1992) Selecting zinc-efficient cereal genotypes for soils of low zinc status. Plant Soil 146:241–250. https://doi.org/10.1007/Bf00012018
Graham RD, Welch RM, Saunders DA, Ortiz-Monasterio I, Bouis HE, Bonierbale M, de Haan S, Burgos G, Thiele G, Liria R, Meisner CA, Beebe SE, Potts MJ, Kadian M, Hobbs PR, Gupta RK, Twomlow S (2007) Nutritious subsistence food systems. Adv Agron 92:1–74. https://doi.org/10.1016/S0065-2113(04)92001-9
Grewal HS, Stangoulis JCR, Potter TD, Graham RD (1997) Zinc efficiency of oilseed rape (Brassica napus and B-juncea) genotypes. Plant Soil 191:123–132. https://doi.org/10.1023/A:1004289422276.
Grüter R, Costerousse B, Bertoni A, Mayer J, Thonar C, Frossard E, Schulin R, Tandy S (2017) Green manure and long-term fertilization effects on soil zinc and cadmium availability and uptake by wheat (Triticum Aestivum L.) at different growth stages. Sci Total Environ 599–600:1330–1343. https://doi.org/10.1016/j.scitotenv.2017.05.070
Habiby H, Afyuni M, Khoshgoftarmanesh AH, Schulin R (2014) Effect of preceding crops and their residues on availability of zinc in a calcareous Zn-deficient soil. Biol Fertil Soils 50:1061–1067. https://doi.org/10.1007/s00374-014-0926-7
Hart JJ, Welch RM, Norvell WA, Kochian LV (2002) Transport interactions between cadmium and zinc in roots of bread and durum wheat seedlings. Physiol Plant 116:73–78. https://doi.org/10.1034/j.1399-3054.2002.1160109.x
Harter RD, Naidu R (1995) Role of metal-organic complexation in metal sorption by soils. Adv Agron 55:219–263. https://doi.org/10.1016/S0065-2113(08)60541-6
Hendershot W, Lalande H, Duquette M (1993) Ion exchange and exchangeable cations. Soil Sampling Methods Anal 19:167–176
Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Circ Calif Agric Exp Station 347:23–32
Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363. https://doi.org/10.1002/bimj.200810425
Hotz C, Brown KH (2004) Assessment of the risk of zinc deficiency in populations and options for its control. International nutrition foundation: for UNU.
Hu DJ, Bell RW, Xie ZC (1996) Zinc and phosphorus responses in transplanted oilseed rape (Brassica napus). Soil Sci Plant Nutr 42:333–344
IUSS Working Group WRB (2014) World Reference Base for Soil Resources. In: International soil classification system for naming soils and creating legends for soil maps. World Soil Resources Reports No. 106, FAO, Rome
Jarrell WM, Beverly RB (1981) The dilution effect in plant nutrition studies. Adv Agron 34:197–224. https://doi.org/10.1016/S0065-2113(08)60887-1
Jiao Y, Grant CA, Bailey LD (2004) Effects of phosphorus and zinc fertilizer on cadmium uptake and distribution in flax and durum wheat. J Sci Food Agric 84:777–785. https://doi.org/10.1002/jsfa.1648
Jones D, Willett V (2006) Experimental evaluation of methods to quantify dissolved organic nitrogen (DON) and dissolved organic carbon (DOC) in soil. Soil Biol Biochem 38:991–999. https://doi.org/10.1016/j.soilbio.2005.08.012
Jones DL, Owen AG, Farrar JF (2002) Simple method to enable the high resolution determination of total free amino acids in soil solutions and soil extracts. Soil Biol Biochem 34:1893–1902. https://doi.org/10.1016/S0038-0717(02)00203-1
Jones DL, Dennis PG, Owen AG, van Hees PAW (2003) Organic acid behavior in soils - misconceptions and knowledge gaps. Plant Soil 248:31–41. https://doi.org/10.1023/A:1022304332313
Khoshgoftarmanesh AH, Chaney RL (2007) Preceding crop affects grain cadmium and zinc of wheat grown in saline soils of Central Iran. J Environ Qual 36:1132–1136. https://doi.org/10.2134/Jeq2006.0276
Kielland K (1995) Landscape patterns of free amino acids in arctic tundra soils. Biogeochemistry 31:85–98
Köleli N, Eker S, Cakmak I (2004) Effect of zinc fertilization on cadmium toxicity in durum and bread wheat grown in zinc-deficient soil. Environ Pollut 131:453–459. https://doi.org/10.1016/j.envpol.2004.02.012
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. https://doi.org/10.1094/Cchem-87-1-0001.
