Skip to main content

Advertisement

SpringerLink
Log in

The Role of Membrane Transporters in the Biofortification of Zinc and Iron in Plants

  • Published:
Biological Trace Element Research Aims and scope Submit manuscript

Abstract

Over three billion people suffer from various health issues due to the low supply of zinc (Zn) and iron (Fe) in their food. Low supply of micronutrients is the main cause of malnutrition and biofortification could help to solve this issue. Understanding the molecular mechanisms of biofortification is challenging. The membrane transporters are involved in the uptake, transport, storage, and redistribution of Zn and Fe in plants. These transporters are also involved in biofortification and help to load the Zn and Fe into the endosperm of the seeds. Very little knowledge is available on the role and functions of membrane transporters involved in seed biofortification. Understanding the mechanism and role of membrane transporters could be helpful to improve biofortification. In this review, we provide the details on membrane transporters involved in the uptake, transport, storage, and redistribution of Zn and Fe. We also discuss available information on transporters involved in seed biofortification. This review will help plant breeders and molecular biologists understand the importance and implications of membrane transporters for seed biofortification.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Availability of Data and Materials

Not applicable to this article.

References

  1. Lockyer S, White A, Buttriss JL (2018) Biofortified crops for tackling micronutrient deficiencies–what impact are these having in developing countries and could they be of relevance within Europe? Nutr Bull 43:319–357

    Article  Google Scholar 

  2. Page V, Feller U (2015) Heavy metals in crop plants: transport and redistribution processes on the whole plant level. Agronomy 5:447–463

    Article  CAS  Google Scholar 

  3. Welch RM, Norvell WA (1999) Mechanisms of cadmium uptake, translocation and deposition in plants. In: McLaughlin MJ, Singh BR (eds) Cadmium in soils and plants. Developments in Plant and Soil Sciences, vol 85. Springer, Dordrecht, 125–150

  4. Briskin DP (1994) Membranes and transport systems in plants: an overview. Weed Sci 42:255–262

    Article  CAS  Google Scholar 

  5. Ahmad I, Maathuis FJM (2014) Cellular and tissue distribution of potassium: physiological relevance, mechanisms and regulation. J Plant Physiol 171:708–714

    Article  CAS  Google Scholar 

  6. Ajeesh Krishna TP, Ceasar SA, Maharajan T, Ramakrishnan M, Duraipandiyan V, Al-Dhabi NA, Ignacimuthu S (2017) Improving the zinc-use efficiency in plants: a review. SABRAO J Breed Genet 49:211–230

  7. Ajeesh Krishna TP, Maharajan T, Victor Roch G et al (2020) Structure, function, regulation and phylogenetic relationship of ZIP family transporters of plants. Front Plant Sci. https://doi.org/10.3389/fpls.2020.00662

    Article  Google Scholar 

  8. Chowdhury R, Nallusamy S, Shanmugam V, et al (2022) Genome-wide understanding of evolutionary and functional relationships of rice yellow stripe-like (YSL) transporter family in comparison with other plant species. Biologia 77:39–53

  9. Kawachi M, Nagasaki-Takeuchi N, Kato M, Maeshima M (2011) Radioisotopes: applications in bio-medical science. Nirmal S (eds) Application of radioisotopes in biochemical analyses: metal binding proteins and metal transporters. InTech 115–126

  10. Menguer PK, Farthing E, Peaston KA et al (2013) Functional analysis of the rice vacuolar zinc transporter OsMTP1. J Exp Bot 64:2871–2883

    Article  CAS  Google Scholar 

  11. Pinto E, Ferreira IM (2015) Cation transporters/channels in plants: tools for nutrient biofortification. J Plant Physiol 179:64–82

    Article  CAS  Google Scholar 

  12. Tang B, Luo M, Zhang Y et al (2021) Natural variations in the P-type ATPase heavy metal transporter gene ZmHMA3 control cadmium accumulation in maize grains. J Exp Bot 72:6230–6246

    Article  CAS  Google Scholar 

  13. Waters BM, Chu H-H, DiDonato RJ et al (2006) Mutations in Arabidopsis yellow stripe-like1 and yellow stripe-like3 reveal their roles in metal ion homeostasis and loading of metal ions in seeds. Plant Physiol 141:1446–1458

    Article  CAS  Google Scholar 

  14. Zou W, Chen J, Meng L et al (2021) The rice cation/H+ exchanger family involved in Cd tolerance and transport. Int J Mol Sci 22:8186

    Article  CAS  Google Scholar 

  15. Conte SS, Walker EL (2011) Transporters contributing to iron trafficking in plants. Mol Plant 4:464–476

    Article  CAS  Google Scholar 

  16. Kobae Y, Uemura T, Sato MH et al (2004) Zinc transporter of Arabidopsis thaliana AtMTP1 is localized to vacuolar membranes and implicated in zinc homeostasis. Plant Cell Physiol 45:1749–1758

