Plant and Soil

, Volume 444, Issue 1–2, pp 315–330 | Cite as

Critical concentration of available soil phosphorus for grain yield and zinc nutrition of winter wheat in a zinc-deficient calcareous soil

  • Xiaoli Hui
  • Laichao Luo
  • Sen Wang
  • Hanbing Cao
  • Ming Huang
  • Mei Shi
  • Sukhdev S. Malhi
  • Zhaohui WangEmail author
Regular Article


Background and aims

The decrease in cereal grain zinc (Zn) caused by phosphorus (P) application has attracted wide attention. However, optimizing P fertilization for both satisfactory grain yield and grain Zn concentration is still a problem due to a poor understanding of the relationship between P application rates and available soil P, and that of available soil P and soil Zn availability, relevant soil factors, and plant Zn uptake and utilization.


A location-fixed field experiment was initiated in 2004 with winter wheat (Triticum aestivum L.) grown at five P rates of 0, 50, 100, 150, and 200 kg P2O5 ha−1, and soil and plant samples were collected during the three growing seasons of 2013–2016.


Winter wheat grain yield increased, and the grain Zn concentration decreased with increasing available soil P in a linear-plus-plateau manner. The grain yield plateau, averaging 6009 ± 155 kg ha−1, was reached at an available soil P concentration of 10.2 ± 2.5 mg kg−1, and the grain Zn plateau, averaging 22.4 ± 0.9 mg kg−1, was reached at an available soil P of 14.2 ± 1.8 mg kg−1. Shoot Zn uptake after flowering was not affected, while Zn remobilization from vegetative parts to grains and the Zn harvest index increased with P application at available soil P levels below 11.6 mg kg−1. The available soil Zn increased, and root mycorrhizal colonization was unaffected at lower available soil P levels.


The decrease in wheat grain Zn concentration with increasing P application at lower available soil P levels was primarily explained by yield dilution effects, not the changes in available soil Zn and root mycorrhizal colonization. Under the experimental conditions, the available soil P would have to be as low as 0.7 ± 0.4 mg kg−1 to achieve the target grain Zn concentration of 40 mg kg−1, and at this level, the grain yield would only be 4127 ± 252 kg ha−1.


Available soil P Available soil Zn Mycorrhizal colonization Grain Zn concentration Zn uptake and remobilization 



This research was supported by the National Key Research and Development Program of China (2018YFD0200401), the China Agricultural Research System (CARS-3), the Special Fund for Agro-scientific Research in the Public Interest (201303104), the Agricultural Scientific Research Talent and Team Program, and staffs and beamline 4W1B of the Beijing Synchrotron Radiation Facility, Institute of High Energy Physics, Chinese Academy of Sciences.

Supplementary material

11104_2019_4273_MOESM1_ESM.docx (139 kb)
ESM 1 (DOCX 139 kb)


