With the global population predicted to grow by at least 25 per cent by 2050, the need for sustainable production of nutritious foods is critical for human and environmental health. Recent advances show that specialized plant membrane transporters can be used to enhance yields of staple crops, increase nutrient content and increase resistance to key stresses, including salinity, pathogens and aluminium toxicity, which in turn could expand available arable land.
This is a preview of subscription content, access via your institution
Open Access articles citing this article.
Label-free quantitative proteomics of maize roots from different root zones provides insight into proteins associated with enhance water uptake
BMC Genomics Open Access 06 March 2022
Stress Biology Open Access 07 January 2022
Subscribe to Journal
Get full journal access for 1 year
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Get time limited or full article access on ReadCube.
All prices are NET prices.
The Food and Agriculture Organization of the United Nations. The State of Food Insecurity in the World 2010 8–11 (FAO, 2010)
The World Bank Repositioning Nutrition as Central to Development: A Strategy for Large-Scale Action Ch. 2, 42–61 (The International Bank for Reconstruction and Development/The World Bank, 2006); http://siteresources.worldbank.org/NUTRITION/Resources/281846-1131636806329/NutritionStrategy.pdf
World Health Organization/FAO. Diet, Nutrition and the Prevention of Chronic Diseases 4–12 (2003); http://whqlibdoc.who.int/trs/who_trs_916.pdf
Foresight. The Future of Food and Farming: Final Project Report 49–74 (The Government Office for Science, 2011), http://www.bis.gov.uk/assets/foresight/docs/food-and-farming/11-546-future-of-food-and-farming-report.pdf
Rockström, J. et al. A safe operating space for humanity. Nature 461, 472–475 (2009)
Foley, J. A. et al. Solutions for a cultivated planet. Nature 478, 337–342 (2011)
Mueller, N. D. et al. Closing yield gaps through nutrient and water management. Nature 490, 254–257 (2012)
Connor, D. J. Organic agriculture cannot feed the world. Field Crops Res. 106, 187–190 (2008)
Conway, G. One Billion Hungry: Can We Feed the World? Ch. 7, 125–142 (Cornell Univ. Press, 2012)
Sanjana, N. E. et al. A transcription activator-like effector toolbox for genome engineering. Nature Protocols 7, 171–192 (2012)
von Uexküll, H. R. & Mutert, E. Global extent, development and economic impact of acid soils. Plant Soil 171, 1–15 (1995)
Ryan, P. R., Delhaize, E. & Jones, D. L. Function and mechanism of organic anion exudation from plant roots. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 527–560 (2001)
Sasaki, T. et al. A wheat gene encoding an aluminum-activated malate transporter. Plant J. 37, 645–653 (2004)These authors identified and characterized the plant aluminium tolerance protein, TaALMT1, an Al-activated anion channel that mediates the efflux of Al-detoxifying malate anion from the wheat root tip.
Delhaize, E. et al. Transgenic barley (Hordeum vulgare L.) expressing the wheat aluminium resistance gene (TaALMT1) shows enhanced phosphorus nutrition and grain production when grown on an acid soil. Plant Biotechnol. J. 7, 391–400 (2009)
Rogers, E. E. & Guerinot, M. L. FRD3, a member of the multidrug and toxin efflux family, controls iron deficiency responses in Arabidopsis. Plant Cell 14, 1787–1799 (2002)
Magalhaes, J. V. et al. A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. Nature Genet. 39, 1156–1161 (2007)
Furukawa, J. et al. An aluminum-activated citrate transporter in barley. Plant Cell Physiol. 48, 1081–1091 (2007)
Maron, L. G. et al. Two functionally distinct members of the MATE (multi-drug and toxic compound extrusion) family of transporters potentially underlie two major aluminum tolerance QTLs in maize. Plant J. 61, 728–740 (2010)
Xia, J., Yamaji, N., Kasai, T. & Ma, J. F. Plasma membrane-localized transporter for aluminum in rice. Proc. Natl Acad. Sci. USA 107, 18381–18385 (2010)
Huang, C.-F., Yamaji, N., Chen, Z. & Ma, J. F. A tonoplast-localized half-size ABC transporter is required for internal detoxification of aluminum in rice. Plant J. 69, 857–867 (2012)
Famoso, A. N. et al. Genetic architecture of aluminum tolerance in rice (Oryza sativa) determined through genome-wide association analysis and QTL mapping. PLoS Genet. 7, e1002221 (2011)
