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Acta Agronomica Sinica ›› 2020, Vol. 46 ›› Issue (02): 228-237.doi: 10.3724/SP.J.1006.2020.92032

• TILLAGE & CULTIVATION · PHYSIOLOGY & BIOCHEMISTRY • Previous Articles     Next Articles

Influence of phosphorus on rice (Oryza sativa L.) grain zinc bioavailability and its relation to inositol phosphate profiles concentration

SU Da1,2,WU Liang-Quan2,K. Rasmussen Søren3,ZHOU Lu-Jian4,PAN Gang4,CHENG Fang-Min4,*()   

  1. 1 Key Laboratory of Ministry of Education for Genetics, Breeding and Multiple Utilization of Crops / College of Agriculture, Fujian Agriculture and Forestry University, Fuzhou 350002, Fujian, China
    2 International Magnesium Institute, Fuzhou 350002, Fujian, China
    3 Department of Plant and Environmental Sciences, Section of Plant and Soil Science, University of Copenhagen, Copenhagen, Denmark
    4 College of Agriculture and Biotechnology, Zhejiang University, Hangzhou 310058, Zhejiang, China
  • Received:2019-06-03 Accepted:2019-08-09 Online:2020-02-12 Published:2019-09-10
  • Contact: Fang-Min CHENG E-mail:chengfm@zju.edu.cn
  • Supported by:
    This study was supported by the National Key Research and Development Project(2016YFD0300502);the National Natural Science Foundation of China(31571602);the Fujian Province Natural Science(2019J01374);the Education and Scientific Research Project for Middle-aged and the Young Teachers in Fujian Province(JAT170156);the Foundation for China Scholarship Council

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Abstract:

The hidden hunger caused by grain zinc (Zn) deficiency in crop poses a potential threat to the health of nearly two billion people worldwide, especially in developing countries. In this study, the long-term phosphorus fertilizer experiment and in vitro detached rice panicle culture systems with varied phosphorus levels were conducted to investigate the effect of phosphorus on rice grain Zn bioavailability and its relation of grain inositol phosphates profiles (phytic acid related metabolic derivatives) concentration. In our results, compared with low phosphorus level, high phosphorus supply increased grain phytic acid phosphorus and total phosphorus concentration (mg g -1). Moreover, high phosphorus supply also increased different grain inositol phosphate profile concentrations (InsP1-6), especially for InsP4-6. On the contrary, grain Zn concentration decreased with phosphorus supply. Both the decrement of Zn and increment of phytic acid phosphorus induced by the higher phosphorus supply in rice grain led to the significant decrement of grain Zn bioavailability. In in vitro detached panicle culture system, the Zn bioavailability in P12 treatment decreased by 81.3% relative to P0 treatment. In conclusion, higher phosphorus input could significantly decrease grain Zn bioavailability through increased grain phytic acid phosphorus and inositol phosphates derivatives concentration, in addition to the decrement of grain Zn concentration.

Key words: phosphorus, phytic acid, zinc bioavailability, inositol phosphate, rice quality

Fig. 1

Differences in PAP, Total P concentration (mg g-1), and PAP/total P among various phosphorus fertilizer levels in field experiment Bars indicated by the same letter among treatments are not significantly different at the 0.05 probability level. LP, MP, HP mean the low phosphorus level, medium phosphorus level, and high phosphorus level. PAP: phytic acid-phosphorus; Total P: total phosphorus; PAP/total P: phytic acid-phosphorus/total phosphorus."

Fig. 2

Effects of different phosphorus levels on grain Zn, Fe, Mn, and Cu concentrations and Zn bioavailability (TAZ) (field phosphorus fertilizer experiment) Bars indicated by the same letter among treatments are not significantly different at the 0.05 probability level. LP, MP, HP mean the low phosphorus level, medium phosphorus level, and high phosphorus level, respectively. TAZ represents Zn bioavailability."

Fig. 3

Effects of different phosphorus levels on grain PAP, total P concentration, and the ratio of PAP to total P (detached panicle culture experiment) Bars indicated by the same letter among treatments are not significant at the 0.05 probability level. P0, P1, P3, P6, P12 mean the P (NaH2PO4·2H2O ) levels of 0, 1, 3, 6, and 12 mmol L-1, respectively. PAP, total P, PAP/total P mean phytic acid-phosphorus, total phosphorus, and phytic acid-phosphorus/total phosphorus, respectively."