  1. Alloway BJ (2009) Soil factors associated with zinc deficiency in crops and humans. Environ Geochem Health 31:537–548PubMedGoogle Scholar
  2. Bagci SA, Ekiz H, Yilmaz A, Cakmak I (2007) Effects of zinc deficiency and drought on grain yield of field-grown wheat cultivars in Central Anatolia. J Agron Crop Sci 193:198–206Google Scholar
  3. Bao SD (2000) Soil and agricultural chemistry analysis, second edn. China Agriculture Press, Beijing (in Chinese)Google Scholar
  4. Bohn L, Meyer AS, Rasmussen SK (2008) Phytate: impact on environment and human nutrition. A challenge for molecular breeding. J Zhejiang Univ Sci B 9:165–191PubMedPubMedCentralGoogle Scholar
  5. Bouain N, Shahzad Z, Rouached A, Khan GA, Berthomieu P, Abdelly C, Poirier Y, Rouached H (2014) Phosphate and zinc transport and signalling in plants: toward a better understanding of their homeostasis interaction. J Exp Bot 65:5725–5741PubMedGoogle Scholar
  6. Cakmak I (2008) Enrichment of cereal grains with zinc: agronomic or genetic biofortification? Plant Soil 302:1–17Google Scholar
  7. Cakmak I, Kutman UB (2017) Agronomic biofortification of cereals with zinc: a review. Eur J Soil Sci 69:172–180Google Scholar
  8. Cakmak I, McLaughlin MJ, White P (2017) Zinc for better crop production and human health. Plant Soil 411:1–4Google Scholar
  9. Chen XP, Zhang YQ, Tong YP, Xue YF, Liu DY, Zhang W, Deng Y, Meng QF, Yue SC, Yan P, Cui ZL, Shi XJ, Guo SW, Sun YX, Ye YL, Wang ZH, Jia LL, Ma WQ, He MR, Zhang XY, Kou CL, Li YT, Tan DS, Cakmak I, Zhang FS, Zou CQ (2017) Harvesting more grain zinc of wheat for human health. Sci Rep 7Google Scholar
  10. Chen XX, Zhang W, Wang Q, Liu YM, Liu DY, Zou CQ (2019) Zinc nutrition of wheat in response to application of phosphorus to a calcareous soil and an acid soil. Plant Soil 434:139–150Google Scholar
  11. Colomb B, Debaeke P, Jouany C, Nolot JM (2007) Phosphorus management in low input stockless cropping systems: crop and soil responses to contrasting P regimes in a 36-year experiment in southern France. Eur J Agron 26:154–165Google Scholar
  12. Deng Y, Feng G, Chen XP, Zou CQ (2017) Arbuscular mycorrhizal fungal colonization is considerable at optimal Olsen-P levels for maximized yields in an intensive wheat-maize cropping system. Field Crop Res 209:1–9Google Scholar
  13. Dwivedi RS, Randhawa NS, Bansal RL (1975) Phosphorus-zinc interaction. Plant Soil 43:639–648Google Scholar
  14. Escrig I, Morell I (1998) Effect of calciumon the soil adsorption of cadmium and zinc in some Spanish sandy soils. Water Air Soil Pollut 105:507–520Google Scholar
  15. García-Miragaya J, Dávalos M (1986) Sorption and desorption of Zn on ca-kaolinite. Water Air Soil Pollut 27:217–224Google Scholar
  16. 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 220:219–228Google Scholar
  17. Gregory PJ, Wahbi A, Adu-Gyamfi J, Heiling M, Gruber R, Joy EJM, Broadley MR (2017) Approaches to reduce zinc and iron deficits in food systems. Glob Food Secur 15:1–10Google Scholar
  18. Hernandez JD, Killorn R (2009) Phosphorus fertilizer by-product effect on the interaction of zinc and phosphorus in corn and soybean. Can J Soil Sci 89:189–196Google Scholar
  19. Huang TM, Huang QN, She X, Ma XL, Huang M, Cao HB, He G, Liu JS, Liang DL, Malhi SS, Wang ZH (2019) Grain zinc concentration and its relation to soil nutrient availability in different wheat cropping regions of China. Soil Tillage Res 191:57–65Google Scholar
  20. Jin JJ, Wang ZH, Dai J, Wang S, Gao YJ, Cao HB, Yu R (2014) Effects of long-term N and P fertilization with different rates on Zn concentration in grain of winter wheat. Plant Nutr Fert Sci 20:1358–1367 (in Chinese)Google Scholar
