1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Plant Biology
  4. Volume 75, 2024
  5. Article

Annual Review of Plant Biology

Volume 75, 2024

Metal Transport Systems in Plants

Abstract

Plants take up metals, including essential micronutrients [iron (Fe), copper (Cu), zinc (Zn), and manganese (Mn)] and the toxic heavy metal cadmium (Cd), from soil and accumulate these metals in their edible parts, which are direct and indirect intake sources for humans. Multiple transporters belonging to different families are required to transport a metal from the soil to different organs and tissues, but only a few of them have been fully functionally characterized. The transport systems (the transporters required for uptake, translocation, distribution, redistribution, and their regulation) differ with metals and plant species, depending on the physiological roles, requirements of each metal, and anatomies of different organs and tissues. To maintain metal homeostasis in response to spatiotemporal fluctuations of metals in soil, plants have developed sophisticated and tightly regulated mechanisms through the regulation of transporters at the transcriptional and/or posttranscriptional levels. The manipulation of some transporters has succeeded in generating crops rich in essential metals but low in Cd accumulation. A better understanding of metal transport systems will contribute to better and safer crop production.

Keyword(s): Arabidopsis, cadmium, essential metals, regulation, rice, transporters
Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-062923-021424
2024-07-22
2024-12-04
Loading full text...

Full text loading...

/deliver/fulltext/arplant/75/1/annurev-arplant-062923-021424.html?itemId=/content/journals/10.1146/annurev-arplant-062923-021424&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Abdel-Ghany SE, Muller-Moule P, Niyogi KK, Pilon M, Shikanai T. 2005.. Two P-type ATPases are required for copper delivery in Arabidopsis thaliana chloroplasts. . Plant Cell 17::1233–51
     [Crossref] [Google Scholar]
  2. 2.
    Abuzeineh A, Vert G, Zelazny E. 2022.. Birth, life and death of the Arabidopsis IRT1 iron transporter: the role of close friends and foes. . Planta 256::112
     [Crossref] [Google Scholar]
  3. 3.
    Alejandro S, Cailliatte R, Alcon C, Dirick L, Domergue F, et al. 2017.. Intracellular distribution of manganese by the trans-Golgi network transporter NRAMP2 is critical for photosynthesis and cellular redox homeostasis. . Plant Cell 29::3068–84
     [Crossref] [Google Scholar]
  4. 4.
    Andrés-Colás N, Sancenón V, Rodríguez-Navarro S, Mayo S, Thiele DJ, et al. 2006.. The Arabidopsis heavy metal P-type ATPase HMA5 interacts with metallochaperones and functions in copper detoxification of roots. . Plant J. 45::225–36
     [Crossref] [Google Scholar]
  5. 5.
    Aoyama T, Kobayashi T, Takahashi M, Nagasaka S, Usuda K, et al. 2009.. OsYSL18 is a rice iron(III)–deoxymugineic acid transporter specifically expressed in reproductive organs and phloem of lamina joints. . Plant Mol. Biol. 70::681–92
     [Crossref] [Google Scholar]
  6. 6.
    Assunção AGL, Herrero E, Lin Y-F, Huettel B, Talukdar S, et al. 2010.. Arabidopsis thaliana transcription factors bZIP19 and bZIP23 regulate the adaptation to zinc deficiency. . PNAS 107::10296–301 6. Identified two transcription factors, bZIP19 and bZIP23, regulating the adaptation to Zn deficiency.
     [Crossref] [Google Scholar]
  7. 7.
    Banci L, Bertini I, McGreevy KS, Rosato A. 2010.. Molecular recognition in copper trafficking. . Nat. Prod. Rep. 27::695–710
     [Crossref] [Google Scholar]
  8. 8.
    Barberon M, Zelazny E, Robert S, Conéjéro G, Curie C, et al. 2011.. Monoubiquitin-dependent endocytosis of the iron-regulated transporter 1 (IRT1) transporter controls iron uptake in plants. . PNAS 108::E450–58
     [Crossref] [Google Scholar]
  9. 9.
    Bashir K, Ishimaru Y, Itai RN, Senoura T, Takahashi M, et al. 2015.. Iron deficiency regulated OsOPT7 is essential for iron homeostasis in rice. . Plant Mol. Biol. 88::165–76
     [Crossref] [Google Scholar]
  10. 10.
    Bashir K, Ishimaru Y, Shimo H, Nagasaka S, Fujimoto M, et al. 2011.. The rice mitochondrial iron transporter is essential for plant growth. . Nat. Commun. 2::322
     [Crossref] [Google Scholar]
  11. 11.
    Bernal M, Casero D, Singh V, Wilson GT, Grande A, et al. 2012.. Transcriptome sequencing identifies SPL7-regulated copper acquisition genes FRO4/FRO5 and the copper dependence of iron homeostasis in Arabidopsis. . Plant Cell 24::738–61
     [Crossref] [Google Scholar]
  12. 12.
    Bertin G, Averbeck D. 2006.. Cadmium: cellular effects, modifications of biomolecules, modulation of DNA repair and genotoxic consequences (a review). . Biochimie 88::1549–59
     [Crossref] [Google Scholar]
  13. 13.
    Blaby-Haas CE, Padilla-Benavides T, Stübe R, Argüello JM, Merchant SS. 2014.. Evolution of a plant-specific copper chaperone family for chloroplast copper homeostasis. . PNAS 111::E5480–87
     [Crossref] [Google Scholar]
  14. 14.
    Cai H, Huang S, Che J, Yamaji N, Ma JF. 2019.. The tonoplast-localized transporter OsHMA3 plays an important role in maintaining Zn homeostasis in rice. . J. Exp. Bot. 70::2717–25
     [Crossref] [Google Scholar]
  15. 15.
    Cailliatte R, Schikora A, Briat JF, Mari S, Curie C. 2010.. High-affinity manganese uptake by the metal transporter NRAMP1 is essential for Arabidopsis growth in low manganese conditions. . Plant Cell 22::904–17
     [Crossref] [Google Scholar]
  16. 16.
    Castaings L, Alcon C, Kosuth T, Correia D, Curie C. 2021.. Manganese triggers phosphorylation-mediated endocytosis of the Arabidopsis metal transporter NRAMP1. . Plant J. 106::1328–37 16. Mn transporter AtNRAMP1 undergoes phosphorylation for its endocytosis in response to high Mn in Arabidopsis.
     [Crossref] [Google Scholar]
  17. 17.
    Chao ZF, Chao DY. 2022.. Similarities and differences in iron homeostasis strategies between graminaceous and nongraminaceous plants. . New Phytol. 236::1655–60
     [Crossref] [Google Scholar]
  18. 18.
