1,969
Views
80
CrossRef citations to date
0
Altmetric
Review Article

Zinc biofortification in rice: leveraging agriculture to moderate hidden hunger in developing countries

, , , , , , , & show all
Pages 147-161 | Received 20 Nov 2016, Accepted 31 May 2017, Published online: 12 Jun 2017

References

  • Arrivault S, Senger T, Krämer U. 2006. The Arabidopsis metal tolerance protein AtMTP3 maintains metal homeostasis by mediating Zn exclusion from the shoot under Fe deficiency and Zn over supply. Plant J. 46:861–879.
  • Axelsen KB, Palmgren MG. 2001. Inventory of the superfamily of P-type ion pumps in Arabidopsis. Plant Physiol. 126:696–706.
  • Begum MC, Islam M, Sarkar MR, Azad MAS, Huda AN, Kabir AH. 2016. Auxin signaling is closely associated with Zn-efficiency in rice (Oryza sativa L.). J Plant Interact. 11:124–129.
  • Behera SK, Shukla AK, Singh MV, Wanjari RH, Singh P. 2015. Yield and zinc, copper, manganese and iron concentration in maize (Zea mays L.) grown on vertisol as influenced by zinc application from various zinc fertilizers. J Plant Nutr. 38:1544–1557.
  • Benedicto A, Hernández-Apaolaza L, Rivas I, Lucena JJ. 2011. Determination of 67Zn distribution in navy bean (Phaseolus vulgaris L.) after foliar application of 67Zn–lignosulfonates using isotope pattern deconvolution. J Agricult Food Chem. 59:8829–8838.
  • Broadley MR, White PJ, Hammond JP, Zelko I, Lux A. 2007. Zn in plants. New Phytol. 173:677–702.
  • Cakmak I, Torun A, Millet E, Feldman M, Fahima T, Korol A, Nevo E, Braun HJ, Özkan H. 2004. Triticum dicoccoides: an important genetic resource for increasing zinc and iron concentration in modern cultivated wheat. Soil Sci Plant Nutr. 50:1047–1054.
  • Cakmak I. 2000. Role of Zn in protecting plant cells from reactive oxygen species. New Phytol. 146:185–205.
  • Cakmak I. 2008a. Zinc deficiency in wheat in Turkey. In: Alloway BJ, editor. Micronutrient deficiencies in global crop production. Dordrecht: Springer; p. 181–200.
  • Cakmak I. 2008b. Enrichment of cereal grains with zinc: agronomic or genetic biofortification? Plant Soil. 302:1–17.
  • Cakmak I, Pfeiffer WH, McClafferty B. 2010. Review: biofortification of durum wheat with zinc and iron. Cereal Chem. 87:10–20.
  • Chand M, Randhawa NS, Bhumbla DR. 1981. Effectiveness of zinc chelates in zinc nutrition of greenhouse rice crop in a saline-sodic soil. Plant Soil. 59:217–225.
  • Chang H-B, Lin C-W, Huang H-J. 2005. Zinc-induced cell death in rice (Oryza sativa L.) roots. Plant Growth Regul. 46:261–266.
  • Chen W, He ZL, Yang X, Feng Y. 2009. Zinc efficiency is correlated with root morphology, ultrastructure, and antioxidative enzymes in rice. J Plant Nutr. 32:287–305.
  • Chen WR, Feng Y, Chao YE. 2008. Genomic analysis and expression pattern of OsZIP1, OsZIP3, and OsZIP4 in two rice (Oryza sativa L.) genotypes with different zinc efficiency. Russ J Plant Physiol. 55:400–409.
  • Chen Y, Cui J, Tian X, Zhao A, Li M, Wang S, Li X, Jia Z, Liu K. 2017. Effect of straw amendment on soil Zn availability and ageing of exogenous water-soluble Zn applied to calcareous soil. PLoS ONE. 12:e0169776.