Rubio, F., Gassmann, W. & Schroeder, J. I. Sodium-driven potassium uptake by the plant potassium transporter HKT1 and mutations conferring salt tolerance. Science 270, 1660–1663 (1995)
Mäser, P. et al. Altered shoot/root Na+ distribution and bifurcating salt sensitivity in Arabidopsis by genetic disruption of the Na+ transporter AtHKT1. FEBS Lett. 531, 157–161 (2002)
Ren, Z. H. et al. A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nature Genet. 37, 1141–1146 (2005)
Sunarpi et al. Enhanced salt tolerance mediated by AtHKT1 transporter-induced Na unloading from xylem vessels to xylem parenchyma cells. Plant J. 44, 928–938 (2005)
Moller, I. S. et al. Shoot Na+ exclusion and increased salinity tolerance engineered by cell type-specific alteration of Na+ transport in Arabidopsis. Plant Cell 21, 2163–2178 (2009)
Huang, S. et al. A sodium transporter (HKT7) is a candidate for Nax1, a gene for salt tolerance in durum wheat. Plant Physiol. 142, 1718–1727 (2006)
Munns, R. et al. Wheat grain yield on saline soils is improved by an ancestral Na+ transporter gene. Nature Biotechnol. 30, 360–364 (2012)A class 1 HKT transporter gene that prevents sodium accumulation in leaves was transferred from a wheat ancestor into modern durum wheat, with a resulting 25% increase in grain yield on saline soils.
Blumwald, E. & Poole, R. Na+/H+-antiport in isolated tonoplast vesicles from storage tissue of Beta vulgaris. Plant Physiol. 78, 163–167 (1985)
Schachtman, D. P. & Schroeder, J. I. Structure and transport mechanism of a high-affinity potassium uptake transporter from higher plants. Nature 370, 655–658 (1994)
Horie, T. et al. Rice OsHKT2;1 transporter mediates large Na+ influx component into K+-starved roots for growth. EMBO J. 26, 3003–3014 (2007)
Apse, M. P., Aharon, G. S., Snedden, W. A. & Blumwald, E. Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285, 1256–1258 (1999)
Barragan, V. et al. Ion exchangers NHX1 and NHX2 mediate active potassium uptake into vacuoles to regulate cell turgor and stomatal function in Arabidopsis. Plant Cell 24, 1127–1142 (2012)
Mian, A. et al. Over-expression of an Na+-and K+-permeable HKT transporter in barley improves salt tolerance. Plant J. 68, 468–479 (2011)
Riesmeier, J. W., Willmitzer, L. & Frommer, W. B. Evidence for an essential role of the sucrose transporter in phloem loading and assimilate partitioning. EMBO J. 13, 1–7 (1994)
Chen, L. Q. et al. Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468, 527–532 (2010)
Chen, L. Q. et al. Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science 335, 207–211 (2012)A FRET (fluorescence (Förster) resonance energy transfer) sucrose nanosensor was used to identify the missing link in phloem loading, that is, the phloem-parenchyma-expressed SWEET sucrose transporters, which are also key susceptibility factors for bacterial pathogens in rice.
Patrick, J. W. Phloem unloading: sieve element unloading and post-sieve element transport. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 191–222 (1997)
Antony, G. et al. Rice xa13 recessive resistance to bacterial blight is defeated by induction of the disease susceptibility gene Os-11N3. Plant Cell 22, 3864–3876 (2010)
Chu, Z. et al. Targeting xa13, a recessive gene for bacterial blight resistance in rice. Theor. Appl. Genet. 112, 455–461 (2006)
Chu, Z. et al. Promoter mutations of an essential gene for pollen development result in disease resistance in rice. Genes Dev. 20, 1250–1255 (2006)
Liu, Q. et al. A paralog of the MtN3/saliva family recessively confers race-specific resistance to Xanthomonas oryzae in rice. Plant Cell Environ. 34, 1958–1969 (2011)
Li, C., Wei, J., Lin, Y. & Chen, H. Gene silencing using the recessive rice bacterial blight resistance gene xa13 as a new paradigm in plant breeding. Plant Cell Rep. 31, 851–862 (2012)
Li, T., Liu, B., Spalding, M. H., Weeks, D. P. & Yang, B. High-efficiency TALEN-based gene editing produces disease-resistant rice. Nature Biotechnol. 30, 390–392 (2012)Synthetic transcriptional-activator-like effectors were used to develop rice plants that are resistant to the blight pathogen Xanthomonas oryzae , such that the pathogen can no longer induce SWEET transporters, thus starving the pathogen by reducing the rice-derived sugar supply to the pathogen.