    Chao ZF, Wang YL, Chen YY, Zhang CY, Wang PY, et al. 2021.. NPF transporters in synaptic-like vesicles control delivery of iron and copper to seeds. . Sci. Adv. 7::eabh2450 18. Two transporters were identified for releasing nicotianamine to the phloem for Fe and Cu transport.
     [Crossref] [Google Scholar]
  19. 19.
    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::1049–62 19. The node-based tonoplast-localized transporter VIT2 is important for the distribution of Fe to rice grains.
     [Crossref] [Google Scholar]
  20. 20.
    Che J, Yokosho K, Yamaji N, Ma JF. 2019.. A vacuolar phytosiderophore transporter alters iron and zinc accumulation in polished rice grains. . Plant Physiol. 181::276–88
     [Crossref] [Google Scholar]
  21. 21.
    Chen Z, Fujii Y, Yamaji N, Masuda S, Takemoto Y, et al. 2013.. Mn tolerance in rice is mediated by MTP8.1, a member of the cation diffusion facilitator family. . J. Exp. Bot. 64::4375–87
     [Crossref] [Google Scholar]
  22. 22.
    Chia J-C, Yan J, Rahmati Ishka M, Faulkner MM, Simons E, et al. 2023.. Loss of OPT3 function decreases phloem copper levels and impairs crosstalk between copper and iron homeostasis and shoot-to-root signaling in Arabidopsis thaliana. . Plant Cell 35::2157–85 22. AtOPT3 is also involved in shoot-to-root signaling of Cu through phloem transport of Cu in Arabidopsis thaliana.
     [Crossref] [Google Scholar]
  23. 23.
    Chu HH, Chiecko J, Punshon T, Lanzirotti A, Lahner B, et al. 2010.. Successful reproduction requires the function of Arabidopsis YELLOW STRIPE-LIKE1 and YELLOW STRIPE-LIKE3 metal-nicotianamine transporters in both vegetative and reproductive structures. . Plant Physiol. 154::197–210
     [Crossref] [Google Scholar]
  24. 24.
    Clemens S, Ma JF. 2016.. Toxic heavy metal and metalloid accumulation in crop plants and foods. . Annu. Rev. Plant Biol. 67::489–512
     [Crossref] [Google Scholar]
  25. 25.
    Codex Aliment. Comm. 2007.. Codex Alimentarius Commission: Procedural Manual. Rome:: Food Agric. Organ. U. N. World Health Organ. , 17th ed..
     [Google Scholar]
  26. 26.
    Connorton JM, Jones ER, Rodríguez-Ramiro I, Fairweather-Tait S, Uauy C, Balk J. 2017.. Wheat vacuolar iron transporter TaVIT2 transports Fe and Mn and is effective for biofortification. . Plant Physiol. 174::2434–44
     [Crossref] [Google Scholar]
  27. 27.
    Deng F, Yamaji N, Xia J, Ma JF. 2013.. A member of the heavy metal P-type ATPase OsHMA5 is involved in xylem loading of copper in rice. . Plant Physiol. 163::1353–62
     [Crossref] [Google Scholar]
  28. 28.
    Ding G, Lei GJ, Yamaji N, Yokosho K, Mitani-Ueno N, et al. 2020.. Vascular cambium-localized AtSPDT mediates xylem-to-phloem transfer of phosphorus for its preferential distribution in Arabidopsis. . Mol. Plant 13::99–111
     [Crossref] [Google Scholar]
  29. 29.
    Dubeaux G, Neveu J, Zelazny E, Vert G. 2018.. Metal sensing by the IRT1 transporter-receptor orchestrates its own degradation and plant metal nutrition. . Mol. Cell 69::953–64 29. IRT1 functions as a transporter-receptor and senses other non-Fe metals for degradation of IRT1 to avoid accumulation of non-Fe metals.
     [Crossref] [Google Scholar]
  30. 30.
    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
     [Crossref] [Google Scholar]
  31. 31.
    Duy D, Wanner G, Meda AR, von Wiren N, Soll J, Philippar K. 2007.. PIC1, an ancient permease in Arabidopsis chloroplasts, mediates iron transport. . Plant Cell 19::986–1006
     [Crossref] [Google Scholar]
  32. 32.
    Eisenhut M, Hoecker N, Schmidt SB, Basgaran RM, Flachbart S, et al. 2018.. The plastid envelope CHLOROPLAST MANGANESE TRANSPORTER1 is essential for manganese homeostasis in Arabidopsis. . Mol. Plant 11::955–69
     [Crossref] [Google Scholar]
  33. 33.
    Enstone DE, Peterson CA, Ma F. 2002.. Root endodermis and exodermis: structure, function, and responses to the environment. . J. Plant Growth Regul. 21::335–51
     [Crossref] [Google Scholar]
  34. 34.
    Eroglu S, Meier B, von Wirén N, Peiter E. 2016.. The vacuolar manganese transporter MTP8 determines tolerance to Fe deficiency-induced chlorosis in Arabidopsis. . Plant Physiol. 170::1030–45
     [Crossref] [Google Scholar]
  35. 35.
    Fourcroy P, Sisó-Terraza P, Sudre D, Savirón M, Reyt G, et al. 2014.. Involvement of the ABCG37 transporter in secretion of scopoletin and derivatives by Arabidopsis roots in response to iron deficiency. . New Phytol. 201::155–67
     [Crossref] [Google Scholar]
  36. 36.
    Fu D, Zhang Z, Wallrad L, Wang Z, Holler S, et al. 2022.. Ca2+-dependent phosphorylation of NRAMP1 by CPK21 and CPK23 facilitates manganese uptake and homeostasis in Arabidopsis. . PNAS 119::e2204574119 36. The Mn transporter AtNRAMP1 undergoes phosphorylation by two kinases, CPK21 and CPK23, to facilitate Mn uptake.
     [Crossref] [Google Scholar]
  37. 37.
    Fujii M, Yokosho K, Yamaji N, Saisho D, Yamane M, et al. 2012.. Acquisition of aluminium tolerance by modification of a single gene in barley. . Nat. Commun. 3::713
     [Crossref] [Google Scholar]
  38. 38.
    Gao H, Xie W, Yang C, Xu J, Li J, et al. 2018.. NRAMP2, a trans-Golgi network-localized manganese transporter, is required for Arabidopsis root growth under manganese deficiency. . New Phytol. 217::179–93
     [Crossref] [Google Scholar]
  39. 39.