  • De Valença AW, Bake A, Brouwer ID, Giller KE. 2017. Agronomic biofortification of crops to fight hidden hunger in sub-Saharan Africa. Glob Food Sec. 12:8–14.
  • Distelfeld A, Cakmak I, Peleg Z, Ozturk L, Yazici AM, Budak H, Saranga Y, Fahima T. 2007. Multiple QTL-effects of wheat Gpc-B1 locus on grain protein and micronutrient concentrations. Plant Physiol. 129:635–643.
  • Dobermann A, Fairhurst T. 2000. Rice: nutrient disorders & nutrient management. Singapore: Potash and Phosphate Institute, PPI of Canada and International Rice Research Institute; p. 192.
  • Drakakaki G, Marcel S, Glahn RP, Lund EK, Pariagh S, Fischer R, Christou P, Stoger E. 2005. Endosperm specific co-expression of recombinant soybean ferritin and Aspergillus phytase in maize results in significant increases in the levels of bioavailable iron. Plant Mol Biol. 59:869–880.
  • Eide DJ. 2006. Zinc transporters and the cellular trafficking of zinc. Biochim Biophys Acta. 1763:711–722.
  • Farooq M, Wahid A, Siddique KHM. 2012. Micronutrient application through seed treatments: a review. J Soil Sci Plant Nutr. 12:125–142.
  • Gao X, Hoffland E, Stomph T, Grant CA, Zou C, Zhang F. 2012. Improving zinc bioavailability in transition from flooded to aerobic rice. A review. Agron Sustain Dev. 32:465–478.
  • Gao X, Zhang F, Hoffland E. 2009. Malate exudation by six aerobic rice genotypes varying in zinc uptake efficiency. J Environ Qual. 38:2315–2321.
  • Gao X, Zou C, Fan X, Zhang F, Hoffland E. 2006. From flooded to aerobic conditions in rice cultivation: consequences for zinc uptake. Plant Soil. 280:41–47.
  • Gao XP, Kuyper TW, Zou CQ, Zhang FS, Hoffland E. 2007. Mycorrhizal responsiveness of aerobic rice genotypes is negatively correlated with their zinc uptake when nonmycorrhizal. Plant Soil. 290:283–291.
  • Genc Y, Shepherd KW, McDonald GK, Graham RD, Leon J. 2003. Inheritance of tolerance to zinc deficiency in barley. Plant Breed. 122:283–284.
  • Gharib AG, Mohseni SG, Mohajer M, Gharib M. 2006. Bioavailability of essential trace elements in the presence of phytate, fiber and calcium. J Radioanal Nuclear Chem. 270:209–215.
  • Gibson RS. 2006. Zinc: the missing link in combating micronutrient malnutrition in developing countries. Proc Nutr Soc. 65:51–60.
  • Gibson RS. 2007. The role of diet- and host-related factors in nutrient bioavailability and thus in nutrient-based dietary requirement estimates. Food Nutr Bull. 28:77–100.
  • Gomez-Coronado F, Poblaciones MJ, Almeida AS, Cakmak I. 2016. Zinc (Zn) concentration of bread wheat grown under Mediterranean conditions as affected by genotype and soil/foliar Zn application. Plant Soil. 401:331–346.
  • Guerinot ML. 2000. The ZIP family of metal transporters. Biochim Biophys Acta. 1465:190–198.
  • Guo JX, Feng XM, Hu XY, Tian GL, Ling N, Wang JH, Shen QR, Guo SW. 2016. Effects of soil zinc availability, nitrogen fertilizer rate and zinc fertilizer application method on zinc biofortification of rice. J Agricul Sci. 154:584–597.
  • Hatch MD, Slack CR. 1970. Photosynthetic CO2 fixation pathways. Annu Rev Plant Physiol. 21:141–162.
  • Haydon MJ, Cobbett CS. 2007. A novel major facilitator superfamily protein at the tonoplast influences zinc tolerance and accumulation in Arabidopsis. Plant Physiol. 143:1705–1719.