    Article  CAS  Google Scholar 

  17. 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

    Article  CAS  Google Scholar 

  18. Nevo Y, Nelson N (2006) The NRAMP family of metal-ion transporters. Biochim Biophys Acta (BBA)-Molecular Cell Res 1763:609–620

  19. Sanz A, Pike S, Khan MA et al (2019) Copper uptake mechanism of Arabidopsis thaliana high-affinity COPT transporters. Protoplasma 256:161–170

    Article  Google Scholar 

  20. Shigaki T, Hirschi KD (2006) Diverse functions and molecular properties emerging for CAX cation/H+ exchangers in plants. Plant Biol 8:419–429

    Article  CAS  Google Scholar 

  21. Williams LE, Mills RF (2005) P1B-ATPases–an ancient family of transition metal pumps with diverse functions in plants. Trends Plant Sci 10:491–502

    Article  CAS  Google Scholar 

  22. Buturi CV, Mauro RP, Fogliano V et al (2021) Mineral biofortification of vegetables as a tool to improve human diet. Foods 10:223

    Article  CAS  Google Scholar 

  23. Viana VE, Maltzahn LE, Costa de Oliveira A, Pegoraro C (2021) Genetic approaches for iron and zinc biofortification and arsenic decrease in Oryza sativa L. grains. Biol Trace Elem Res 11:1–19

  24. Huang S, Wang P, Yamaji N, Ma JF (2020) Plant nutrition for human nutrition: hints from rice research and future perspectives. Mol Plant 13:825–835

    Article  CAS  Google Scholar 

  25. Ishimaru Y, Suzuki M, Kobayashi T et al (2005) OsZIP4, a novel zinc-regulated zinc transporter in rice. J Exp Bot 56:3207–3214

    Article  CAS  Google Scholar 

  26. Lee S, An G (2009) Over-expression of OsIRT1 leads to increased iron and zinc accumulations in rice. Plant Cell Environ 32:408–416

    Article  CAS  Google Scholar 

  27. Wu T-Y, Gruissem W, Bhullar NK (2018) Facilitated citrate-dependent iron translocation increases rice endosperm iron and zinc concentrations. Plant Sci 270:13–22

    Article  CAS  Google Scholar 

  28. Inoue H, Kobayashi T, Nozoye T et al (2009) Rice OsYSL15 is an iron-regulated iron (III)-deoxymugineic acid transporter expressed in the roots and is essential for iron uptake in early growth of the seedlings. J Biol Chem 284:3470–3479

    Article  CAS  Google Scholar 

  29. Evens NP, Buchner P, Williams LE, Hawkesford MJ (2017) The role of ZIP transporters and group F bZIP transcription factors in the Zn-deficiency response of wheat (Triticum aestivum). Plant J 92:291–304

    Article  CAS  Google Scholar 

  30. Connorton JM, Jones ER, Rodríguez-Ramiro I et al (2017) Wheat vacuolar iron transporter TaVIT2 transports Fe and Mn and is effective for biofortification. Plant Physiol 174:2434–2444

    Article  CAS  Google Scholar 

  31. Gupta OP, Pandey V, Saini R et al (2021) Comparative physiological, biochemical and transcriptomic analysis of hexaploid wheat (T. aestivum L.) roots and shoots identifies potential pathways and their molecular regulatory network during Fe and Zn starvation. Genomics 113:3357–3372

    Article  CAS  Google Scholar 

  32. Li S, Zhou X, Huang Y et al (2013) Identification and characterization of the zinc-regulated transporters, iron-regulated transporter-like protein (ZIP) gene family in maize. BMC Plant Biol 13:1–14

    Article  CAS  Google Scholar 

  33. Han J, Song X, Li P et al (2009) Maize ZmFDR3 localized in chloroplasts is involved in iron transport. Sci China Ser C Life Sci 52:864–871

    Article  CAS  Google Scholar 

  34. Li S, Zhou X, Li H et al (2015) Overexpression of ZmIRT1 and ZmZIP3 enhances iron and zinc accumulation in transgenic Arabidopsis. PLoS One 10:e0136647

    Article  Google Scholar 

  35. Gustin JL, Zanis MJ, Salt DE (2011) Structure and evolution of the plant cation diffusion facilitator family of ion transporters. BMC Evol Biol 11:1–13

    Article  Google Scholar 

  36. Kolaj-Robin O, Russell D, Hayes KA et al (2015) Cation diffusion facilitator family: structure and function. FEBS Lett 589:1283–1295

    Article  CAS  Google Scholar 

  37. Guerinot ML (2000) The ZIP family of metal transporters. Biochim Biophys Acta (BBA)-Biomembranes 1465:190–198

    Article  CAS  Google Scholar 

  38. Martins V, Carneiro F, Conde C et al (2017) The grapevine VvCAX3 is a cation/H+ exchanger involved in vacuolar Ca 2+ homeostasis. Planta 246:1083–1096