Kutman UB, Yildiz B, Cakmak I (2011) Effect of nitrogen on uptake, remobilization and partitioning of zinc and iron throughout the development of durum wheat. Plant Soil 342:149–164. https://doi.org/10.1007/s11104-010-0679-5
Kuzyakov Y, Friedel JK, Stahr K (2000) Review of mechanisms and quantification of priming effects. Soil Biol Biochem 32:1485–1498. https://doi.org/10.1016/S0038-0717(00)00084-5
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. https://doi.org/10.1016/j.soilbio.2013.11.001
Lindsay WL, Norvell WA (1978) Development of a Dtpa soil test for zinc, iron, manganese, and copper. Soil Sci Soc Am J 42:421–428. https://doi.org/10.2136/sssaj1978.03615995004200030009x.
Ma YB, Uren NC (1997) The effects of temperature, time and cycles of drying and rewetting on the extractability of zinc added to a calcareous soil. Geoderma 75:89–97. https://doi.org/10.1016/S0016-7061(96)00080-8
Mertens J, Smolders E (2013) Zinc. In: Alloway BJ (ed) Heavy metals in soils: trace metals and metalloids in soils and their bioavailability. Springer, Dordrecht
Miranda KM, Espey MG, Wink DA (2001) A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide 5:62–71. https://doi.org/10.1006/niox.2000.0319
Morel C, Plenchette C, Fardeau JC (1992) The Management of Phosphate Fertilization in wheat crops. Agronomie 12:565–579. https://doi.org/10.1051/agro:19920801.
Mulvaney R (1996) Nitrogen-inorganic forms. Methods of soil analysis Part 3:1123–1184
Oberholzer HR, Leifeld J, Mayer J (2014) Changes in soil carbon and crop yield over 60 years in the Zurich organic fertilization experiment, following land-use change from grassland to cropland. J Plant Nutr Soil Sc 177:696–704. https://doi.org/10.1002/jpln.201300385
Oliver DP, Schultz JE, Tiller KG, Merry RH (1993) The effect of crop rotations and tillage practices on cadmium concentration in wheat-grain. Aust J Agric Res 44:1221–1234. https://doi.org/10.1071/Ar9931221
Oliver DP, Hannam R, Tiller KG, Wilhelm NS, Merry RH, Cozens GD (1994) The effects of zinc fertilization on cadmium concentration in wheat-grain. J Environ Qual 23:705–711. https://doi.org/10.2134/jeq1994.00472425002300040013x
Olsen SR, Cole C, Watanabe FS, Dean L (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. US Department of Agriculture, Washington, DC
Palmgren MG, Clemens S, Williams LE, Kraemer U, Borg S, Schjorring JK, Sanders D (2008) Zinc biofortification of cereals: problems and solutions. Trends Plant Sci 13:464–473. https://doi.org/10.1016/j.tplants.2008.06.005
Puschenreiter M, Gruber B, Wenzel WW, Schindlegger Y, Hann S, Spangl B, Schenkeveld WDC, Kraemer SM, Oburger E (2017) Phytosiderophore-induced mobilization and uptake of cd, cu, Fe, Ni, Pb and Zn by wheat plants grown on metal-enriched soils. Environ Exp Bot 138:67–76. https://doi.org/10.1016/j.envexpbot.2017.03.011
R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria URL http://www.R-project.org/
Randall PJ, Spencer K, Freney JR (1981) Sulfur and nitrogen-fertilizer effects on wheat .1. Concentrations of sulfur and nitrogen and the nitrogen to sulfur ratio in grain, in relation to the yield response. Aust J Agric Res 32:203–212. https://doi.org/10.1071/Ar9810203
Reuter D, Robinson J (1986) Plant analysis: an interpretation manual. Inkata Press, Melbourne