Masuda, H. et al. Increase in iron and zinc concentrations in rice grains via the introduction of barley genes involved in phytosiderophore synthesis. Rice 1, 100–108 (2008)
Lee, S. et al. Iron fortification of rice seeds through activation of the nicotianamine synthase gene. Proc. Natl Acad. Sci. USA 106, 22014–22019 (2009)These authors showed that increasing nicotianamine levels resulted in increased levels of iron in polished rice and also that the iron is bioavailable using animal feeding studies.
Lee, S. et al. Activation of rice nicotianamine synthase 2 (OsNAS2) enhances iron availability for biofortification. Mol. Cells 33, 269–275 (2012)
Ishimaru, Y. et al. Rice metal-nicotianamine transporter, OsYSL2, is required for the long-distance transport of iron and manganese. Plant J. 62, 379–390 (2010)
Wirth, J. et al. Rice endosperm iron biofortification by targeted and synergistic action of nicotianamine synthase and ferritin. Plant Biotechnol. J. 7, 631–644 (2009)
Masuda, H. et al. Iron biofortification in rice by the introduction of multiple genes involved in iron nutrition. Sci. Rep. 2, 543–549 (2012)
Lee, S. et al. Bio-available zinc in rice seeds is increased by activation tagging of nicotianamine synthase. Plant Biotechnol. J. 9, 865–873 (2011)
Palmgren, M. G. et al. Zinc biofortification of cereals: problems and solutions. Trends Plant Sci. 13, 464–473 (2008)
Lanquar, V. et al. Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low iron. EMBO J. 24, 4041–4051 (2005)
Kim, S. A. et al. Localization of iron in Arabidopsis seed requires the vacuolar membrane transporter VIT1. Science 314, 1295–1298 (2006)These authors used X-ray fluorescence microprobe spectroscopy to localize iron in seeds and showed that failure to store iron properly in the vacuole via the VIT1 transporter leads to seedling lethality under iron limitation.
Morrissey, J. et al. The ferroportin metal efflux proteins function in iron and cobalt homeostasis in Arabidopsis. Plant Cell 21, 3326–3338 (2009)
Zhang, Y., Xu, Y.-H., Yi, H.-Y. & Gong, J.-M. Vacuolar membrane transporters OsVIT1 and OsVIT2 modulate iron translocation between flag leaves and seeds in rice. Plant J. 72, 400–410 (2012)
Podar, D. et al. Metal selectivity determinants in a family of transition metal transporters. J. Biol. Chem. 287, 3185–3196 (2012)
Eide, D., Broderius, M., Fett, J. & Guerinot, M. L. A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proc. Natl Acad. Sci. USA 93, 5624–5628 (1996)
Cakmak, I. Plant nutrition research: priorities to meet human needs for food in sustainable ways. Plant Soil 247, 3–24 (2002)
López-Arredondo, D. L. & Herrera-Estrella, L. Engineering phosphorus metabolism in plants to produce a dual fertilization and weed control system. Nature Biotechnol. 30, 889–893 (2012)
Gamuyao, R. et al. The protein kinase Pstol1 from traditional rice confers tolerance of phosphorus deficiency. Nature 488, 535–539 (2012)
Beebe, S. E. et al. Quantitative trait loci for root architecture traits correlated with phosphorus acquisition in common bean. Crop Sci. 46, 413–423 (2006)
Shin, R. & Schachtman, D. P. Hydrogen peroxide mediates plant root cell response to nutrient deprivation. Proc. Natl Acad. Sci. USA 101, 8827–8832 (2004)
Remy, E. et al. The Pht1;9 and Pht1;8 transporters mediate inorganic phosphate acquisition by the Arabidopsis thaliana root during phosphorus starvation. New Phytol. 195, 356–371 (2012)
Versaw, W. K. & Harrison, M. J. A chloroplast phosphate transporter, PHT2;1, influences allocation of phosphate within the plant and phosphate-starvation responses. Plant Cell 14, 1751–1766 (2002)
Nagarajan, V. K. et al. Arabidopsis Pht1;5 mobilizes phosphate between source and sink organs and influences the interaction between phosphate homeostasis and ethylene signaling. Plant Physiol. 156, 1149–1163 (2011)
Arpat, A. B. et al. Functional expression of PHO1 to the Golgi and trans-Golgi network and its role in export of inorganic phosphate. Plant J. 71, 479–491 (2012)
Javot, H., Penmetsa, R. V., Terzaghi, N., Cook, D. R. & Harrison, M. J. A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proc. Natl Acad. Sci. USA 104, 1720–1725 (2007)A phosphate transporter (MtPT4) was shown to be necessary for Medicago truncatula plants to obtain phosphate delivered via the fungal symbiont and furthermore, that MtPT4 transporter function is essential to maintain the symbiosis.