    Garcia-Molina A, Andrés-Colás N, Perea-García A, Neumann U, Dodani SC, et al. 2013.. The Arabidopsis COPT6 transport protein functions in copper distribution under copper-deficient conditions. . Plant Cell Physiol. 54::1378–90
     [Crossref] [Google Scholar]
  40. 40.
    GBD 2015 Mortal. Causes Death Collab. 2016.. Global, regional, and national life expectancy, all-cause mortality, and cause-specific mortality for 249 causes of death, 1980–2015: a systematic analysis for the Global Burden of Disease Study 2015. . Lancet 388::1459544
     [Crossref] [Google Scholar]
  41. 41.
    Graham RD, Knez M, Welch RM. 2012.. How much nutritional iron deficiency in humans globally is due to an underlying zinc deficiency?. Adv. Agron. 115::1–40
     [Crossref] [Google Scholar]
  42. 42.
    Grillet L, Lan P, Li W, Mokkapati G, Schmidt W. 2018.. IRON MAN is a ubiquitous family of peptides that control iron transport in plants. . Nat. Plants 4::953–63 42. In this article, IRON MAN (IMA) was identified as a sensing signal of Fe deficiency.
     [Crossref] [Google Scholar]
  43. 43.
    Grillet L, Schmidt W. 2019.. Iron acquisition strategies in land plants: not so different after all. . New Phytol. 224::11–18
     [Crossref] [Google Scholar]
  44. 44.
    Grotz N, Fox T, Connolly E, Park W, Guerinot ML, et al. 1998.. Identification of a family of zinc transporter genes from Arabidopsis that respond to zinc deficiency. . PNAS 95::7220–24
     [Crossref] [Google Scholar]
  45. 45.
    Hao X, Zeng M, Wang J, Zeng Z, Dai J, et al. 2018.. A node-expressed transporter OsCCX2 is involved in grain cadmium accumulation of rice. . Front. Plant Sci. 9::476
     [Crossref] [Google Scholar]
  46. 46.
    Hindt MN, Akmakjian GZ, Pivarski KL, Punshon T, Baxter I, et al. 2017.. BRUTUS and its paralogs, BTS LIKE1 and BTS LIKE2, encode important negative regulators of the iron deficiency response in Arabidopsis thaliana. . Metallomics 9::876–90
     [Crossref] [Google Scholar]
  47. 47.
    Hirayama T, Lei GJ, Yamaji N, Nakagawa N, Ma JF. 2018.. The putative peptide gene FEP1 regulates iron deficiency response in Arabidopsis. . Plant Cell Physiol. 59::1739–52
     [Crossref] [Google Scholar]
  48. 48.
    Huang S, Sasaki A, Yamaji N, Okada H, Mitani-Ueno N, et al. 2020.. The ZIP transporter family member OsZIP9 contributes to root zinc uptake in rice under zinc-limited conditions. . Plant Physiol. 183::1224–34 48. OsZIP9 expressed in both the root exodermis and endodermis is required for Zn uptake under zinc-limited conditions.
     [Crossref] [Google Scholar]
  49. 49.
    Huang S, Wang P, Yamaji N, Ma JF. 2020.. Plant nutrition for human nutrition: hints from rice research and future perspectives. . Mol. Plant 13::825–35
     [Crossref] [Google Scholar]
  50. 50.
    Huang S, Yamaji N, Ma JF. 2022.. Zinc transport in rice: how to balance optimal plant requirements and human nutrition. . J. Exp. Bot. 73::1800–8
     [Crossref] [Google Scholar]
  51. 51.
    Huang XY, Deng F, Yamaji N, Pinson SR, Fujii-Kashino M, et al. 2016.. A heavy metal P-type ATPase OsHMA4 prevents copper accumulation in rice grain. . Nat. Commun. 7::12138
     [Crossref] [Google Scholar]
  52. 52.
    Hussain D, Haydon MJ, Wang Y, Wong E, Sherson SM, et al. 2004.. P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis. . Plant Cell 16::1327–39
     [Crossref] [Google Scholar]
  53. 53.
    Inaba S, Kurata R, Kobayashi M, Yamagishi Y, Mori I, 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::323–34
     [Crossref] [Google Scholar]
  54. 54.
    Inoue H, Kobayashi T, Nozoye T, Takahashi M, Kakei Y, 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::3470–79
     [Crossref] [Google Scholar]
  55. 55.
    Ishikawa S, Ishimaru Y, Igura M, Kuramata M, Abe T, et al. 2012.. Ion-beam irradiation, gene identification, and marker-assisted breeding in the development of low-cadmium rice. . PNAS 109::19166–71
     [Crossref] [Google Scholar]
  56. 56.
    Ishimaru Y, Masuda H, Bashir K, Inoue H, Tsukamoto T, et al. 2010.. Rice metal-nicotianamine transporter, OsYSL2, is required for the long-distance transport of iron and manganese. . Plant J. 62::379–90
     [Crossref] [Google Scholar]
  57. 57.
    Ishimaru Y, Masuda H, Suzuki M, Bashir K, Takahashi M, et al. 2007.. Overexpression of the OsZIP4 zinc transporter confers disarrangement of zinc distribution in rice plants. . J. Exp. Bot. 58::2909–15
     [Crossref] [Google Scholar]
  58. 58.
    Ishimaru Y, Suzuki M, Tsukamoto T, Suzuki K, Nakazono M, et al. 2006.. Rice plants take up iron as an Fe3+-phytosiderophore and as Fe2+. . Plant J. 45::335–46
     [Crossref] [Google Scholar]
  59. 59.
    Jeong J, Guerinot ML. 2009.. Homing in on iron homeostasis in plants. . Trends Plant Sci. 14::280–85
     [Crossref] [Google Scholar]
  60. 60.
    Ju C, Zhang Z, Deng J, Miao C, Wang Z, et al. 2022.. Ca2+-dependent successive phosphorylation of vacuolar transporter MTP8 by CBL2/3-CIPK3/9/26 and CPK5 contributes to manganese homeostasis in Arabidopsis. . Mol. Plant 15::419–37
     [Crossref] [Google Scholar]
  61. 61.
    Jung HI, Gayomba SR, Rutzke MA, Craft E, Kochian LV, et al. 2012.. COPT6 is a plasma membrane transporter that functions in copper homeostasis in Arabidopsis and is a novel target of SQUAMOSA promoter-binding protein-like 7. . J. Biol. Chem. 287::33252–67
     [Crossref] [Google Scholar]
  62. 62.
    Kabata-Pendias AL, Wiacek K. 1985.. Excessive uptake of heavy metals by plants from contaminated soils. . Soil Sci. Ann. 36::33–42
     [Google Scholar]
  63. 63.