Schoenau J, O’Halloran I (2008) Sodium bicarbonate-extractable phosphorus. In: Carter MR, Gregorich EG (eds) Soil sampling and methods of analysis. 2nd edn. CRC Press, FL USA
Schulte EE, Kelling KA (2004) Soil and applied sulfur, A2525. University of Wisconsin-Extension, Madison, Understanding Plant Nutrients
Sinclair SA, Krämer U (2012) The zinc homeostasis network of land plants. Bba-Mol Cell Res 1823:1553–1567. https://doi.org/10.1016/j.bbamcr.2012.05.016
Smolders E, Mertens J (2013) Cadmium. In: Alloway BJ (ed) Heavy metals in soils: trace metals and metalloids in soils and their bioavailability. Springer, Dordrecht
Soltani S, Khoshgoftarmanesh AH, Afyuni M, Shrivani M, Schulin R (2014) The effect of preceding crop on wheat grain zinc concentration and its relationship to total amino acids and dissolved organic carbon in rhizosphere soil solution. Biol Fertil Soils 50:239–247. https://doi.org/10.1007/s00374-013-0851-1
Wangstrand H, Eriksson J, Oborn I (2007) Cadmium concentration in winter wheat as affected by nitrogen fertilization. Eur J Agron 26:209–214. https://doi.org/10.1016/j.eja.2006.09.010
Wessells KR, Brown KH (2012) Estimating the global prevalence of zinc deficiency: results based on zinc availability in National Food Supplies and the prevalence of stunting. PLoS One 7. doi:https://doi.org/10.1371/journal.pone.0050568.
Xue YF, Yue SC, Zhang YQ, Cui ZL, Chen XP, Yang FC, Cakmak I, McGrath SP, Zhang FS, Zou CQ (2012) Grain and shoot zinc accumulation in winter wheat affected by nitrogen management. Plant Soil 361:153–163. https://doi.org/10.1007/s11104-012-1510-2
Zhao FJ, Hawkesford MJ, McGrath SP (1999) Sulphur assimilation and effects on yield and quality of wheat. J Cereal Sci 30:1–17. https://doi.org/10.1006/jcrs.1998.0241.
Zörb C, Grover C, Steinfurth D, Muhling KH (2010) Quantitative proteome analysis of wheat gluten as influenced by N and S nutrition. Plant Soil 327:225–234. https://doi.org/10.1007/s11104-009-0049-3
Zou CQ, Zhang YQ, Rashid A, Ram H, Savasli E, Arisoy RZ, Ortiz-Monasterio I, Simunji S, Wang ZH, Sohu V, Hassan M, Kaya Y, Onder O, Lungu O, Mujahid MY, Joshi AK, Zelenskiy Y, Zhang FS, Cakmak I (2012) Biofortification of wheat with zinc through zinc fertilization in seven countries. Plant Soil 361:119–130. https://doi.org/10.1007/s11104-012-1369-2
Acknowledgements
We thank Ismail Cakmak (Sabanci University, Istanbul) and Jochen Mayer (Agroscope, Zurich) for providing the soils, Benjamin Costerousse and Samuel Ndungu for their assistance in rhizobium inoculation, Steffen Schweizer and Christian Arter for their help in sample preparation and analysis, Andreas Papritz for statistical advice, and Björn Studer, Laurie Schönholzer and Christophe Zeder for their expert advice and technical support in the chemical analysis of the samples. Furthermore, we thank the Mercator Research Program of the ETH Zurich World Food System Center and the ETH Zurich Foundation for supporting this project financially.
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Grüter, R., Meister, A., Schulin, R. et al. Green manure effects on zinc and cadmium accumulation in wheat grains (Triticum aestivum L.) on high and low zinc soils. Plant Soil 422, 437–453 (2018). https://doi.org/10.1007/s11104-017-3486-4
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DOI: https://doi.org/10.1007/s11104-017-3486-4