Fig. 4

Effect of exogenous phosphorus treatments on grain P distributions in brown rice in detached panicle culture experiment (scanning electron microscopic images of brown rice with 5000 ×; scale bars are 100 μm) A, B, C represent P0, P3, and P12 treatments, respectively."

Fig. 5

Effects of different phosphorus levels on grain inositol phosphate (InsP1-6) concentrations (detached panicle culture experiment) P0, P1, P3, P6, P12 mean the P (NaH2PO4·2H2O) levels of 0, 1, 3, 6, and 12 mmol L-1, respectively."

Fig. 6

Ratio of inositol phosphate composition/total inositol phosphate in different exogenous phosphorus treatment (detached panicle culture experiment) A: P0; B: P1; C: P3; D: P6; E: P12."

Fig. 7

Effect of exogenous phosphorus treatment on grain Zn distributions in detached panicle culture experiment (scanning electron microscopic images of brown rice with 5000 ×; scale bars are 100 μm) A, B, C represent P0, P3, and P12 treatment, respectively."

Fig. 8

Effects of different phosphorus levels on grain Zn concentration and its bioavailability (TAZ) (detached panicle culture experiment) Bars indicated by the same letter among treatments are not significant at the 0.05 probability level. P0, P1, P3, P6, P12 mean the P (NaH2PO4·2H2O) levels of 0, 1, 3, 6, and 12 mmol L-1, respectively. TAZ: Zn bio-availability."

Fig. 9

Correlation of grain phosphorus components and Zn bioavailability under P treatment (left: heatmap of field phosphorus fertilizer experiment; right: correlation in both field and detached rice panicle culture systems) PAP: phytic acid phosphours; TP: total phosphours; TAF: Zn bio-availabiity. ** P < 0.01."