Yang, S. Y. et al. Nonredundant regulation of rice arbuscular mycorrhizal symbiosis by two members of the PHOSPHATE TRANSPORTER1 gene family. Plant Cell 24, 4236–4251 (2012)
McAllister, C. H., Beatty, P. H. & Good, A. G. Engineering nitrogen use efficient crop plants: the current status. Plant Biotechnol. J. 10, 1011–1025 (2012)
Wang, Y. Y., Hsu, P. K. & Tsay, Y. F. Uptake, allocation and signaling of nitrate. Trends Plant Sci. 17, 458–467 (2012)
Kiba, T. et al. The Arabidopsis nitrate transporter NRT2.4 plays a double role in roots and shoots of nitrogen-starved plants. Plant Cell 24, 245–258 (2012)
Liu, K. H. & Tsay, Y. F. Switching between the two action modes of the dual-affinity nitrate transporter CHL1 by phosphorylation. EMBO J. 22, 1005–1013 (2003)
Wang, R., Liu, D. & Crawford, N. M. The Arabidopsis CHL1 protein plays a major role in high-affinity nitrate uptake. Proc. Natl Acad. Sci. USA 95, 15134–15139 (1998)
Ho, C. H., Lin, S. H., Hu, H. C. & Tsay, Y. F. CHL1 functions as a nitrate sensor in plants. Cell 138, 1184–1194 (2009)These authors provided the first report of a nutrient transporter in plants that also acts as a sensor for its own substrate, nitrate, over a wide range of concentrations.
Hu, H. C., Wang, Y. Y. & Tsay, Y. F. AtCIPK8, a CBL-interacting protein kinase, regulates the low-affinity phase of the primary nitrate response. Plant J. 57, 264–278 (2009)
Little, D. Y. et al. The putative high-affinity nitrate transporter NRT2.1 represses lateral root initiation in response to nutritional cues. Proc. Natl Acad. Sci. USA 102, 13693–13698 (2005)
Krouk, G. et al. Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Dev. Cell 18, 927–937 (2010)
Ruffel, S. et al. Nitrogen economics of root foraging: transitive closure of the nitrate-cytokinin relay and distinct systemic signaling for N supply vs. demand. Proc. Natl Acad. Sci. USA 108, 18524–18529 (2011)
Nour-Eldin, H. H. et al. NRT/PTR transporters are essential for translocation of glucosinolate defence compounds to seeds. Nature 488, 531–534 (2012)
Gilbert-Diamond, D. et al. Rice consumption contributes to arsenic exposure in US women. Proc. Natl Acad. Sci. USA 108, 20656–20660 (2011)
Ueno, D. et al. Gene limiting cadmium accumulation in rice. Proc. Natl Acad. Sci. USA 107, 16500–16505 (2010)
Song, W. Y. et al. Arsenic tolerance in Arabidopsis is mediated by two ABCC-type phytochelatin transporters. Proc. Natl Acad. Sci. USA 107, 21187–21192 (2010)
Ma, J. F. et al. Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Proc. Natl Acad. Sci. USA 105, 9931–9935 (2008)These authors demonstrated that arsenite, a toxic form of soil arsenic, is transported into and within the rice plant by two novel transporters, providing new possible strategies for minimizing arsenic entry into the food chain by altering these transporters.