    Kamiya T, Akahori T, Maeshima M. 2005.. Expression profile of the genes for rice cation/H+ exchanger family and functional analysis in yeast. . Plant Cell Physiol. 46::1735–40
     [Crossref] [Google Scholar]
  64. 64.
    Kato T, Kumazaki K, Wada M, Taniguchi R, Nakane T, et al. 2019.. Crystal structure of plant vacuolar iron transporter VIT1. . Nat. Plants 5::308–15
     [Crossref] [Google Scholar]
  65. 65.
    Kennedy G, Nantel G, Shetty P. 2003.. The scourge of “hidden hunger”: global dimensions of micronutrient deficiencies. . Food Nutr. Agric. 32::8–16
     [Google Scholar]
  66. 66.
    Khan MA, Castro-Guerrero NA, McInturf SA, Nguyen NT, Dame AN, et al. 2018.. Changes in iron availability in Arabidopsis are rapidly sensed in the leaf vasculature and impaired sensing leads to opposite transcriptional programs in leaves and roots. . Plant Cell Environ. 41::2263–76
     [Crossref] [Google Scholar]
  67. 67.
    Kim SA, Punshon T, Lanzirotti A, Li L, Alonso JM, et al. 2006.. Localization of iron in Arabidopsis seed requires the vacuolar membrane transporter VIT1. . Science 314::1295–98
     [Crossref] [Google Scholar]
  68. 68.
    Klaumann S, Nickolaus SD, Fürst SH, Starck S, Schneider S, Ekkehard Neuhaus H, Trentmann O. 2011.. The tonoplast copper transporter COPT5 acts as an exporter and is required for interorgan allocation of copper in Arabidopsis thaliana. . New Phytol. 192::393–404
     [Crossref] [Google Scholar]
  69. 69.
    Kobayashi T. 2019.. Understanding the complexity of iron sensing and signaling cascades in plants. . Plant Cell Physiol. 60::1440–46
     [Crossref] [Google Scholar]
  70. 70.
    Kobayashi T, Nagano AJ, Nishizawa NK. 2021.. Iron deficiency-inducible peptide-coding genes OsIMA1 and OsIMA2 positively regulate a major pathway of iron uptake and translocation in rice. . J. Exp. Bot. 72::2196–211
     [Crossref] [Google Scholar]
  71. 71.
    Kobayashi T, Nagasaka S, Senoura T, Itai RN, Nakanishi H, et al. 2013.. Iron-binding haemerythrin RING ubiquitin ligases regulate plant iron responses and accumulation. . Nat. Commun. 4::2792
     [Crossref] [Google Scholar]
  72. 72.
    Kobayashi Y, Kuroda K, Kimura K, Southron-Francis JL, Furuzawa A, et al. 2008.. Amino acid polymorphisms in strictly conserved domains of a P-type ATPase HMA5 are involved in the mechanism of copper tolerance variation in Arabidopsis. . Plant Physiol. 148::969–80
     [Crossref] [Google Scholar]
  73. 73.
    Koike S, Inoue H, Mizuno D, Takahashi M, Nakanishi H. et al. 2004.. OsYSL2 is a rice metal-nicotianamine transporter that is regulated by iron and expressed in the phloem. . Plant J. 39::415–24
     [Crossref] [Google Scholar]
  74. 74.
    Kumar RK, Chu HH, Abundis C, Vasques K, Chan-Rodriguez D, et al. 2017.. Iron-nicotianamine transporters are required for proper long distance iron signaling. . Plant Physiol. 175::1254–68
     [Crossref] [Google Scholar]
  75. 75.
    Lan HX, Wang ZF, Wang QH, Wang MM, Bao YM, et al. 2013.. Characterization of a vacuolar zinc transporter OZT1 in rice (Oryza sativa L.). . Mol. Biol. Rep. 40::1201–10
     [Crossref] [Google Scholar]
  76. 76.
    Lanquar V, Ramos MS, Lelièvre F, Barbier-Brygoo H, Krieger-Liszkay A, et al. 2010.. Export of vacuolar manganese by AtNRAMP3 and AtNRAMP4 is required for optimal photosynthesis and growth under manganese deficiency. . Plant Physiol. 152::1986–99
     [Crossref] [Google Scholar]
  77. 77.
    Lee J, Peña MM, Nose Y, Thiele DJ. 2002.. Biochemical characterization of the human copper transporter Ctr1. . J. Biol. Chem. 277::4380–87
     [Crossref] [Google Scholar]
  78. 78.
    Lee S, Lee J, Ricachenevsky FK, Punshon T, Tappero R, et al. 2021.. Redundant roles of four ZIP family members in zinc homeostasis and seed development in Arabidopsis thaliana. . Plant J. 108::1162–73
     [Crossref] [Google Scholar]
  79. 79.
    Lei GJ, Yamaji N, Ma JF. 2021.. Two metallothionein genes highly expressed in rice nodes are involved in distribution of Zn to the grain. . New Phytol. 229::1007–20
     [Crossref] [Google Scholar]
  80. 80.
    Li J, Wang W, Yuan J, Xu J, He L, et al. 2021.. Ubiquitin-independent proteasome system is required for degradation of Arabidopsis COPPER TRANSPORTER 2. . Plant Sci. 304::110825
     [Crossref] [Google Scholar]
  81. 81.
    Li L, Zhu Z, Liao Y, Yang C, Fan N, et al. 2022.. NRAMP6 and NRAMP1 cooperatively regulate root growth and manganese translocation under manganese deficiency in Arabidopsis. . Plant J. 110::1564–77
     [Crossref] [Google Scholar]
  82. 82.
    Lilay GH, Castro PH, Guedes JG, Almeida DM, Campilho A, et al. 2020.. Rice F-bZIP transcription factors regulate the zinc deficiency response. . J. Exp. Bot. 71::3664–77
     [Crossref] [Google Scholar]
  83. 83.
    Lilay GH, Persson DP, Castro PH, Liao F, Alexander RD, et al. 2021.. Arabidopsis bZIP19 and bZIP23 act as zinc sensors to control plant zinc status. . Nat. Plants 7::137–43
     [Crossref] [Google Scholar]
  84. 84.
    Lin Y-F, Liang H-M, Yang S-Y, Boch A, Clemens S, et al. 2009.. Arabidopsis IRT3 is a zinc-regulated and plasma membrane localized zinc/iron transporter. . New Phytol. 182::392–404
     [Crossref] [Google Scholar]
  85. 85.