    Article  CAS  Google Scholar 

  39. Neeraj J, Rajani N, Shigaki T (2009) Mining cation (CAX) transporter diversity for nutrition-enhanced crops and phytoremediation. Int J Integr Biol 7:22–25

    Google Scholar 

  40. Choe M, Choe W, Cha S, Lee I (2018) Changes of cationic transport in AtCAX5 transformant yeast by electromagnetic field environments. J Biol Phys 44:433–448

    Article  CAS  Google Scholar 

  41. Møller J V, Juul B, le Maire M (1996) Structural organization, ion transport, and energy transduction of P-type ATPases. Biochim Biophys Acta (BBA)-Reviews Biomembr 1286:1–51

  42. Ram H, Sardar S, Gandass N (2021) Vacuolar iron transporter (like) proteins: regulators of cellular iron accumulation in plants. Physiol Plant 171:823–832

    Article  CAS  Google Scholar 

  43. Yang M, Li Y, Liu Z et al (2020) A high activity zinc transporter OsZIP9 mediates zinc uptake in rice. Plant J 103:1695–1709

    Article  CAS  Google Scholar 

  44. Zhang Y, Xu Y, Yi H, Gong J (2012) Vacuolar membrane transporters OsVIT1 and OsVIT2 modulate iron translocation between flag leaves and seeds in rice. Plant J 72:400–410

    Article  CAS  Google Scholar 

  45. Grotz N, Fox T, Connolly E et al (1998) Identification of a family of zinc transporter genes from Arabidopsis that respond to zinc deficiency. Proc Natl Acad Sci 95:7220–7224

    Article  CAS  Google Scholar 

  46. Huang S, Sasaki A, Yamaji N et al (2020) The ZIP transporter family member OsZIP9 contributes to root zinc uptake in rice under zinc-limited conditions. Plant Physiol 183:1224–1234

    Article  CAS  Google Scholar 

  47. Watts-Williams SJ, Wege S, Ramesh SA, et al (2020) Identification of a unique ZIP transporter involved in zinc uptake via the arbuscular mycorrhizal fungal pathway. BioRxiv

  48. Cai H, Huang S, Che J et al (2019) The tonoplast-localized transporter OsHMA3 plays an important role in maintaining Zn homeostasis in rice. J Exp Bot 70:2717–2725

    Article  CAS  Google Scholar 

  49. Che J, Yamaji N, Ma JF (2021) Role of a vacuolar iron transporter OsVIT2 in the distribution of iron to rice grains. New Phytol 230:1049–1062

    Article  CAS  Google Scholar 

  50. Cao Y, Zhao X, Liu Y, et al (2019) Genome-wide identification of ZmHMAs and association of natural variation in ZmHMA2 and ZmHMA3 with leaf cadmium accumulation in maize. PeerJ 7:e7877

  51. Li S, Liu X, Zhou X et al (2019) Improving zinc and iron accumulation in maize grains using the zinc and iron transporter ZmZIP5. Plant Cell Physiol 60:2077–2085. https://doi.org/10.1093/pcp/pcz104

    Article  CAS  Google Scholar 

  52. Zang J, Huo Y, Liu J et al (2020) Maize YSL2 is required for iron distribution and development in kernels. J Exp Bot 71:5896–5910

    Article  CAS  Google Scholar 

  53. Gupta OP, Pandey V, Saini R et al (2020) Identifying transcripts associated with efficient transport and accumulation of Fe and Zn in hexaploid wheat (T. aestivum L.). J Biotechnol 316:46–55

    Article  CAS  Google Scholar 

  54. Vatansever R, Filiz E, Eroglu S (2017) Genome-wide exploration of metal tolerance protein (MTP) genes in common wheat (Triticum aestivum): insights into metal homeostasis and biofortification. Biometals 30:217–235

    Article  CAS  Google Scholar 

  55. Menguer PK, Vincent T, Miller AJ et al (2018) Improving zinc accumulation in cereal endosperm using Hv MTP 1, a transition metal transporter. Plant Biotechnol J 16:63–71

    Article  CAS  Google Scholar 

  56. Takahashi M, Nozoye T, Kitajima N et al (2009) In vivo analysis of metal distribution and expression of metal transporters in rice seed during germination process by microarray and X-ray fluorescence imaging of Fe, Zn, Mn, and Cu. Plant Soil 325:39–51

    Article  CAS  Google Scholar 

  57. Díaz-Benito P, Banakar R, Rodríguez-Menéndez S et al (2018) Iron and zinc in the embryo and endosperm of rice (Oryza sativa L.) seeds in contrasting 2′-deoxymugineic acid/nicotianamine scenarios. Front Plant Sci 9:1190