Ishikawa, S. et al. Ion-beam irradiation, gene identification, and marker-assisted breeding in the development of low-cadmium rice. Proc. Natl Acad. Sci. USA 109, 19166–19171 (2012)
Kim, T.-H., Böhmer, M., Hu, H., Nishimura, N. & Schroeder, J. I. Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling. Annu. Rev. Plant Biol. 61, 561–591 (2010)
Kusumi, K., Hirotsuka, S., Kumamaru, T. & Iba, K. Increased leaf photosynthesis caused by elevated stomatal conductance in a rice mutant deficient in SLAC1, a guard cell anion channel protein. J. Exp. Bot. 63, 5635–5644 (2012)
Hu, H. et al. Carbonic anhydrases are upstream regulators of CO2-controlled stomatal movements in guard cells. Nature Cell Biol. 12, 87–93 (2010)
Kuromori, T. et al. ABC transporter AtABCG25 is involved in abscisic acid transport and responses. Proc. Natl Acad. Sci. USA 107, 2361–2366 (2010)
Kang, J. et al. PDR-type ABC transporter mediates cellular uptake of the phytohormone abscisic acid. Proc. Natl Acad. Sci. USA 107, 2355–2360 (2010)
Weber, A. P. & Brautigam, A. The role of membrane transport in metabolic engineering of plant primary metabolism. Curr. Opin. Biotechnol http://dx.doi.org/10.1016/j.copbio.2012.09.010 (4 October 2012)
Delhaize, E., Gruber, B. D. & Ryan, P. R. The roles of organic anion permeases in aluminium tolerance and mineral nutrition. FEBS Lett. 581, 2255–2262 (2007)
US Geological Survey Mineral Commodity Summaries 2012 118–119 (US Geological Survey, 2012); http://minerals.usgs.gov/minerals/pubs/mcs/2012/mcs2012.pdf
Research in our laboratories was supported by: the Division of Chemical Sciences, Geosciences and Biosciences, Office of Basic Energy Sciences at the US Department of Energy (DOE) under grant numbers DE-FG02-03ER15449 (to J.I.S.), DE-FG02-04ER15542 (to W.B.F.) and DE-FG-2-06ER15809 (to M.L.G.); by the Grains Research and Development Corporation, Australia (to R.M. and E.D.); by the US National Science Foundation under grant numbers IOS:0842720 (to M.J.H.), MCB0918220 (to J.I.S.) and IOS-091994 and DBI 0701119 (to M.L.G.); by the UK Biotechnology and Biological Sciences Research Council under grant number BB/J004561/1 (to D.S.); by the National Institutes of Health under grant numbers GM060396-P42ES010337 (to J.I.S.) and GM078536 and P42ES007373 (to M.L.G.); by the US Department of Agriculture under grant number 2009-02273 (to L.V.K.); by a Generation Challenge Grant under grant number G7010.03.06 (to L.V.K.); by the Howard Hughes Medical Institute under grant number 55005946 (to L.H.E.); the CREST Japan Science and Technology Agency (to N.K.N.); by the Ministry of Education, Culture, Sports, Science and Technology, Japan under grant number 23119507 (to T.H.); and by the Academia Sinica, Taiwan and the National Science Council, Taiwan under grant number NSC 101-2321-B-001-005 (to Y.F.T.).
The authors declare no competing financial interests.
About this article
Cite this article
Schroeder, J., Delhaize, E., Frommer, W. et al. Using membrane transporters to improve crops for sustainable food production. Nature 497, 60–66 (2013). https://doi.org/10.1038/nature11909
This article is cited by
Label-free quantitative proteomics of maize roots from different root zones provides insight into proteins associated with enhance water uptake
BMC Genomics (2022)
Integrated mRNA and miRNA Expression Analyses of Pinus massoniana Roots and Shoots in Long-Term Response to Phosphate Deficiency
Journal of Plant Growth Regulation (2022)
Effect of ACGT motif in spatiotemporal regulation of AtAVT6D, which improves tolerance to osmotic stress and nitrogen-starvation
Plant Molecular Biology (2022)
Environmental Science and Pollution Research (2022)
Molecular Biology Reports (2022)