    Liu SM, Jiang J, Liu Y, Meng J, Xu SL, et al. 2019.. Characterization and evaluation of OsLCT1 and OsNramp5 mutants generated through CRISPR/Cas9-mediated mutagenesis for breeding low Cd rice. . Rice Sci. 26::88–97
     [Crossref] [Google Scholar]
  86. 86.
    Luo J-S, Huang J, Zeng D-L, Peng J-S, Zhang G-B, et al. 2018.. A defensin-like protein drives cadmium efflux and allocation in rice. . Nat. Commun. 9::645
     [Crossref] [Google Scholar]
  87. 87.
    Ma F, Peterson CA. 2001.. Frequencies of plasmodesmata in Allium cepa L. roots: implications for solute transport pathways. . J Exp. Bot. 52::1051–61
     [Crossref] [Google Scholar]
  88. 88.
    Ma JF, Nomoto K. 1996.. Effective regulation of iron acquisition in graminaceous plants. The role of mugineic acids as phytosiderophores. . Physiol. Plant. 97::609–17
     [Crossref] [Google Scholar]
  89. 89.
    Ma JF, Shen RF, Shao JF. 2021.. Transport of cadmium from soil to grain in cereal crops: a review. . Pedosphere 31::3–10
     [Crossref] [Google Scholar]
  90. 90.
    Ma JF, Tsay YF. 2021.. Transport systems of mineral elements in plants: transporters, regulation and utilization. . Plant Cell Physiol. 62::539–40
     [Crossref] [Google Scholar]
  91. 91.
    Mary V, Schnell Ramos M, Gillet C, Socha AL, Giraudat J, et al. 2015.. Bypassing iron storage in endodermal vacuoles rescues the iron mobilization defect in the natural resistance associated-macrophage protein3 natural resistance associated-macrophage protein4 double mutant. . Plant Physiol. 169::748–59
     [Crossref] [Google Scholar]
  92. 92.
    Masuda H, Ishimaru Y, Aung MS, Kobayashi T, Kakei Y, et al. 2012.. Iron biofortification in rice by the introduction of multiple genes involved in iron nutrition. . Sci. Rep. 2::543–49
     [Crossref] [Google Scholar]
  93. 93.
    Menguer PK, Farthing E, Peaston KA, Ricachenevsky FK, Fett JP, et al. 2013.. Functional analysis of the rice vacuolar zinc transporter OsMTP1. . J. Exp. Bot. 64::2871–83
     [Crossref] [Google Scholar]
  94. 94.
    Migocka M, Papierniak A, Kosieradzka A, Posyniak E, Maciaszczyk-Dziubinska E, et al. 2015.. Cucumber metal tolerance protein CsMTP9 is a plasma membrane H+-coupled antiporter involved in the Mn2+ and Cd2+ efflux from root cells. . Plant J. 84::1045–58
     [Crossref] [Google Scholar]
  95. 95.
    Mills RF, Doherty ML, López-Marqués RL, Weimar T, Dupree P, et al. 2008.. ECA3, a Golgi-localized P2A-type ATPase, plays a crucial role in manganese nutrition in Arabidopsis. . Plant Physiol. 146::116–28
     [Crossref] [Google Scholar]
  96. 96.
    Morel M, Crouzet J, Gravot A, Auroy P, Leonhardt N, et al. 2009.. AtHMA3, a P1B-ATPase allowing Cd/Zn/Co/Pb vacuolar storage in Arabidopsis. . Plant Physiol. 149::894–904
     [Crossref] [Google Scholar]
  97. 97.
    Morrissey J, Baxter IR, Lee J, Li L, Lahner B, et al. 2009.. The ferroportin metal efflux proteins function in iron and cobalt homeostasis in Arabidopsis. . Plant Cell 21::3326–38
     [Crossref] [Google Scholar]
  98. 98.
    Mu S, Yamaji N, Sasaki A, Luo L, Du B, et al. 2021.. A transporter for delivering zinc to the developing tiller bud and panicle in rice. . Plant J. 105::786–99
     [Crossref] [Google Scholar]
  99. 99.
    Narayanan N, Beyene G, Chauhan RD, Gaitán-Solís E, Gehan J, et al. 2019.. Biofortification of field-grown cassava by engineering expression of an iron transporter and ferritin. . Nat. Biotechnol. 37::144–51
     [Crossref] [Google Scholar]
  100. 100.
    Nawrot T, Plusquin M, Hogervorst J, Roels HA, Celis H, et al. 2006.. Environmental exposure to cadmium and risk of cancer: a prospective population-based study. . Lancet Oncol. 7::119–26
     [Crossref] [Google Scholar]
  101. 101.
    Oomen RJFJ, Wu J, Lelièvre F, Blanchet S, Richaud P, et al. 2009.. Functional characterization of NRAMP3 and NRAMP4 from the metal hyperaccumulator Thlaspi caerulescens. . New Phytol. 181::637–50
     [Crossref] [Google Scholar]
  102. 102.
    Pang C, Chai J, Zhu P, Shanklin J, Liu Q. 2023.. Structural mechanism of intracellular autoregulation of zinc uptake in ZIP transporters. . Nat. Commun. 14::3404
     [Crossref] [Google Scholar]
  103. 103.
    Peiter E, Montanini B, Gobert A, Pedas P, Husted S, et al. 2007.. A secretory pathway-localized cation diffusion facilitator confers plant manganese tolerance. . PNAS 104::8532–37
     [Crossref] [Google Scholar]
  104. 104.
    Perea-García A, Garcia-Molina A, Andrés-Colás N, Vera-Sirera F, Pérez-Amador MA. et al. 2013.. Arabidopsis copper transport protein COPT2 participates in the cross talk between iron deficiency responses and low-phosphate signaling. . Plant Physiol. 162::180–94
     [Crossref] [Google Scholar]
  105. 105.
    Printz B, Lutts S, Hausman JF, Sergeant K. 2016.. Copper trafficking in plants and its implication on cell wall dynamics. . Front. Plant Sci. 7::601
     [Crossref] [Google Scholar]
  106. 106.
    Puig S, Mira H, Dorcey E, Sancenon V, Andrés-Colás N, et al. 2007.. Higher plants possess two different types of ATX1-like copper chaperones. . Biochem. Biophys. Res. Commun. 354::385–90
     [Crossref] [Google Scholar]
  107. 107.
    Ramesh SA, Shin R, Eide DJ, Schachtman DP. 2003.. Differential metal selectivity and gene expression of two zinc transporters from rice. . Plant Physiol. 133::126–34
     [Crossref] [Google Scholar]
  108. 108.
    Rengel Z, Cakmak I, White PJ, eds. 2022.. Marschner's Mineral Nutrition of Plants. New York:: Academic. , 4th ed..