  • Hippler FWR, Boaretto RM, Quaggio JA, Boaretto AE, Abreu-Junior CH, Mattos JD. 2015. Uptake and distribution of soil applied zinc by citrus trees—addressing fertilizer use efficiency with 68Zn labeling. PLoS ONE. 10:e0116903.
  • Hotz C, Brown KH. 2004. International Zn nutrition consultative group technical document #1. Assessment of the risk of Zn deficiency in populations and options for its control. International nutrition foundation for UNU. Food and Nutr Bull. 25:91–204.
  • 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.
  • Impa SM, Morete MJ, Ismail AM, Schulin R, Johnson-Beebout SE. 2013. Zn uptake, translocation, and grain Zn loading in rice (Oryza sativa L.) genotypes selected for Zn deficiency tolerance and high grain Zn. J Exp Bot. 64:2739–2751.
  • Ishimaru Y, Suzuki M, Kobayashi T, Takahashi M, Nakanishi H, Mori S, Nishizawa NK. 2005. OsZIP4, a novel Zn-regulated Zn transporter in rice. J Exp Bot. 56:3207–3214.
  • Jan M, Anwar-ul-Haq M, Tanveer-ul-Haq AA, Wariach EA. 2016. Evaluation of soil and foliar applied Zn sources on rice (Oryza sativa L.) genotypes in saline environments. Int J Agricul Biol. 18:643–648.
  • Jiang W, Struik PC, Lingna J, van-Keulen H, Ming Z, Stomph TJ. 2007. Uptake and distribution of root applied or foliar applied Zn after flowering in aerobic rice. Ann Appl Biol. 150:383–391.
  • Johnson AA, Kyriacou B, Callahan DL, Carruthers L, Stangoulis J, Lombi E, Tester M. 2011. Constitutive overexpression of the OsNAS gene family reveals single-gene strategies for effective iron- and zinc-biofortification of rice endosperm. PLoS ONE. 6:e24476.
  • Khan GA, Bouraine S, Wege S, Li Y, De Carbonnel M, Berthomieu P, Poirier Y, Rouached H. 2014. Coordination between zinc and phosphate homeostasis involves the transcription factor PHR1, the phosphate exporter PHO1, and its homologue PHO1; H3 in Arabidopsis. J Exp Bot. 65:871–884.
  • Khan MU, Qasim M, Subhan M, Jamil M, Ahmad RD. 2003. Response of rice to different methods of Zn application in calcaerous soils. Pak J Appl Sci. 3:524–529.
  • Khush GS, Lee S, Cho J-I, Jeon J-S. 2012. Biofortification of crops for reducing malnutrition. Plant Biotechnol Rep. 6:195–202.
  • Kobae Y, Uemura T, Sato MH, Ohnishi M, Mimura T, Nakagawa T, Maeshima M. 2004. Zn transporter of Arabidopsis thaliana AtMTP1 is localized to vacuolar membranes and implicated in Zn homeostasis. Plant Cell Physiol. 45:1749–1758.
  • Kobayashi T, Nagasaka S, Senoura T, Itai RN, Nakanishi H, Nishizawa NK. 2013. Iron-binding haemerythrin RING ubiquitin ligases regulate plant iron responses and accumulation. Nat Commun. 4:2792–2803.
  • Krämer U, Talke IN, Hanikenne M. 2007. Transition metal transport. FEBS Lett. 581:2263–2272.
  • Lee S, Jeong HJ, Kim SA, Lee J, Guerinot ML, An G. 2010. OsZIP5 is a plasma membrane zinc transporter in rice. Plant Mol Biol. 73:507–517.
  • Leitenmaier B, Küpper H. 2013. Compartmentation and complexation of metals in hyperaccumulator plants. Front Plant Sci. 4:374–380.
  • Lin Y-F, Liang H-M, Yang S-Y, Boch A, Clemens S, Chen -C-C, Wu J-F, Huang J-L, Yeh K-C. 2009. Arabidopsis IRT3 is a zinc-regulated and plasma membrane localized zinc/iron transporter. New Phytol. 182:392–404.