  21. Karami M, Afyuni M, Khoshgoftarmanesh AH, Papritz A, Schulin R (2009) Grain zinc, iron, and copper concentrations of wheat grown in Central Iran and their relationships with soil and climate variables. J Agric Food Chem 57:10876–10882PubMedGoogle Scholar
  22. Khan A, Lu GY, Ayaz M, Zhang HT, Wang RJ, Lv FL, Yang XY, Sun BH, Zhang SL (2018) Phosphorus efficiency, soil phosphorus dynamics and critical phosphorus level under long-term fertilization for single and double cropping systems. Agric Ecosyst Environ 256:1–11Google Scholar
  23. Kizilgoz I, Sakin E (2010) The effects of increased phosphorus application on shoot dry matter, shoot P and Zn concentrations in wheat (Triticum durum L.) and maize (Zea mays L.) grown in a calcareous soil. Afr J Biotechnol 9:5893–5896Google Scholar
  24. 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 342:149–164Google Scholar
  25. Lambert R, Grant C, Sauvé S (2007) Cadmium and zinc in soil solution extracts following the application of phosphate fertilizers. Sci Total Environ 378:293–305PubMedGoogle Scholar
  26. Li HY, Wang SX, Li M, Tian XH, Zhao AQ, Guo CH (2014) Effects of combined foliar Zn application with N and P under different water and nitrogen managements on Zn nutritional quality of winter wheat. Sci Agric Sin 47:4016–4026 (in Chinese)Google Scholar
  27. Li MH, Yu R, Yang YE, Wang ZH (2016) Effects of soil moisture on wheat grain yield and zinc utilization in zinc-deficient dryland soil. Plant Nutr Fert Sci 22:388–394 (in Chinese)Google Scholar
  28. Lindsay WL (1979) Chemical equilibria in soils. Clay Miner 28:319–319Google Scholar
  29. Liu H, Wang ZH, Li FC, Li KY, Yang N, Yang YE, Huang DL, Liang DL, Zhao HB, Mao H, Liu JS, Qiu WH (2014) Grain iron and zinc concentrations of wheat and their relationships to yield in major wheat production areas in China. Field Crops Res 156:151–160Google Scholar
  30. Ma JC, He P, Xu XP, He WT, Liu YX, Yang FQ, Chen F, Li ST, Tu SH, Jin JY, Johnston AM, Zhou W (2016) Temporal and spatial changes in soil available phosphorus in China (1990-2012). Field Crops Res 192:13–20Google Scholar
  31. Ma QX, Wang ZH, Hui XL, Zhang X, Zhang YY, Hou SB, Huang N, Luo LC, Zhang SJ, Dang HY (2019a) Optimization of phosphorus rate and soil available phosphorus based on grain yield and nutrient contents in dryland wheat production. Sci Agric Sin 52:73–85 (in Chinese)Google Scholar
  32. Ma XN, Luo WQ, Li J, Wu FY (2019b) Arbuscular mycorrhizal fungi increase both concentrations and bioavilability of Zn in wheat (Triticum aestivum L.) grain on Zn-spiked soils. Appl Soil Ecol 135:91–97Google Scholar
  33. MacDonald GK, Bennett EM, Potter PA, Ramankutty N (2011) Agronomic phosphorus imbalances across the world's croplands. Proc Natl Acad of Sci USA 108:3086–3091Google Scholar
  34. Mai WX, Tian XH, Lu XC, Yang XW (2011) Effect of Zn and P supply on grain Zn bioavailability in wheat. Chin J Eco-Agric 19:1243–1249 (in Chinese)Google Scholar
  35. Mandal B, Mandal LN (1990) Effect of phosphorus application on transformation of zinc fraction in soil and on the zinc nutrition of lowland rice. Plant Soil 121:115–123Google Scholar
  36. Marschner P (2012) Marschner's mineral nutrition of higher plants. Academic Press, San DiegoGoogle Scholar
  37. Mattigod SV, Sposito G (1977) Estimated association constants for some complexes of trace metals with inorganic ligands. Soil Sci Soc Am J 41:1092–1097Google Scholar
  38. National Bureau of Statistics of China (NBS) (2016) China statistical yearbook [Online]. Available: [23 November 2017]
  39. Nikolic M, Nikolic N, Kostic L, Pavlovic J, Bosnic P, Stevic N, Savic J, Hristov N (2016) The assessment of soil availability and wheat grain status of zinc and iron in Serbia: implications for human nutrition. Sci Total Environ 553:141–148PubMedGoogle Scholar