     [Google Scholar]
  109. 109.
    Robe K, Barberon M. 2023.. Nutrient carriers at the heart of plant nutrition and sensing. . Curr. Opin. Plant Biol. 74::102376
     [Crossref] [Google Scholar]
  110. 110.
    Robe K, Conejero G, Gao F, Lefebvre-Legendre L, Sylvestre-Gonon E, et al. 2021.. Coumarin accumulation and trafficking in Arabidopsis thaliana: a complex and dynamic process. . New Phytol. 229::2062–79
     [Crossref] [Google Scholar]
  111. 111.
    Ródenas R, Vert G. 2021.. Regulation of root nutrient transporters by CIPK23: ‘one kinase to rule them all. .’ Plant Cell Physiol. 62::553–63
     [Crossref] [Google Scholar]
  112. 112.
    Römheld V, Marschner H. 1986.. Evidence for a specific uptake system for iron phytosiderophores in roots of grasses. . Plant Physiol. 80::175–80
     [Crossref] [Google Scholar]
  113. 113.
    Sancenón V, Puig S, Mateu-Andrés I, Dorcey E, Thiele DJ, et al. 2004.. The Arabidopsis copper transporter COPT1 functions in root elongation and pollen development. . J. Biol. Chem. 279::15348–55
     [Crossref] [Google Scholar]
  114. 114.
    Sancenón V, Puig S, Mira H, Thiele DJ, Peñarrubia L. 2003.. Identification of a copper transporter family in Arabidopsis thaliana. . Plant Mol. Biol. 51::577–87
     [Crossref] [Google Scholar]
  115. 115.
    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::6013–21
     [Crossref] [Google Scholar]
  116. 116.
    Sasaki A, Yamaji N, Mitani-Ueno N, Kashino M, Ma JF. 2015.. A node-localized transporter OsZIP3 is responsible for the preferential distribution of Zn to developing tissues in rice. . Plant J. 84::374–84
     [Crossref] [Google Scholar]
  117. 117.
    Sasaki A, Yamaji N, Xia J, Ma JF. 2011.. OsYSL6 is involved in the detoxification of excess manganese in rice. . Plant Physiol. 157::1832–40
     [Crossref] [Google Scholar]
  118. 118.
    Sasaki A, Yamaji N, Yokosho K, Ma JF. 2012.. Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. . Plant Cell 24::2155–67
     [Crossref] [Google Scholar]
  119. 119.
    Schmid NB, Giehl RFH, Döll S, Mock H-P, Strehmel N, et al. 2014.. Feruloyl-CoA 6′-hydroxylase1-dependent coumarins mediate iron acquisition from alkaline substrates in Arabidopsis. . Plant Physiol. 164::160–72
     [Crossref] [Google Scholar]
  120. 120.
    Schneider A, Steinberger I, Herdean A, Gandini C, Eisenhut M, et al. 2016.. The evolutionarily conserved protein PHOTOSYNTHESIS AFFECTED MUTANT71 is required for efficient manganese uptake at the thylakoid membrane in Arabidopsis. . Plant Cell 28::892–910
     [Google Scholar]
  121. 121.
    Schroeder JI, Delhaize E, Frommer WB, Guerinot ML, Harrison MJ, et al. 2013.. Using membrane transporters to improve crops for sustainable food production. . Nature 497::60–66
     [Crossref] [Google Scholar]
  122. 122.
    Schwarz B, Bauer P. 2020.. FIT, a regulatory hub for iron deficiency and stress signaling in roots, and FIT-dependent and -independent gene signatures. . J. Exp. Bot. 71::1694–1705
     [Crossref] [Google Scholar]
  123. 123.
    Senoura T, Kobayashi T, An G, Nakanishi H, Nishizawa NK. 2020.. Defects in the aconitase-encoding OsACO1 gene alter iron homeostasis. . Plant Mol. Biol. 104::629–45
     [Crossref] [Google Scholar]
  124. 124.
    Senoura T, Sakashita E, Kobayashi T, Takahashi M, Aung MS, et al. 2017.. The iron-chelate transporter OsYSL9 plays a role in iron distribution in developing rice grains. . Plant Mol. Biol. 95::375–87
     [Crossref] [Google Scholar]
  125. 125.
    Shao JF, Che J, Yamaji N, Shen RF, Ma JF. 2017.. Silicon reduces cadmium accumulation by suppressing expression of transporter genes involved in cadmium uptake and translocation in rice. . J. Exp. Bot. 68::5641–51
     [Crossref] [Google Scholar]
  126. 126.
    Shao JF, Xia J, Yamaji N, Shen RF, Ma JF. 2018.. Effective reduction of cadmium accumulation in rice grain by expressing OsHMA3 under the control of the OsHMA2 promoter. . J. Exp. Bot. 69::2743–52
     [Crossref] [Google Scholar]
  127. 127.
    Shao JF, Yamaji N, Shen RF, Ma JF. 2017.. The key to Mn homeostasis in plants: regulation of Mn transporters. . Trends Plant Sci. 22::215–24
     [Crossref] [Google Scholar]
  128. 128.
    Shikanai T, Müller-Moulé P, Munekage Y, Niyogi KK, Pilon M. 2003.. PAA1, a P-type ATPase of Arabidopsis, functions in copper transport in chloroplasts. . Plant Cell 15::1333–46
     [Crossref] [Google Scholar]
  129. 129.
    Shin LJ, Lo JC, Yeh KC. 2012.. Copper chaperone Antioxidant Protein1 is essential for copper homeostasis. . Plant Physiol. 159::1099–110
     [Crossref] [Google Scholar]
  130. 130.
    Spielmann J, Cointry V, Devime F, Ravanel S, Neveu J, Vert G. 2022.. Differential metal sensing and metal-dependent degradation of the broad spectrum root metal transporter IRT1. . Plant J. 112::1252–65
     [Crossref] [Google Scholar]
  131. 131.
    Suzuki M, Bashir K, Inoue H, Takahashi M, Nakanishi H, et al. 2012.. Accumulation of starch in Zn-deficient rice. . Rice 5::9
     [Crossref] [Google Scholar]
  132. 132.
    Takahashi R, Ishimaru Y, Shimo H, Ogo Y, Senoura T, et al. 2012.. The OsHMA2 transporter is involved in root-to-shoot translocation of Zn and Cd in rice. . Plant Cell Environ. 35::1948–57
     [Crossref] [Google Scholar]
  133. 133.