  • Liu D-Y, Zhang W, Pang L-L, Zhang Y-Q, Wang X-Z, Liu Y-M, Chen X-P, Zhang F-S, Zou C-Q. 2017. Effects of zinc application rate and zinc distribution relative to root distribution on grain yield and grain Zn concentration in wheat. Plant Soil. 411:167–178.
  • Liu H, Gan W, Rengel Z, Zhao P. 2016. Effects of zinc fertilizer rate and application method on photosynthetic characteristics and grain yield of summer maize. J Soil Sci Plant Nutr. 16:550–562.
  • Lucca P, Hurrelland R, Potrykus I. 2001. Genetic engineering approaches to improve the bioavailability and the level of iron in rice grains. Theor Appl Genet. 102:392–397.
  • Lucca P, Poletti S, Sautter C. 2006. Genetic engineering approaches to enrich rice with iron and vitamin A. Plant Physiol. 126:291–303.
  • Mao H, Wang J, Wang Z, Zan Y, Lyons G, Zou C. 2014. Using agronomic biofortification to boost zinc, selenium, and iodine concentrations of food crops grown on the loess plateau in China. J Soil Sci Plant Nutr. 14:459–470.
  • Maret W. 2013. Zinc biochemistry: from a single zinc enzyme to a key element of life. Adv Nutr Int Rev J. 4:82–91.
  • McBeath TM, McLaughlin MJ. 2014. Efficacy of zinc oxides as fertilisers. Plant Soil. 374:843–855.
  • McCauley A, Jones C, Jacobsen J. 2009. Plant nutrient functions and deficiency and toxicity symptoms. Nutr Manage Modu. 9:11–12.
  • Milner MJ, Seamon J, Craft E, Kochian LV. 2013. Transport properties of members of the ZIP family in plants and their role in Zn and Mn homeostasis. J Exp Bot. 64:369–381.
  • Moreau S, Thomson RM, Kaiser BN, Trevaskis B, Guerinot ML, Udvardi MK, Puppo A, Day DA. 2002. GmZIP1 encodes a symbiosis-specific zinc transporter in soybean. J Biol Chem. 277:4738–4746.
  • Morgounov A, Gómez-Becerra HF, Abugalieva A, Dzhunusova M, Yessimbekova M, Muminjanov H, Zelenskiy Y, Ozturk L, Cakmak I. 2007. Iron and zinc grain density in common wheat grown in Central Asia. Euphytica. 155:193–203.
  • Naik SK, Das DK. 2007. Effect of split application of Zn on yield of rice (Oryza sativa L.) in an inceptisol. Arch Agron Soil Sci. 53:305–313.
  • Nakandalage N, Nicolas M, Norton RM, Hirotsu N, Milham P, Seneweera S. 2016. Improving rice zinc biofortification success rates through genetic and crop management approaches in a changing environment. Front Plant Sci. 7:764.
  • Nattinee P, Cakmak I, Panomwan B, Jumniun W, Benjavan R. 2009. Role of Zn fertilizers in increasing grain Zn concentration and improving grain yield of rice. In: The Proceedings of the International Plant Nutrition Colloquium XVI. Department of Plant Sciences, UC Davis USA, 22 May, 2009.
  • Palmgren MG, Clemens S, Williams LE, Krämer U, Borg S, Schjørring JK, Sanders D. 2008. Zinc biofortification of cereals: problems and solutions. Trends Plant Sci. 13:464–473.
  • Pandey N, Gupta B, Pathak GC. 2013. Foliar application of Zn at flowering stage improves plant’s performance, yield and yield attributes of black gram. Indian J Exp Biol. 51:548–555.
  • Papoyan A, Kochian LV. 2004. Identification of Thlaspica erulescens genes that may be involved in heavy metal hyper accumulation and tolerance. Characterization of a novel heavy metal transporting ATPase. Plant Physiol. 136:3814–3823.
