1932

Abstract

One of life's decisive innovations was to harness the catalytic power of metals for cellular chemistry. With life's expansion, global atmospheric and biogeochemical cycles underwent dramatic changes. Although initially harmful, they permitted the evolution of multicellularity and the colonization of land. In land plants as primary producers, metal homeostasis faces heightened demands, in part because soil is a challenging environment for nutrient balancing. To avoid both nutrient metal limitation and metal toxicity, plants must maintain the homeostasis of metals within tighter limits than the homeostasis of other minerals. This review describes the present model of protein metalation and sketches its transfer from unicellular organisms to land plants as complex multicellular organisms. The inseparable connection between metal and redox homeostasis increasingly draws our attention to more general regulatory roles of metals. Mineral co-option, the use of nutrient or other metals for functions other than nutrition, is an emerging concept beyond that of nutritional immunity.

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2024-07-22
2025-02-14
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Literature Cited

  1. 1.
    Abdel-Ghany SE, Müller-Moulé P, Niyogi KK, Pilon M, Shikanai T. 2005.. Two P-type ATPases are required for copper delivery in Arabidopsis thaliana chloroplasts. . Plant Cell 17::123351
    [Crossref] [Google Scholar]
  2. 2.
    Akmakjian GZ, Riaz N, Guerinot ML. 2021.. Photoprotection during iron deficiency is mediated by the bHLH transcription factors PYE and ILR3. . PNAS 118::e2024918118 2. Describes Fe deficiency responses of shoots expanding from the known role of PYE-ILR3 in repressing FERRITIN transcription.
    [Crossref] [Google Scholar]
  3. 3.
    Alloway BJ. 2009.. Soil factors associated with zinc deficiency in crops and humans. . Environ. Geochem. Health 31::53748
    [Crossref] [Google Scholar]
  4. 4.
    Alloway BJ, Tills AR. 1984.. Copper deficiency in world crops. . Outlook Agric. 13::3242
    [Crossref] [Google Scholar]
  5. 5.
    Anbar AD. 2008.. Elements and evolution. . Science 322::148183
    [Crossref] [Google Scholar]
  6. 6.
    Andreini C, Bertini I, Cavallaro G, Holliday GL, Thornton JM. 2008.. Metal ions in biological catalysis: from enzyme databases to general principles. . J. Biol. Inorg. Chem. 13::120518
    [Crossref] [Google Scholar]
  7. 7.
    Andrés-Colás N, Sancenon V, Rodriguez-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::22536
    [Crossref] [Google Scholar]
  8. 8.
    Andresen E, Küpper H. 2013.. Cadmium toxicity in plants. . Met. Ions Life Sci. 11::395413
    [Google Scholar]
  9. 9.
    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::86179
    [Crossref] [Google Scholar]
  10. 10.
    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::10296301
    [Crossref] [Google Scholar]
  11. 11.
    Barberon M, Geldner N. 2014.. Radial transport of nutrients: the plant root as a polarized epithelium. . Plant Physiol. 166::52837
    [Crossref] [Google Scholar]
  12. 12.
    Barberon M, Vermeer JE, De Bellis D, Wang P, Naseer S, et al. 2016.. Adaptation of root function by nutrient-induced plasticity of endodermal differentiation. . Cell 164::44759 12. Example of a metal homeostasis–dependent change in root anatomy.
    [Crossref] [Google Scholar]
  13. 13.
    Becher M, Talke IN, Krall L, Krämer U. 2004.. Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri. . Plant J. 37::25168
    [Crossref] [Google Scholar]
  14. 14.
    Bellés JM, Garro R, Pallás V, Fayos J, Rodrigo I, Conejero V. 2006.. Accumulation of gentisic acid as associated with systemic infections but not with the hypersensitive response in plant-pathogen interactions. . Planta 223::50011
    [Crossref] [Google Scholar]
  15. 15.
    Beneš I, Schreiber K, Ripperger H, Kircheiss A. 1983.. Metal complex formation by nicotianamine, a possible phytosiderophore. . Experientia 39::26162
    [Crossref] [Google Scholar]
  16. 16.
    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::73861
    [Crossref] [Google Scholar]
  17. 17.