    Takemoto Y, Tsunemitsu Y, Fujii-Kashino M, Mitani-Ueno N, Yamaji N, et al. 2017.. The tonoplast-localized transporter MTP8.2 contributes to manganese detoxification in the shoots and roots of Oryza sativa L. . Plant Cell Physiol. 58::1573–82
     [Crossref] [Google Scholar]
  134. 134.
    Tan L, Qu M, Zhu Y, Peng C, Wang J, et al. 2020.. ZINC TRANSPORTER5 and ZINC TRANSPORTER9 function synergistically in zinc/cadmium uptake. . Plant Physiol. 183::1235–49
     [Crossref] [Google Scholar]
  135. 135.
    Tan L, Zhu Y, Fan T, Peng C, Wang J, 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::112–18
     [Crossref] [Google Scholar]
  136. 136.
    Tang L, Mao B, Li Y, Lv Q, Zhang LP, et al. 2017.. Knockout of OsNramp5 using the CRISPR/Cas9 system produces low Cd-accumulating indica rice without compromising yield. . Sci. Rep. 7::14438
     [Crossref] [Google Scholar]
  137. 137.
    Tang M, Zhou C, Meng L, Mao D, Peng C, et al. 2016.. Overexpression of OsSPL9 enhances accumulation of Cu in rice grain and improves its digestibility and metabolism. . J. Genet. Genom. 43::673–76
     [Crossref] [Google Scholar]
  138. 138.
    Tsunemitsu Y, Genga M, Okada T, Yamaji N, Ma JF, et al. 2018.. A member of cation diffusion facilitator family, MTP11, is required for manganese tolerance and high fertility in rice. . Planta 248::231–41
     [Crossref] [Google Scholar]
  139. 139.
    Ueno D, Milner MJ, Yamaji N, Yokosho K, Koyama E, et al. 2011.. Elevated expression of TcHMA3 plays a key role in the extreme Cd tolerance in a Cd-hyperaccumulating ecotype of Thlaspi caerulescens. . Plant J. 66::852–62
     [Crossref] [Google Scholar]
  140. 140.
    Ueno D, Sasaki A, Yamaji N, Miyaji T, Fujii Y, et al. 2015.. A polarly localized transporter for efficient manganese uptake in rice. . Nat. Plants 1::15170
     [Crossref] [Google Scholar]
  141. 141.
    Ueno D, Yamaji N, Kono I, Huang CF, Ando T, et al. 2010.. Gene limiting cadmium accumulation in rice. . PNAS 107::16500–5 141. OsHMA3 was identified as a tonoplast-localized transporter for Cd and determines Cd accumulation in rice grain.
     [Crossref] [Google Scholar]
  142. 142.
    Uraguchi S, Kamiya T, Sakamoto T, Kasai K, Sato Y, et al. 2011.. Low-affinity cation transporter (OsLCT1) regulates cadmium transport into rice grains. . PNAS 108::20959–64
     [Crossref] [Google Scholar]
  143. 143.
    Verret F, Gravot A, Auroy P, Leonhardt N, David P, et al. 2004.. Overexpression of AtHMA4 enhances root-to-shoot translocation of zinc and cadmium and plant metal tolerance. . FEBS Lett. 576::306–12
     [Crossref] [Google Scholar]
  144. 144.
    Vert G, Grotz N, Dédaldéchamp F, Gaymard F, Guerinot ML, et al. 2002.. IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. . Plant Cell 14::1223–33
     [Crossref] [Google Scholar]
  145. 145.
    von Grebmer K, Saltzman A, Birol E, Wiesman D, Prasai N, et al. 2014.. Synopsis of 2014 Global Hunger Index: the challenge of hidden hunger. Rep. , Int. Food Policy Res. Inst., Washington, DC:
     [Google Scholar]
  146. 146.
    Wang P, Yamaji N, Inoue K, Mochida K, Ma JF. 2020.. Plastic transport systems of rice for mineral elements in response to diverse soil environment changes. . New Phytol. 226::156–69
     [Crossref] [Google Scholar]
  147. 147.
    Wang S, Li L, Ying Y, Wang J, Shao JF, et al. 2020.. A transcription factor OsbHLH156 regulates Strategy II iron acquisition through localising IRO2 to the nucleus in rice. . New Phytol. 225::1247–60
     [Crossref] [Google Scholar]
  148. 148.
    Wang Z, Zhang Y, Liu Y, Fu D, You Z, et al. 2023.. Calcium-dependent protein kinases CPK21 and CPK23 phosphorylate and activate the iron-regulated transporter IRT1 to regulate iron deficiency in Arabidopsis. . Sci. China Life Sci. 66::2646–62
     [Crossref] [Google Scholar]
  149. 149.
    Waters BM, Chu HH, DiDonato RJ, Roberts LA, Eisley RB, 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::1446–58
     [Crossref] [Google Scholar]
  150. 150.
    White PJ, Broadley MR. 2005.. Biofortifying crops with essential mineral elements. . Trends Plant Sci. 10::586–93
     [Crossref] [Google Scholar]
  151. 151.
    Wong CKE, Cobbett CS. 2009.. HMA P-type ATPases are the major mechanism for root-to-shoot Cd translocation in Arabidopsis thaliana. . New Phytol. 181::71–78
     [Crossref] [Google Scholar]
  152. 152.
    Wong CKE, Jarvis RS, Sherson SM, Cobbett CS. 2009.. Functional analysis of the heavy metal binding domains of the Zn/Cd-transporting ATPase, HMA2, in Arabidopsis thaliana. . New Phytol. 181::79–88
     [Crossref] [Google Scholar]
  153. 153.
    World Health Organ. 2002.. The World Health Report: 2002: Reducing Risks, Promoting Healthy Life. Geneva:: World Health Organ.
     [Google Scholar]
  154. 154.
    Yamaji N, Ma JF. 2014.. The node, a hub for mineral nutrient distribution in graminaceous plants. . Trends Plant Sci. 19::556–63
     [Crossref] [Google Scholar]
  155. 155.
    Yamaji N, Ma JF. 2017.. Node-controlled allocation of mineral elements in Poaceae. . Curr. Opi. Plant Biol. 39::18–24
     [Crossref] [Google Scholar]
  156. 156.
    Yamaji N, Ma JF. 2019.. Bioimaging of multiple elements by high-resolution LA-ICP-MS reveals altered distribution of mineral elements in the nodes of rice mutants. . Plant J. 99::1254–63
     [Crossref] [Google Scholar]
  157. 157.
    Yamaji N, Sasaki A, Xia JX, Yokosho K, Ma JF. 2013.. A node-based switch for preferential distribution of manganese in rice. . Nat. Commun. 4::2442
     [Crossref] [Google Scholar]
  158. 158.