[1] Noulas C, Tziouvalekas M, Karyotis T . Zinc in soils, water and food crops. J Trace Elem Med Biol, 2018,49:252-260.
doi: 10.1016/j.jtemb.2018.02.009 pmid: 29472130
[2] Hefferon K . Biotechnological approaches for generating zinc-enriched crops to combat malnutrition. Nutrients, 2019,11:253.
doi: 10.1186/1471-2148-11-253 pmid: 21917168
[3] Maqbool M A, Beshir A . Zinc biofortification of maize (Zea mays L.): Status and challenges. Plant Breed, 2019,138:1-28.
doi: 10.1111/pbr.2019.138.issue-1
[4] Jaksomsak P, Tuiwong P, Rerkasem B, Guild G E, Palmer L J, Stangoulis J C, Promuthai C . The impact of foliar applied zinc fertilizer on zinc and phytate accumulation in dorsal and ventral grain sections of four Thai rice varieties with different grain zinc. J Cereal Sci, 2018,79:6-12.
doi: 10.1016/j.jcs.2017.09.004
[5] Li W, Huang J, Zhao H, Tan Y, Cui H, Poirier Y, Shu Q . Production of low phytic acid rice by hairpin RNA- and artificial microRNA-mediated silencing ofOsMIK in seeds. Plant Cell Tissue Organ Cult, 2014,119:15-25.
doi: 10.1007/s11240-014-0510-8
[6] Liang J, Li Z, Tsuji K, Nakano K, Nout M J R, Hamer R J . Milling characteristics and distribution of phytic acid and zinc in long-, medium- and short-grain rice. J Cereal Sci, 2008,48:83-91.
doi: 10.1016/j.jcs.2007.08.003
[7] Perera I, Seneweera S, Hirotsu N . Manipulating the phytic acid content of rice grain toward improving micronutrient bioavailability. Rice, 2018,11:4.
doi: 10.1186/s12284-018-0200-y pmid: 29327163
[8] Julia C, Wissuwa M, Kretzschmar T, Jeong K, Rose T J . Phosphorus uptake, partitioning and redistribution during grain filling in rice. Ann Bot-london, 2016,118:1151-1162.
doi: 10.1093/aob/mcw164 pmid: 27590335
[9] Ova E A, Kutman U B, Ozturk L, Cakmak I . High phosphorus supply reduced zinc concentration of wheat in native soil but not in autoclaved soil or nutrient solution. Plant Soil, 2015,393:147-162.
doi: 10.5696/2156-9614-9.24.191212 pmid: 31893173
[10] Saneoka H, Koba T . Plant growth and phytic acid accumulation in grain as affected by phosphorus application in maize (Zea mays L.). Grassl Sci, 2003,48:485-489.
[11] Miller G A, Youngs V L . Environmental and cultivar effects on oat phytic acid concentration. Cereal Chem, 1980,57:189-191.
[12] Raboy V, Dickinson D B . Effect of phosphorus and zinc nutrition on soybean seed phytic acid and zinc. Plant Physiol, 1984,75:1094-1098.
doi: 10.1104/pp.75.4.1094 pmid: 16663741
[13] Noack S R, Mclaughlin M J, Smernik R J, Mcbeath T M, Armstrong R . Phosphorus speciation in mature wheat and canola plants as affected by phosphorus supply. Plant Soil, 2014,378:125-137.
doi: 10.1007/s11104-013-2015-3
[14] Su D, Zhou L J, Zhao Q, Pan G, Cheng F M . 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, 2018,66:1601-1611.
doi: 10.1021/acs.jafc.7b04883 pmid: 29401375
[15] Raboy V . Seeds for a better future: ‘low phytate’, grains help to overcome malnutrition and reduce pollution. Trends Plant Sci, 2001,6:458-462.
doi: 10.1016/s1360-1385(01)02104-5 pmid: 11590064
[16] Zhang W, Liu D, Liu Y, Chen X, Zou C . Overuse of phosphorus fertilizer reduces the grain and flour protein contents and zinc bioavailability of winter wheat (Triticum aestivum L.). J Agric Food Chem, 2017,65:1473-1482.
doi: 10.1021/acs.jafc.6b04778 pmid: 28171726
[17] Imran M, Rehim A, Sarwar N, Hussain S . Zinc bioavailability in maize grains in response of phosphorous-zinc interaction. J Plant Nutr Soil Sc, 2016,179:60-66.
doi: 10.1002/jpln.v179.1
[18] Liu Z H, Cheng F M, Cheng W D, Zhang G P . Positional variations in phytic acid and protein content within a panicle ofjaponica rice. J Cereal Sci, 2005,41:297-303.
doi: 10.1016/j.jcs.2004.09.010
[19] Bi J, Liu Z, Lin Z, Alim M A, Li G, Wang S H, Ding Y F . Phosphorus accumulation in grains ofjaponica rice as affected by nitrogen fertilizer. Plant Soil, 2013,369:231-240.
doi: 10.1007/s11104-012-1561-4
[20] Wilcox J R, Premachandra G S, Young K A, Raboy V . Isolation of high seed inorganic P, low-phytate soybean mutants. Crop Sci, 2000,40:1601-1605.
doi: 10.2135/cropsci2000.4061601x
[21] Zhou L, Ye Y, Zhao Q, Du X, Zakari S A, Su D, Pan G, Chen F M . Suppression of ROS generation mediated by higher InsP3 level is critical for the delay of seed germination in lpa rice. Plant Growth Regul, 2018,85:411-424.
doi: 10.1007/s10725-018-0402-8
[22] Wei Y Y, Shohag M, Wang Y Y, Lu L L, Wu C Y, Yang X . Effect of zinc sulfate fortification in germinated brown rice on seed zinc concentration, bioavailability, and seed germination. J Agric Food Chem, 2012,60:1871-1879.