  40. Ova EA, Kutman UB, Ozturk L, Cakmak I (2015) High phosphorus supply reduced zinc concentration of wheat in native soil but not in autoclaved soil or nutrient solution. Plant Soil 393:147–162Google Scholar
  41. Pellegrino E, Öpik M, Bonari E, Ercoli L (2015) Responses of wheat to arbuscular mycorrhizal fungi: a meta-analysis of field studies from 1975 to 2013. Soil Biol Biochem 84:210–217Google Scholar
  42. Pérez-Novo C, Bermúdez-Couso A, López-Periago E, Fernández-Calviño D, Arias-Estévez M (2011) Zinc adsorption in acid soils : influence of phosphate. Geoderma 162:358–364Google Scholar
  43. Poulton PR, Johnston AE, White RP (2013) Plant-available soil phosphorus. Part I: the response of winter wheat and spring barley to Olsen P on a silty clay loam. Soil Use Manag 29:4–11Google Scholar
  44. Rahman MA, Jahiruddin M, Islam MR (2007) Critical limit of zinc for rice in calcareous soils. J Agric Rural Dev 5:43–47Google Scholar
  45. Reeve JR, Endelman JB, Miller BE, Hole DJ (2012) Residual effects of compost on soil quality and dryland wheat yield sixteen years after compost application. Soil Sci Soc Am J 76:278–285Google Scholar
  46. Rezapour S (2014) Effect of sulfur and composted manure on SO-S, P and micronutrient availability in a calcareous saline-sodic soil. Chem Ecol 30:147–155Google Scholar
  47. Riley D, Barber SA (1971) Effect of ammonium and nitrate fertilization on phosphorus uptake as related to root-induced pH changes at the root-soil interface. Soil Sci Soc Am J 35:301–306Google Scholar
  48. 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 250:225–239Google Scholar
  49. Ryan MH, Mcinerney JK, Record IR, Angus JF (2008) Zinc bioavailability in wheat grain in relation to phosphorus fertiliser, crop sequence and mycorrhizal fungi. J Sci Food Agric 88:1208–1216Google Scholar
  50. Sacristan D, Gonzalez-Guzman A, Barron V, Torrent J, Del Campillo MC (2019) Phosphorus-induced zinc deficiency in wheat pot-grown on noncalcareous and calcareous soils of different properties. Arch Agron Soil Sci 65:208–223Google Scholar
  51. Sánchez-Rodríguez AR, Del Campillo MC, Torrent J (2017) Phosphorus reduces the zinc concentration in cereals pot-grown on calcareous Vertisols from southern Spain. J Sci Food Agric 97:3427–3432PubMedGoogle Scholar
  52. Singh JP, Karamanos RE, Stewart JWB (1988) The mechanism of phosphorus-induced zinc deficiency in bean (Phaseolus vulgaris L.). Can J Soil Sci 68:345–358Google Scholar
  53. Singh J, Brar BS, Sekhon BS, Mavi MS, Singh G, Kaur G (2016) Impact of long-term phosphorous fertilization on Olsen-P and grain yields in maize-wheat cropping sequence. Nutr Cycl Agroecosyst 106:157–168Google Scholar
  54. Srivastava PC, Bhatt M, Pachauri SP, Tyagi AK (2014) Effect of zinc application methods on apparent utilization efficiency of zinc and phosphorus fertilizers under basmati rice-wheat rotation. Arch Agron Soil Sci 60:33–48Google Scholar
  55. Stomph TJ, Choi EY, Stangoulis JCR (2011) Temporal dynamics in wheat grain zinc distribution: is sink limitation the key? Ann Bot 107:927–937PubMedPubMedCentralGoogle Scholar
  56. Su D, Zhou LJ, Zhao Q, Pan G, Cheng FM (2018) Different phosphorus supplies altered the accumulations and quantitative distributions of phytic acid, zinc, and iron in rice (Oryza sativa L.) grains. J Agric Food Chem 66:1601–1611PubMedGoogle Scholar
  57. Tang X, Ma YB, Hao XY, Li XY, Li JM, Huang SM, Yang XY (2009) Determining critical values of soil Olsen-P for maize and winter wheat from long-term experiments in China. Plant Soil 323:143–151Google Scholar