    Article  Google Scholar 

  58. Stephens BW, Cook DR, Grusak MA (2011) Characterization of zinc transport by divalent metal transporters of the ZIP family from the model legume Medicago truncatula. Biometals 24:51–58

    Article  CAS  Google Scholar 

  59. Hall J, áL, Williams LE, (2003) Transition metal transporters in plants. J Exp Bot 54:2601–2613

    Article  CAS  Google Scholar 

  60. Kumar L, Meena NL, Singh U (2016) Zinc transporter: mechanism for improving Zn availability. In: Singh U, Praharaj C, Singh S, Singh N (eds) Biofortification of food crops. Springer, New Delhi, 129–146

  61. Cohen CK, Garvin DF, Kochian LV (2004) Kinetic properties of a micronutrient transporter from Pisum sativum indicate a primary function in Fe uptake from the soil. Planta 218:784–792

    Article  CAS  Google Scholar 

  62. Gupta N, Ram H, Kumar B (2016) Mechanism of zinc absorption in plants: uptake, transport, translocation and accumulation. Rev Environ Sci Bio/Technology 15:89–109

    Article  CAS  Google Scholar 

  63. Bashir K, Ishimaru Y, Nishizawa NK (2012) Molecular mechanisms of zinc uptake and translocation in rice. Plant Soil 361:189–201

    Article  CAS  Google Scholar 

  64. Zhang X, Zhang D, Sun W, Wang T (2019) The adaptive mechanism of plants to iron deficiency via iron uptake, transport, and homeostasis. Int J Mol Sci 20:2424

    Article  Google Scholar 

  65. Kim SA, Lou GM (2007) Mining iron: iron uptake and transport in plants. FEBS Lett 581:2273–2280

    Article  CAS  Google Scholar 

  66. Kobayashi T, Nozoye T, Nishizawa NK (2019) Iron transport and its regulation in plants. Free Radic Biol Med 133:11–20

    Article  CAS  Google Scholar 

  67. Bashir K, Seki M, Nishizawa NK (2019) The transport of essential micronutrients in rice. Mol Breed 39:1–17

    Article  Google Scholar 

  68. Tan L, Zhu Y, Fan T et al (2019) OsZIP7 functions in xylem loading in roots and inter-vascular transfer in nodes to deliver Zn/Cd to grain in rice. Biochem Biophys Res Commun 512:112–118

    Article  CAS  Google Scholar 

  69. Liu XS, Feng SJ, Zhang BQ et al (2019) OsZIP1 functions as a metal efflux transporter limiting excess zinc, copper and cadmium accumulation in rice. BMC Plant Biol 19:1–16

    Google Scholar 

  70. Meng L, Sun L, Tan L (2018) Progress in ZIP transporter gene family in rice. Yi Chuan= Hered 40:33–43

  71. Lee S, Kim SA, Lee J et al (2010) Zinc deficiency-inducible OsZIP8 encodes a plasma membrane-localized zinc transporter in rice. Mol Cells 29:551–558

    Article  CAS  Google Scholar 

  72. Ricachenevsky FK, Punshon T, Lee S et al (2018) Elemental profiling of rice FOX lines leads to characterization of a new Zn plasma membrane transporter, OsZIP7. Front Plant Sci 9:865

    Article  Google Scholar 

  73. 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

    Article  CAS  Google Scholar 

  74. Ishimaru Y, Masuda H, Suzuki M et al (2007) Overexpression of the OsZIP4 zinc transporter confers disarrangement of zinc distribution in rice plants. J Exp Bot 58:2909–2915

    Article  CAS  Google Scholar 

  75. Yang X, Huang J, Jiang Y, Zhang H-S (2009) Cloning and functional identification of two members of the ZIP (Zrt, Irt-like protein) gene family in rice (Oryza sativa L.). Mol Biol Rep 36:281–287

    Article  CAS  Google Scholar 

  76. Mondal TK, Ganie SA, Rana MK, Sharma TR (2014) Genome-wide analysis of zinc transporter genes of maize (Zea mays). Plant Mol Biol Report 32:605–616

    Article  CAS  Google Scholar 

  77. Lilay GH, Persson DP, Castro PH et al (2021) Arabidopsis bZIP19 and bZIP23 act as zinc sensors to control plant zinc status. Nat Plants 7:137–143

    Article  CAS  Google Scholar 

  78. Clemens S, Deinlein U, Ahmadi H et al (2013) Nicotianamine is a major player in plant Zn homeostasis. Biometals 26:623–632

    Article  CAS  Google Scholar 

  79. Verret F, Gravot A, Auroy P et al (2005) Heavy metal transport by AtHMA4 involves the N-terminal degenerated metal binding domain and the C-terminal His11 stretch. FEBS Lett 579:1515–1522