doi: 10.1021/jf205025b pmid: 22273463
[23] Miller L V, Krebs N F, Hambidge K M . A mathematical model of zinc absorption in humans as a function of dietary zinc and phytate. J Nutr, 2007,137:135-141.
doi: 10.1093/jn/137.1.135 pmid: 17182814
[24] Brombach C, Manorut P, Kolambage-Dona P P P, Ezzeldin M F, Chen B, Corns W T, Feldmann J, Krupp E M . Methylmercury varies more than one order of magnitude in commercial European rice. Food Chem, 2017,214:360-365.
doi: 10.1016/j.foodchem.2016.07.064 pmid: 27507486
[25] 戴云云, 丁艳锋, 刘正辉, 王强盛, 李刚华, 王绍华 . 花后水稻穗部夜间远红外增温处理对稻米品质的影响. 中国水稻科学, 2009,23:414-420.
doi: 10.3969/j.issn.1001-7216.2009.04.12
Dai Y Y, Ding Y F, Liu Z H, Wang Q S, Li G H, Wang S H . Effects of elevated night temperature by far-infrared radiation at grain filling on grain quality of rice. Chin J Rice Sci, 2009,23:414-420 (in Chinese with English abstract).
doi: 10.3969/j.issn.1001-7216.2009.04.12
[26] Coelho C M M, Santos J C P, Tsai S M, Vitorello V A V C . Seed phytate content and phosphorus uptake and distribution in dry bean genotypes. Braz J Plant Physiol, 2002,14:51-58.
doi: 10.1590/S1677-04202002000100007
[27] Sompong U, Somta P, Raboy V, Srinives P . Mapping of quantitative trait loci for phytic acid and phosphorus contents in seed and seedling of mungbean [Vigna radiata(L.) Wilczek]. Breed Sci, 2012,62:87-92.
doi: 10.1270/jsbbs.62.87 pmid: 23136518
[28] Taliman N A, Dong Q, Echigo K, Raboy V, Saneoka H . Effect of phosphorus fertilization on the growth, photosynthesis, nitrogen fixation, mineral accumulation, seed yield, and seed quality of a soybean low-phytate line. Plants, 2019,8:119.
doi: 10.3390/plants8050119 pmid: 31071932
[29] Park M, Singvilay O, Shin W, Kim E, Chung J, Sa T . Effects of long-term compost and fertilizer application on soil phosphorus status under paddy cropping system. Commun Soil Sci Plan, 2004,35:1635-1644.
doi: 10.1081/CSS-120038559
[30] Zhang W, Liu D, Li C, Cui Z, Chen X, Russell Y, Zou C . Zinc accumulation and remobilization in winter wheat as affected by phosphorus application. Field Crops Res, 2015,184:155-161.
doi: 10.1016/j.fcr.2015.10.002
[31] Zhang J, Wu L H, Wang M Y . Iron and zinc biofortification in polished rice and accumulation in rice plant (Oryza sativa L.) as affected by nitrogen fertilization. Acta Agric Scand B-S P, 2008,58:267-272.
[32] Xue Y F, Yue S C, Zhang Y Q, Cui Z, Chen X, Yang F, Cakmak I, McGrath S P, Zhang F S, Zou C Q, . Grain and shoot zinc accumulation in winter wheat affected by nitrogen management. Plant Soil, 2012,361:153-163.
doi: 10.1007/s11104-012-1510-2
[33] Kutman U B, Yildiz B, Cakmak I . Effect of nitrogen on uptake, remobilization and partitioning of zinc and iron throughout the development of durum wheat. Plant Soil, 2011,342:149-164.
doi: 10.1007/s11104-010-0679-5
[34] Bolland M D A . Residual value of superphosphate and Queensland rock phosphate measured using yields of serradella, burr medic and subterranean clover grown in rotation with wheat and bicarbonate-extractable soil phosphorus. Commun Soil Sci Plan, 1993,24:1243-1269.
doi: 10.1080/00103629309368874
[35] Orabi A A, Mashadi H, Abdallah A, Morsy M F . Effect of zinc and phosphorus on the grain yield of corn (Zea mays L.) grown on a calcareous soil. Plant Soil, 1981,63:291-294.
doi: 10.1007/BF02374607
[36] Zhang Y, Deng Y, Chen R, Cui Z L, Chen X P, Yost R, Zhang F S, Zou C Q . The reduction in zinc concentration of wheat grain upon increased phosphorus-fertilization and its mitigation by foliar zinc application. Plant Soil, 2012,361:143-152.
doi: 10.1007/s11104-012-1238-z
[37] Liang J, Han B, Nout M J, Hamer R J . Effects of soaking, germination and fermentation on phytic acid, total and in vitro soluble zinc in brown rice. Food Chem, 2008,110:821-828.
doi: 10.1016/j.foodchem.2008.02.064 pmid: 26047266
[38] Bohn L, Josefsen L, Meyer A A, Rasmussen S K . Quantitative analysis of phytate globoids isolated from wheat bran and characterization of their sequential dephosphorylation by wheat phytase. J Agr Food Chem, 2007,55:7547-7552.
doi: 10.1021/jf071191t pmid: 17696444
[39] 苏达, 吴良泉, Søren K R, 周庐建, 程方民 . 低植酸水稻种质资源筛选、遗传生理调控与环境生态适应性研究进展. 中国水稻科学, 2019,33:95-107.
Su D, Wu L Q, Søren K R, Zhou L J, Cheng F M . Research advances on the low phytic acid rice breeding and their genetic physiological regulation and environmental adaptability. Chin J Rice Sci, 2019,33:95-107 (in Chinese with English abstract).
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