  • Qadar A. 2002. Selecting rice genotypes tolerant to Zn deficiency and sodicity stresses. Differences in Zn, iron, manganese, copper, phosphorus concentrations, and phosphorus/Zn ratio in their leaves. J Plant Nutr. 25:457–473.
  • Qu LQ, Yoshihara T, Ooyama A, Goto F, Takaiwa F. 2005. Iron accumulation does not parallel the high expression level of ferritin in transgenic rice seeds. Planta. 222:225–233.
  • Ramesh SA, Choimes S, Schachtman D. 2004. Over-expression of an Arabidopsis zinc transporter in Hordeum vulgare increases short-term zinc uptake after zinc deprivation and seed zinc content. Plant Mol Biol. 54:373–385.
  • Ramesh SA, Shin R, Eide DJ, Schachtman DP. 2003. Differential metal selectivity and gene expression of two zinc transporters from rice. Plant Physiol. 133:126–134.
  • Rashid A. 2001. Secondary and micronutrients; soil science. Islamabad: National Book Foundation; p. 372–379.
  • Rehman H. 2012. N-Zn dynamics under different rice production systems [ PhD dissertation]. Faisalabad: University of Agriculture.
  • Robson AD. 2012. Zinc in soils and plants: proceedings of the international symposium on ‘zinc in soils and plants’ held at the University of Western Australia, 27–28 September, 1993. Vol. 55. New York, NY: Springer Science & Business Media.
  • Ruffo M, Olson R, Daverede I. 2016. Maize yield response to zinc sources and effectiveness of diagnostic indicators. Commun Soil Sci Plant Anal. 47:137–141.
  • Sadeghzadeh B, Rengel Z. 2011. Zn in soils and crop nutrition. In: Hawkesford MJ, Barraclough P, editors. The molecular basis of nutrient use efficiency in crops. London: Wiley; p. 335–376.
  • Sadeghzadeh B. 2013. A review of Zn nutrition and plant breeding. J Soil Sci Plant Nutr. 13:905–927.
  • Samreen T, Shah HU, Ullah S, Javid M. 2013. Zinc effect on growth rate, chlorophyll, protein and mineral contents of hydroponically grown mung beans plant (Vigna radiata). Arabian J Chem. 7: 145–152.
  • Schulin R, Tandya S, Thonarb C, Grütera R, Costeroussea B, Müllera I, Helfensteina J, Dürr-Austera T, Aghilia F, Dorostkarc V, Khoshgoftarmaneshc A. 2015. Zinc biofortification of wheat through soil organic matter management. OF ABSTRACTS; p. 42. Available from: https://www.ethz.ch/content/dam/ethz/special-interest/dual/worldfoodsystemcenterdam/WFS%20Conference/Presentations/Session%2012-5%20Rainer%20Schulin.pdf
  • Sharifianpour G, Zaharah AR, Ishak CF, Hanafi MM, Khayyambashi B, Alifar N, Sharifkhani A. 2015. Effects of application of different sources of Zn and composts on Zn concentration and uptake by upland rice. J Agron. 14:23–29.
  • Shivay YS, Kumar D, Prasad R, Ahlawat LPS. 2008. Relative yield and zinc uptake by rice from zinc sulphate and zinc oxide coatings onto urea. Nutr Cycl Agroecosyst. 80:181–188.
  • Singh R, Prasad SK, Singh MK. 2014. Effect of nitrogen and zinc fertilizer on Zn biofortification in pearlmillet (Pennisetum glaucum). Indian J Agron. 59:474–476.
  • Srivastava PC, Ghosh D, Sing VP. 1999. Evaluation of different zinc sources for lowland rice production. Biol Fert Soil. 30:168–172.
  • Srivastava PC, Singh AP, Kumar S, Ramachandran V, Shrivastava M, D’Souza SF. 2008. Desorption and transformation of zinc in a mollisol and its uptake by plants in a rice–wheat rotation fertilized with either zinc-enriched biosludge from molasses or with inorganic zinc. Biol Fert Soil. 44:1035–1041.