    Article  CAS  Google Scholar 

  80. Hussain D, Haydon MJ, Wang Y et al (2004) P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis. Plant Cell 16:1327–1339

    Article  CAS  Google Scholar 

  81. Verret F, Gravot A, Auroy P et al (2004) Overexpression of AtHMA4 enhances root-to-shoot translocation of zinc and cadmium and plant metal tolerance. FEBS Lett 576:306–312

    Article  CAS  Google Scholar 

  82. Takahashi R, Bashir K, Ishimaru Y et al (2012) The role of heavy-metal ATPases, HMAs, in zinc and cadmium transport in rice. Plant Signal Behav 7:1605–1607

    Article  CAS  Google Scholar 

  83. Sasaki A, Yamaji N, Ma JF (2014) Overexpression of OsHMA3 enhances Cd tolerance and expression of Zn transporter genes in rice. J Exp Bot 65:6013–6021

    Article  CAS  Google Scholar 

  84. Satoh-Nagasawa N, Mori M, Nakazawa N et al (2012) Mutations in rice (Oryza sativa) heavy metal ATPase 2 (OsHMA2) restrict the translocation of zinc and cadmium. Plant Cell Physiol 53:213–224

    Article  CAS  Google Scholar 

  85. Takahashi R, Ishimaru Y, Shimo H et al (2012) The OsHMA2 transporter is involved in root-to-shoot translocation of Zn and Cd in rice. Plant Cell Environ 35:1948–1957

    Article  CAS  Google Scholar 

  86. Tan J, Wang J, Chai T et al (2013) Functional analyses of T a HMA 2, a P1B-type ATPase in wheat. Plant Biotechnol J 11:420–431

    Article  CAS  Google Scholar 

  87. Moradi K, Abdollahi Mandoulakani B (2020) Expression pattern of HMA1, HMA2 and HMA9 genes under Zn deficiency conditions in bread wheat cultivars with different Zn uptake efficiency. Cereal Res 9:347–357

    Google Scholar 

  88. Zhiguo E, Tingting LI, Chen C, Lei W (2018) Genome-wide survey and expression analysis of P1B-ATPases in rice, maize and sorghum. Rice Sci 25:208–217

    Article  Google Scholar 

  89. Song W-Y, Choi KS, Kim DY et al (2010) Arabidopsis PCR2 is a zinc exporter involved in both zinc extrusion and long-distance zinc transport. Plant Cell 22:2237–2252. https://doi.org/10.1105/tpc.109.070185

    Article  CAS  Google Scholar 

  90. Ramesh SA, Choimes S, Schachtman DP (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

    Article  CAS  Google Scholar 

  91. Ramegowda Y, Venkategowda R, Jagadish P et al (2013) Expression of a rice Zn transporter, OsZIP1, increases Zn concentration in tobacco and finger millet transgenic plants. Plant Biotechnol Rep 7:309–319

    Article  Google Scholar 

  92. Bughio N, Yamaguchi H, Nishizawa NK et al (2002) Cloning an iron-regulated metal transporter from rice. J Exp Bot 53:1677–1682

    Article  CAS  Google Scholar 

  93. Ishimaru Y, Suzuki M, Tsukamoto T, Suzuki K, Nakazono M, Kobayashi T, Wada Y, Watanabe S, Matsuhashi S, Takahashi M, Nakanishi H (2006) Rice plants take up iron as an Fe3+-phytosiderophore and as Fe2+. Plant J 45:335–346

    Article  CAS  Google Scholar 

  94. Wang W, Ye J, Ma Y et al (2020) OsIRO3 plays an essential role in iron deficiency responses and regulates iron homeostasis in rice. Plants 9:1095

    Article  CAS  Google Scholar 

  95. 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

    Article  CAS  Google Scholar 

  96. Lee S, Jeong HJ, Kim SA et al (2010) OsZIP5 is a plasma membrane zinc transporter in rice. Plant Mol Biol 73:507–517

    Article  CAS  Google Scholar 

  97. Koike S, Inoue H, Mizuno D et al (2004) OsYSL2 is a rice metal-nicotianamine transporter that is regulated by iron and expressed in the phloem. Plant J 39:415–424

    Article  CAS  Google Scholar 

  98. Senoura T, Sakashita E, Kobayashi T et al (2017) The iron-chelate transporter OsYSL9 plays a role in iron distribution in developing rice grains. Plant Mol Biol 95:375–387

    Article  CAS  Google Scholar 

  99. Lee S, Kim Y-Y, Lee Y, An G (2007) Rice P1B-type heavy-metal ATPase, OsHMA9, is a metal efflux protein. Plant Physiol 145:831–842. https://doi.org/10.1104/pp.107.102236

    Article  CAS  Google Scholar 

  100. Ishimaru Y, Takahashi R, Bashir K et al (2012) Characterizing the role of rice NRAMP5 in manganese, iron and cadmium transport. Sci Rep 2:1–8