  58. Tang HL, Li XQ, Zu C, Zhang FS, Shen JB (2013) Spatial distribution and expression of intracellular and extracellular acid phosphatases of cluster roots at different developmental stages in white lupin. J Plant Physiol 15:1243–1250Google Scholar
  59. Trouvelot A, Kough JL, Gianinazzipearson V (1986) Mesure du taux de mycorhization VA d'un systeme radiculaire. Recherche de methodes d'estimation ayant une signification fonctionnelle. Mycorrhizae: Physiol Genet:217–221Google Scholar
  60. Wang S, Wang ZH, Li SS, Diao CP, Liu L, Hui XL, Huang M, Luo LC, He G, Cao HB, Yu R, Malhi SS (2018) Identification of high-yield and high-Zn wheat cultivars for overcoming “yield dilution” in dryland cultivation. Eur J Agron 101:57–62Google Scholar
  61. Wei XR, Hao MD, Shao MA, Gale WJ (2006) Changes in soil properties and the availability of soil micronutrients after 18 years of cropping and fertilization. Soil Tillage Res 91:120–130Google Scholar
  62. White PJ, Broadley MR (2009) Biofortification of crops with seven mineral elements often lacking in human diets-iron, zinc, copper, calcium, magnesium, selenium and iodine. New Phytol 182:49–84Google Scholar
  63. White PJ, George TS, Hammond JP, James EK (2014) Improving crop mineral nutrition. Plant Soil 384:1–5Google Scholar
  64. Zadoks JC, Chang TT, Konzak CF (1974) A decimal code for the growth stages of cereals. Weed Res 14:415–421Google Scholar
  65. 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 361:143–152Google Scholar
  66. Zhang YQ, Wen MX, Li XP, Shi XJ (2014) Long-term fertilisation causes excess supply and loss of phosphorus in purple paddy soil. J Sci Food Agric 94:1175–1183PubMedGoogle Scholar
  67. Zhang W, Liu DY, Li C, Cui ZL, Chen XP, Russell Y, Zou CQ (2015) Zinc accumulation and remobilization in winter wheat as affected by phosphorus application. Field Crops Res 184:155–161Google Scholar
  68. Zhang W, Liu DY, Liu YM, Cui ZL, Chen XP, Zou CQ (2016) Zinc uptake and accumulation in winter wheat relative to changes in root morphology and mycorrhizal colonization following varying phosphorus application on calcareous soil. Field Crops Res 197:74–82Google Scholar
  69. Zhang T, Sun HD, Lv ZY, Cui LL, Mao H, Kopittke PM (2017) Using synchrotron-based approaches to examine the foliar application of ZnSO4 and ZnO nanoparticles for field-grown winter wheat. J Agric Food Chem 66:2572–2579PubMedGoogle Scholar
  70. Zheng SJ, Yang ZM, Hu AT (1999) Study on the cell nutrition of phosphorus and zinc interaction in corn and wheat. Plant Nutr Fert Sci 5:150–155 (in Chinese)Google Scholar
  71. 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, Yaqub Mujahid M, Joshi AK, Zelenskiy Y, Zhang FS, Cakmak I (2012) Biofortification of wheat with zinc through zinc fertilization in seven countries. Plant Soil 361:119–130Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Xiaoli Hui
    • 1
    • 2
  • Laichao Luo
    • 3
  • Sen Wang
    • 1
    • 2
  • Hanbing Cao
    • 1
    • 2
  • Ming Huang
    • 4
  • Mei Shi
    • 1
    • 2
  • Sukhdev S. Malhi
    • 5
  • Zhaohui Wang
    • 1
    • 2
    Email author
  1. 1.State Key Laboratory of Crop Stress Biology in Arid AreasNorthwest A&F UniversityYanglingChina
  2. 2.Key Laboratory of Plant Nutrition and Agri-environment in Northwest China, Ministry of Agriculture, College of Natural Resources and EnvironmentNorthwest A&F UniversityYanglingChina
  3. 3.Anhui Province Key Lab of Farmland Ecological Conservation and Pollution Prevention, School of Resources and EnvironmentAnhui Agricultural UniversityHefeiChina
  4. 4.College of AgricultureHenan University of Science and TechnologyLuoyangChina
  5. 5.Department of Renewable ResourcesUniversity of AlbertaEdmontonCanada

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