    Bernal M, Krämer U. 2021.. Involvement of Arabidopsis multi-copper oxidase-encoding LACCASE12 in root-to-shoot iron partitioning: a novel example of copper-iron crosstalk. . Front. Plant Sci. 12::688318
    [Crossref] [Google Scholar]
  18. 18.
    Boyd RS. 2010.. Elemental defenses of plants by metals. . Nat. Educ. Knowl. 3::57
    [Google Scholar]
  19. 19.
    Brady DC, Crowe MS, Turski ML, Hobbs GA, Yao X, et al. 2014.. Copper is required for oncogenic BRAF signalling and tumorigenesis. . Nature 509::49296
    [Crossref] [Google Scholar]
  20. 20.
    Brawley HN, Kreinbrink AC, Hierholzer JD, Vali SW, Lindahl PA. 2023.. Labile iron pool of isolated Escherichia coli cytosol likely includes Fe-ATP and Fe-citrate but not Fe-glutathione or aqueous Fe. . J. Am. Chem. Soc. 145::210417
    [Crossref] [Google Scholar]
  21. 21.
    Briat JF, Ravet K, Arnaud N, Duc C, Boucherez J, et al. 2010.. New insights into ferritin synthesis and function highlight a link between iron homeostasis and oxidative stress in plants. . Ann. Bot. 105::81122
    [Crossref] [Google Scholar]
  22. 22.
    Bruinsma JJ, Jirakulaporn T, Muslin AJ, Kornfeld K. 2002.. Zinc ions and cation diffusion facilitator proteins regulate Ras-mediated signaling. . Dev. Cell 2::56778
    [Crossref] [Google Scholar]
  23. 23.
    Burkhead JL, Reynolds KA, Abdel-Ghany SE, Cohu CM, Pilon M. 2009.. Copper homeostasis. . New Phytol. 182::799816
    [Crossref] [Google Scholar]
  24. 24.
    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::90417
    [Crossref] [Google Scholar]
  25. 25.
    Capdevila DA, Edmonds KA, Giedroc DP. 2017.. Metallochaperones and metalloregulation in bacteria. . Essays Biochem. 61::177200
    [Crossref] [Google Scholar]
  26. 26.
    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::132837
    [Crossref] [Google Scholar]
  27. 27.
    Castaings L, Caquot A, Loubet S, Curie C. 2016.. The high-affinity metal transporters NRAMP1 and IRT1 team up to take up iron under sufficient metal provision. . Sci. Rep. 6::37222
    [Crossref] [Google Scholar]
  28. 28.
    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
    [Crossref] [Google Scholar]
  29. 29.
    Chen CC, Chien WF, Lin NC, Yeh KC. 2014.. Alternative functions of Arabidopsis YELLOW STRIPE-LIKE3: from metal translocation to pathogen defense. . PLOS ONE 9::e98008
    [Crossref] [Google Scholar]
  30. 30.
    Chen Y-Y, Wang Y, Shin L-J, Wu J-F, Shanmugam V, et al. 2013.. Iron is involved in the maintenance of circadian period length in Arabidopsis. . Plant Physiol. 161::140920
    [Crossref] [Google Scholar]
  31. 31.
    Cheng C-Y, Krishnakumar V, Chan AP, Thibaud-Nissen F, Schobel S, Town CD. 2016.. Araport11: a complete reannotation of the Arabidopsis thaliana reference genome. . Plant J. 89::789804
    [Crossref] [Google Scholar]
  32. 32.
    Chia JC, 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::215785
    [Crossref] [Google Scholar]
  33. 33.
    Chu H-H, Car S, Socha AL, Hindt MN, Punshon T, Guerinot ML. 2017.. The Arabidopsis MTP8 transporter determines the localization of manganese and iron in seeds. . Sci. Rep. 7::11024
    [Crossref] [Google Scholar]
  34. 34.
    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::197210
    [Crossref] [Google Scholar]
  35. 35.
    Clemens S. 2001.. Molecular mechanisms of plant metal tolerance and homeostasis. . Planta 212::47586
    [Crossref] [Google Scholar]
  36. 36.
    Clemens S. 2022.. The cell biology of zinc. . J. Exp. Bot. 73::168898
    [Crossref] [Google Scholar]
  37. 37.
    Colangelo EP, Guerinot ML. 2004.. The essential basic helix-loop-helix protein FIT1 is required for the iron deficiency response. . Plant Cell 16::3400
    [Crossref] [Google Scholar]
  38. 38.