    Article  Google Scholar 

  101. Takahashi R, Ishimaru Y, Nakanishi H, Nishizawa NK (2011) Role of the iron transporter OsNRAMP1 in cadmium uptake and accumulation in rice. Plant Signal Behav 6:1813–1816

    Article  CAS  Google Scholar 

  102. Kakei Y, Ishimaru Y, Kobayashi T et al (2012) OsYSL16 plays a role in the allocation of iron. Plant Mol Biol 79:583–594

    Article  CAS  Google Scholar 

  103. Singh SP, Keller B, Gruissem W, Bhullar NK (2017) Rice nicotianamine synthase 2 expression improves dietary iron and zinc levels in wheat. Theor Appl Genet 130:283–292

    Article  CAS  Google Scholar 

  104. Ueno D, Yamaji N, Ma JF (2009) Further characterization of ferric—phytosiderophore transporters ZmYS1 and HvYS1 in maize and barley. J Exp Bot 60:3513–3520

    Article  CAS  Google Scholar 

  105. Curie C, Panaviene Z, Loulergue C et al (2001) Maize yellow stripe1 encodes a membrane protein directly involved in Fe (III) uptake. Nature 409:346–349

    Article  CAS  Google Scholar 

  106. Deshpande P, Dapkekar A, Oak M et al (2018) Nanocarrier-mediated foliar zinc fertilization influences expression of metal homeostasis related genes in flag leaves and enhances gluten content in durum wheat. PLoS One 13:e0191035

    Article  Google Scholar 

  107. Sharma S, Kaur G, Kumar A et al (2020) Gene expression pattern of vacuolar-iron transporter-like (VTL) genes in hexaploid wheat during metal stress. Plants 9:229

    Article  CAS  Google Scholar 

  108. Durmaz E, Coruh C, Dinler G et al (2011) Expression and cellular localization of ZIP1 transporter under zinc deficiency in wild emmer wheat. Plant Mol Biol Report 29:582–596

    Article  CAS  Google Scholar 

  109. Carey-Fung O, Beasley JT (2021) Johnson AAT (2021) Annotation and molecular characterisation of the TaIRO3 and TaHRZ iron homeostasis genes in bread wheat (Triticum aestivum L.). Genes 12:653

    Article  CAS  Google Scholar 

  110. Eide D, Broderius M, Fett J, Lou GM (1996) A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proc Natl Acad Sci 93:5624–5628

    Article  CAS  Google Scholar 

  111. Krausko M, Labajová M, Peterková D, Jásik J (2021) Specific expression of AtIRT1 in phloem companion cells suggests its role in iron translocation in aboveground plant organs. Plant Signal Behav 16:1–11

  112. Vert G, Grotz N, Dédaldéchamp F et al (2002) IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell 14:1223–1233

    Article  CAS  Google Scholar 

  113. Nakanishi H, Ogawa I, Ishimaru Y et al (2006) Iron deficiency enhances cadmium uptake and translocation mediated by the Fe2+ transporters OsIRT1 and OsIRT2 in rice. Soil Sci Plant Nutr 52:464–469

    Article  CAS  Google Scholar 

  114. Jiang Y, Chen X, Chai S et al (2021) TpIRT1 from Polish wheat (Triticum polonicum L.) enhances the accumulation of Fe, Mn Co, and Cd in Arabidopsis. Plant Sci 312:111058

    Article  CAS  Google Scholar 

  115. Xiong H, Kobayashi T, Kakei Y et al (2012) AhNRAMP1 iron transporter is involved in iron acquisition in peanut. J Exp Bot 63:4437–4446

    Article  CAS  Google Scholar 

  116. Connolly EL, Campbell NH, Grotz N et al (2003) Overexpression of the FRO2 ferric chelate reductase confers tolerance to growth on low iron and uncovers posttranscriptional control. Plant Physiol 133:1102–1110

    Article  CAS  Google Scholar 

  117. Durrett TP, Gassmann W, Rogers EE (2007) The FRD3-mediated efflux of citrate into the root vasculature is necessary for efficient iron translocation. Plant Physiol 144:197–205

    Article  CAS  Google Scholar 

  118. Roschzttardtz H, Séguéla-Arnaud M, Briat J-F et al (2011) The FRD3 citrate effluxer promotes iron nutrition between symplastically disconnected tissues throughout Arabidopsis development. Plant Cell 23:2725–2737

    Article  CAS  Google Scholar 

  119. Yokosho K, Yamaji N, Ueno D et al (2009) OsFRDL1 is a citrate transporter required for efficient translocation of iron in rice. Plant Physiol 149:297–305

    Article  CAS  Google Scholar 

  120. Morrissey J, Baxter IR, Lee J et al (2009) The ferroportin metal efflux proteins function in iron and cobalt homeostasis in Arabidopsis. Plant Cell 21:3326–3338. https://doi.org/10.1105/tpc.109.069401