  • Stomph TJ, Hoebe N, Spaans E, Van der Putten PEL. 2011. The relative contribution of post-flowering uptake of Zn to rice grain Zn density. 3rd International Zn Symposium; 2011 Oct 10–14; Hyderabad, India.
  • Suzuki M, Takahashi T, Tsukamoto T, Watanabe S, Matsuhashi S, Yazaki J, Kishimoto N, Kikuchi S, Nakanishi H, Mori S. 2006. Biosynthesis and secretion of mugineic acid family phytosiderophores in Zn-deficient barley. Agron J. 48:85–97.
  • Swamy BM, Rahman MA, Inabangan-Asilo MA, Amparado A, Manito C, Chadha-Mohanty P, Reinke R, Slamet-Loedin IH. 2016. Advances in breeding for high grain Zinc in rice. Rice. 9:49–57.
  • Talke IN, Hanikenne M, Krämer U. 2006. Zn-dependent global transcriptional control, transcriptional de-regulation and higher gene copy number for genes in metal homeostasis of the hyper accumulator Arabidopsis halleri. Plant Physiol. 142:148–167.
  • Tariq M, Hameed S, Malik KA, Hafeez FY. 2007. Plant root associated bacteria for Zn mobilization in rice. Pak J Bot. 39:245–253.
  • Thacher TD, Fischer PR, Strand MA, Pettifor JM. 2006. Nutritional rickets around the world: causes and future directions. Ann Trop Paed. 26:1–16.
  • Thomine S, Lelièvre F, Debarbieux E, Schroeder JI, Barbier-Brygoo H. 2003. AtNRAMP3, a multispecific vacuolar metal transporter involved in plant responses to iron deficiency. Plant J. 34:685–695.
  • Uauy C, Distelfeld A, Fahima T, Blechl A, Dubcovsky J. 2006. A NAC gene regulating senescence improves grain protein, zinc, and iron content in wheat. Science. 314:1298–1301.
  • USEPA. 2005. Integrated risk information system-database. Philadelphia (PA): Environment Protection Agency, USA.
  • Vasconcelos M, Datta K, Oliva N, Khalekuzzaman M, Torrizo L, Krishnan S, Oliveira M, Goto F, Datta K. 2003. Enhanced iron and zinc accumulation in transgenic rice with the ferritin gene. Plant Sci. 164:371–378.
  • Velu G, Ortiz-Monasterio I, Cakmak I, Hao Y, Singh RP. 2014. Biofortification strategies to increase grain zinc and iron concentrations in wheat. J Cereal Sci. 59:365–372.
  • Von Wirén N, Klair S, Bansal S, Briat J-F, Khodr H, Shioiri T, Leigh RA, Hider RC. 1999. Nicotianamine chelates both FeIII and FeII. Implications for metal transport in plants. Plant Physiol. 119:1107–1114.
  • Wang JW, Mao H, Zhao HB, Huang DL, Wang ZH. 2012. Different increases in maize and wheat grain zinc concentrations caused by soil and foliar applications of zinc in Loess Plateau, China. Field Crop Res. 135:89–96.
  • Xu Y, Wang B, Yu J, Ao G, Zhao Q. 2010. Cloning and characterisation of ZmZLP1, a gene encoding an endoplasmic reticulum-localised Zn transporter in Zea mays. Funct Plant Biol. 37:194–205.
  • Yang X, Hajiboland R, Römheld V. 2003. Bicarbonate had greater effects than high pH on inhibiting root growth of zinc-inefficient rice genotype. J Plant Nutr. 26:399–415.
  • Zhang F, Shen J, Zhang J, Zuo Y, Li L, Chen X. 2010. Rhizosphere processes and management for improving nutrient use efficiency and crop productivity: implications for China. Adv Agron. 107:1–32.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.