    Yamaji N, Takemoto Y, Miyaji T, Mitani-Ueno N, Yoshida KT, et al. 2017.. Reducing phosphorus accumulation in rice grains with an impaired transporter in the node. . Nature 541::92–95
     [Crossref] [Google Scholar]
  159. 159.
    Yamaji N, Xia J, Mitani-Ueno N, Yokosho K, Ma JF. 2013.. Preferential delivery of zinc to developing tissues in rice is mediated by P-type heavy metal ATPase OsHMA2. . Plant Physiol. 162::927–39
     [Crossref] [Google Scholar]
  160. 160.
    Yamasaki H, Hayashi M, Fukazawa M, Kobayashi Y, Shikanai T. 2009.. SQUAMOSA promoter binding protein–like7 is a central regulator for copper homeostasis in Arabidopsis. . Plant Cell 21::347–61
     [Crossref] [Google Scholar]
  161. 161.
    Yan J, Chia J-C, Sheng H, Jung H-I, Zavodna T-O, et al. 2017.. Arabidopsis pollen fertility requires the transcription factors CITF1 and SPL7 that regulate copper delivery to anthers and jasmonic acid synthesis. . Plant Cell 29::3012–29
     [Crossref] [Google Scholar]
  162. 162.
    Yang CH, Wang C, Singh S, Fan N, Liu S, et al. 2021.. Golgi-localised manganese transporter PML3 regulates Arabidopsis growth through modulating Golgi glycosylation and cell wall biosynthesis. . New Phytol. 231::2200–14
     [Crossref] [Google Scholar]
  163. 163.
    Yang CH, Zhang Y, Huang CF. 2019.. Reduction in cadmium accumulation in japonica rice grains by CRISPR/Cas9-mediated editing of OsNRAMP5. . J. Int. Agric. 18::688–97
     [Crossref] [Google Scholar]
  164. 164.
    Yang M, Li Y, Liu Z, Tian J, Liang L, et al. 2020.. A high activity zinc transporter OsZIP9 mediates zinc uptake in rice. . Plant J. 103::1695–709
     [Crossref] [Google Scholar]
  165. 165.
    Yokosho K, Yamaji N, Ma JF. 2016.. OsFRDL1 expressed in nodes is required for distribution of iron to grains in rice. . J. Exp. Bot. 67::5485–94
     [Crossref] [Google Scholar]
  166. 166.
    Yokosho K, Yamaji N, Ueno D, Mitani N, Ma JF. 2009.. OsFRDL1 is a citrate transporter required for efficient translocation of iron in rice. . Plant Physiol. 149::297–305
     [Crossref] [Google Scholar]
  167. 167.
    Yu E, Wang W, Yamaji N, Fukuoka S, Che J, et al. 2022.. Duplication of a manganese/cadmium transporter gene reduces cadmium accumulation in rice grain. . Nat. Food 3::597–607
     [Crossref] [Google Scholar]
  168. 168.
    Yuan L, Yang S, Liu B, Zhang M, Wu K. 2012.. Molecular characterization of a rice metal tolerance protein, OsMTP1. . Plant Cell Rep. 31::67–79
     [Crossref] [Google Scholar]
  169. 169.
    Yuan M, Chu Z, Li X, Xu C, Wang S. 2010.. The bacterial pathogen Xanthomonas oryzae overcomes rice defenses by regulating host copper redistribution. . Plant Cell 22::3164–76
     [Crossref] [Google Scholar]
  170. 170.
    Yuan M, Li X, Xiao J, Wang S. 2011.. Molecular and functional analyses of COPT/Ctr-type copper transporter-like gene family in rice. . BMC Plant Biol. 11::69
     [Crossref] [Google Scholar]
  171. 171.
    Zhai Z, Gayomba SR, Jung H, Vimalakumari NK, Pineros M, et al. 2014.. OPT3 is a phloem-specific iron transporter that is essential for systemic iron signaling and redistribution of iron and cadmium in Arabidopsis. . Plant Cell 26::2249–64
     [Crossref] [Google Scholar]
  172. 172.
    Zhang B, Zhang C, Liu C, Jing Y, Wang Y, et al. 2018.. Inner envelope CHLOROPLAST MANGANESE TRANSPORTER 1 supports manganese homeostasis and phototrophic growth in Arabidopsis. . Mol. Plant 11::943–54
     [Crossref] [Google Scholar]
  173. 173.
    Zhang C, Lu W, Yang Y, Shen Z, Ma JF, et al. 2018.. OsYSL16 is required for preferential Cu distribution to floral organs in rice. . Plant Cell Physiol. 59::2039–51
     [Crossref] [Google Scholar]
  174. 174.
    Zhang C, Shinwari KI, Luo L, Zheng L. 2018.. OsYSL13 is involved in iron distribution in rice. . Int. J. Mol. Sci. 19::3537
     [Crossref] [Google Scholar]
  175. 175.
    Zhang Y, Xu Y-H, Yi H-Y, Gong J-M. 2012.. Vacuolar membrane transporters OsVIT1 and OsVIT2 modulate iron translocation between flag leaves and seeds in rice. . Plant J. 72::400–10
     [Crossref] [Google Scholar]
  176. 176.
    Zhang Z, Fu D, Sun Z, Ju C, Miao C, et al. 2021.. Tonoplast-associated calcium signaling regulates manganese homeostasis in Arabidopsis. . Mol. Plant 14::805–19
     [Crossref] [Google Scholar]
  177. 177.
    Zhang Z, Fu D, Xie D, Wang Z, Zhao Y, et al. 2023.. CBL1/9-CIPK23-NRAMP1 axis regulates manganese toxicity. . New Phytol. 239::660–72
     [Crossref] [Google Scholar]
  178. 178.
    Zhao FJ, Tang Z, Song JJ, Huang XY, Wang P. 2022.. Toxic metals and metalloids: uptake, transport, detoxification, phytoremediation, and crop improvement for safer food. . Mol. Plant 15::27–44
     [Crossref] [Google Scholar]
  179. 179.
    Zheng L, Yamaji N, Yokosho K, Ma JF. 2012.. YSL16 is a phloem-localized transporter of the copper-nicotianamine complex that is responsible for copper distribution in rice. . Plant Cell 24::3767–82
     [Crossref] [Google Scholar]
/content/journals/10.1146/annurev-arplant-062923-021424
Loading
Metal Transport Systems in Plants
Annual Review of Plant Biology 75, 1 (2024); https://doi.org/10.1146/annurev-arplant-062923-021424
/content/journals/10.1146/annurev-arplant-062923-021424
/content/journals/10.1146/annurev-arplant-062923-021424
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error