    Article  CAS  Google Scholar 

  121. Thomine S and Vert G (2013) Iron transport in plants: better be safe than sorry. Curr Opin Plant Biol 16:322–327

    Article  CAS  Google Scholar 

  122. Lanquar V, Lelièvre F, Bolte S et al (2005) Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low iron. EMBO J 24:4041–4051

    Article  CAS  Google Scholar 

  123. Desbrosses-Fonrouge A-G, Voigt K, Schröder A et al (2005) Arabidopsis thaliana MTP1 is a Zn transporter in the vacuolar membrane which mediates Zn detoxification and drives leaf Zn accumulation. FEBS Lett 579:4165–4174

    Article  CAS  Google Scholar 

  124. 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 oversupply. Plant J 46:861–879

    Article  CAS  Google Scholar 

  125. Morel M, Crouzet J, Gravot A, Auroy P, Leonhardt N, Vavasseur A, Richaud P (2009) AtHMA3, a P1B-ATPase allowing Cd/Zn/co/Pb vacuolar storage in Arabidopsis. Plant Physiol 149:894–904

    Article  CAS  Google Scholar 

  126. Chu H-H, Conte SS, Chan Rodriguez D et al (2013) Arabidopsis thaliana Yellow Stripe1-Like4 and Yellow Stripe1-Like6 localize to internal cellular membranes and are involved in metal ion homeostasis. Front Plant Sci 4:283

    Google Scholar 

  127. Lee S, Lee J, Ricachenevsky FK, et al (2021) Redundant roles of four ZIP family members in zinc homeostasis and seed development in Arabidopsis thaliana. Plant J

  128. Gaitán-Solís E, Taylor NJ, Siritunga D et al (2015) Overexpression of the transporters AtZIP1 and AtMTP1 in cassava changes zinc accumulation and partitioning. Front Plant Sci 6:492

    Article  Google Scholar 

  129. Tan L, Qu M, Zhu Y, Peng C, Wang J, Gao D, Chen C (2020) zinc transporter5 and zinc transporter9 function synergistically in zinc/cadmium uptake. Plant Physiol 183:1235–1249

    Article  CAS  Google Scholar 

  130. Tan S, Han R, Li P et al (2015) Over-expression of the MxIRT1 gene increases iron and zinc content in rice seeds. Transgenic Res 24:109–122

    Article  CAS  Google Scholar 

  131. Xiong H, Guo X, Kobayashi T et al (2014) Expression of peanut iron regulated transporter 1 in tobacco and rice plants confers improved iron nutrition. Plant Physiol Biochem 80:83–89

    Article  CAS  Google Scholar 

  132. Masuda H, Usuda K, Kobayashi T et al (2009) Overexpression of the barley nicotianamine synthase gene HvNAS1 increases iron and zinc concentrations in rice grains. Rice 2:155–166

    Article  Google Scholar 

  133. Nozoye T, Otani M, Senoura T et al (2017) Overexpression of barley nicotianamine synthase 1 confers tolerance in the sweet potato to iron deficiency in calcareous soil. Plant Soil 418:75–88

    Article  CAS  Google Scholar 

  134. Barabasz A, Krämer U, Hanikenne M et al (2010) Metal accumulation in tobacco expressing Arabidopsis halleri metal hyperaccumulation gene depends on external supply. J Exp Bot 61:3057–3067

    Article  CAS  Google Scholar 

  135. Narayanan N, Beyene G, Chauhan RD et al (2015) Overexpression of Arabidopsis VIT1 increases accumulation of iron in cassava roots and stems. Plant Sci 240:170–181

    Article  CAS  Google Scholar 

  136. Gao F, Robe K, Gaymard F et al (2019) The transcriptional control of iron homeostasis in plants: a tale of bHLH transcription factors? Front Plant Sci 10:6

    Article  Google Scholar 

  137. Wang N, Cui Y, Liu Y et al (2013) Requirement and functional redundancy of Ib subgroup bHLH proteins for iron deficiency responses and uptake in Arabidopsis thaliana. Mol Plant 6:503–513

    Article  CAS  Google Scholar 

  138. Yuan Y, Wu H, Wang N et al (2008) FIT interacts with AtbHLH38 and AtbHLH39 in regulating iron uptake gene expression for iron homeostasis in Arabidopsis. Cell Res 18:385–397

    Article  CAS  Google Scholar 

  139. Yuan YX, Zhang J, Wang DW, Ling HQ (2005) AtbHLH29 of Arabidopsis thaliana is a functional ortholog of tomato FER involved in controlling iron acquisition in strategy I plants. Cell Res 15:613–621

    Article  CAS  Google Scholar 

  140. Colangelo EP, Lou GM (2004) The essential basic helix-loop-helix protein FIT1 is required for the iron deficiency response. Plant Cell 16:3400–3412

    Article  CAS  Google Scholar 

  141. Jakoby M, Wang H-Y, Reidt W et al (2004) FRU (BHLH029) is required for induction of iron mobilization genes in Arabidopsis thaliana. FEBS Lett 577:528–534

    Article  CAS  Google Scholar 

  142. Bauer P, Ling H-Q, Lou GM (2007) FIT, the FER-like iron deficiency induced transcription factor in Arabidopsis. Plant Physiol Biochem 45:260–261

    Article  CAS  Google Scholar 

  143. Kim Y-C, Kang Y, Yang E-Y, et al (2021) Applications and major achievements of genome editing in vegetable crops: a review. Front Plant Sci 12:

  144. Ahmed T, Noman M, Shahid M et al (2021) Potential application of CRISPR/Cas9 system to engineer abiotic stress tolerance in plants. Protein Pept Lett 28:861–877

    Article  CAS  Google Scholar 

  145. Qin Y, Park T-S, Cho YS, Lim M-H (2021) TALEN-mediated bar-knockout rice production and transcriptome profiling. Plant Breed Biotechnol 9:32–44

    Article  CAS  Google Scholar 

  146. Ceasar SA, Rajan V, Prykhozhij SV et al (2016) Insert, remove or replace: a highly advanced genome editing system using CRISPR/Cas9. Biochim Biophys Acta - Mol Cell Res 1863:2333–2344. https://doi.org/10.1016/j.bbamcr.2016.06.009

    Article  CAS  Google Scholar 

  147. Hillary VE, Ceasar SA (2019) Application of CRISPR/Cas9 genome editing system in cereal crops. Open Biotechnol J 13:

  148. Zhang D, Zhang Z, Unver T, Zhang B (2021) CRISPR/Cas: a powerful tool for gene function study and crop improvement. J Adv Res 29:207–221

    Article  CAS  Google Scholar 

  149. Tan L, Qu M, Zhu Y et al (2020) Zinc transporter5 and zinc transporter9 function synergistically in zinc/cadmium uptake1. Plant Physiol 183:1235–1249. https://doi.org/10.1104/pp.19.01569

    Article  CAS  Google Scholar 

  150. Inaba S, Kurata R, Kobayashi M et al (2015) Identification of putative target genes of bZIP19, a transcription factor essential for Arabidopsis adaptation to Zn deficiency in roots. Plant J 84:323–334

    Article  CAS  Google Scholar 

  151. Zhang D, Zhang Z, Unver T, Zhang B (2020) CRISPR/Cas: a powerful tool for gene function study and crop improvement. J Adv Res

  152. Fiaz S, Ahmad S, Noor MA et al (2019) Applications of the CRISPR/Cas9 system for rice grain quality improvement: perspectives and opportunities. Int J Mol Sci 20:888

    Article  CAS  Google Scholar 

  153. Gindri RG, Navarro BB, da Cruz Dias PV et al (2020) Physiological responses of rice (Oryza sativa L.) oszip7 loss-of-function plants exposed to varying Zn concentrations. Physiol Mol Biol Plants 26:1349–1359

    Article  CAS  Google Scholar 

  154. Wang Y, Yang J, Miao R, et al (2021) A novel zinc transporter essential for Arabidopsis zinc and iron-dependent growth. J Plant Physiol 256:153296

  155. Gu D, Zhou X, Ma Y, et al (2021) Expression of a Brassica napus metal transport protein (BnMTP3) in Arabidopsis thaliana confers tolerance to Zn and Mn. Plant Sci 304:110754

Download references

Acknowledgements

We sincerely thank Rajagiri College of Social Sciences, Kochi, Kerala, for providing the research facilities and support.

Funding

This work was financially supported by Rajagiri College of Social Sciences (Autonomous), Kerala, India, under Seed Money for Faculty Minor Research.

Author information

Authors and Affiliations

  1. Department of Biosciences, Rajagiri College of Social Sciences, Kochi, 683104, Kerala, India

    T. P. Ajeesh Krishna, T. Maharajan & S. Antony Ceasar

Authors
  1. T. P. Ajeesh Krishna
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. T. Maharajan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. Antony Ceasar
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

TPAK, TM, and SAC conceptualized and wrote the manuscript. SAC critically revised the manuscript for publication.

Corresponding author

Correspondence to S. Antony Ceasar.

Ethics declarations

Ethics Approval and Consent to Participate

Not applicable.

Consent for Publication

All authors have agreed for publication.

Competing Interests

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Krishna, T.P.A., Maharajan, T. & Ceasar, S.A. The Role of Membrane Transporters in the Biofortification of Zinc and Iron in Plants. Biol Trace Elem Res 201, 464–478 (2023). https://doi.org/10.1007/s12011-022-03159-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-022-03159-w

Keywords

Search

Navigation