    Connolly EL, Fett JP, Guerinot ML. 2002.. Expression of the IRT1 metal transporter is controlled by metals at the levels of transcript and protein accumulation. . Plant Cell 14::134757
    [Crossref] [Google Scholar]
  39. 39.
    Culotta VC, Yang M, O'Halloran TV. 2006.. Activation of superoxide dismutases: putting the metal to the pedal. . Biochim. Biophys. Acta Mol. Cell Res. 1763::74758
    [Crossref] [Google Scholar]
  40. 40.
    Curie C, Cassin G, Couch D, Divol F, Higuchi K, et al. 2009.. Metal movement within the plant: contribution of nicotianamine and yellow stripe. 1 -like transporters. . Ann. Bot. 103::111
    [Crossref] [Google Scholar]
  41. 41.
    Desbrosses-Fonrouge AG, Voigt K, Schröder A, Arrivault S, Thomine S, Krämer U. 2005.. Arabidopsis thaliana MTP1 is a Zn transporter in the vacuolar membrane which mediates Zn detoxification and drives leaf Zn accumulation. . FEBS Lett. 579::416574
    [Crossref] [Google Scholar]
  42. 42.
    Devireddy LR, Hart DO, Goetz DH, Green MR. 2010.. A mammalian siderophore synthesized by an enzyme with a bacterial homolog involved in enterobactin production. . Cell 141::100617
    [Crossref] [Google Scholar]
  43. 43.
    Dinneny JR, Long TA, Wang JY, Jung JW, Mace D, et al. 2008.. Cell identity mediates the response of Arabidopsis roots to abiotic stress. . Science 320::94245
    [Crossref] [Google Scholar]
  44. 44.
    Distéfano AM, Martin MV, Córdoba JP, Bellido AM, D'Ippólito S, et al. 2017.. Heat stress induces ferroptosis-like cell death in plants. . J. Cell Biol. 216::46376
    [Crossref] [Google Scholar]
  45. 45.
    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::95364.e5 45. Shows that IRT1 acts as a cytosolic sensor of non-iron metal cations, which are its secondary substrates.
    [Crossref] [Google Scholar]
  46. 46.
    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::197205
    [Crossref] [Google Scholar]
  47. 47.
    Eide D, Broderius M, Fett J, Guerinot ML. 1996.. A novel iron-regulated metal transporter from plants identified by functional expression in yeast. . PNAS 93::562428
    [Crossref] [Google Scholar]
  48. 48.
    Eroglu S, Meier B, von Wirén N, Peiter E. 2016.. The vacuolar manganese transporter MTP8 determines tolerance to iron deficiency-induced chlorosis in Arabidopsis. . Plant Physiol. 170::103045
    [Crossref] [Google Scholar]
  49. 49.
    Escudero V, Ferreira Sánchez D, Abreu I, Sopeña-Torres S, Makarovsky-Saavedra N, et al. 2022.. Arabidopsis thaliana Zn2+-efflux ATPases HMA2 and HMA4 are required for resistance to the necrotrophic fungus Plectosphaerella cucumerina BMM. . J. Exp. Bot. 73::33950
    [Crossref] [Google Scholar]
  50. 50.
    Foster AW, Clough SE, Aki Z, Young TR, Clarke AR, Robinson NJ. 2022.. Metalation calculators for E. coli strain JM109 (DE3): aerobic, anaerobic, and hydrogen peroxide exposed cells cultured in LB media. . Metallomics 14::mfac058
    [Crossref] [Google Scholar]
  51. 51.
    Foster AW, Pernil R, Patterson CJ, Scott AJP, Palsson LO, et al. 2017.. A tight tunable range for Ni(II) sensing and buffering in cells. . Nat. Chem. Biol. 13::40914
    [Crossref] [Google Scholar]
  52. 52.
    Foster AW, Robinson NJ. 2011.. Promiscuity and preferences of metallothioneins: the cell rules. . BMC Biol. 9::25
    [Crossref] [Google Scholar]
  53. 53.
    Foster AW, Young TR, Chivers PT, Robinson NJ. 2022.. Protein metalation in biology. . Curr. Opin. Chem. Biol. 66::102095
    [Crossref] [Google Scholar]
  54. 54.
    Fraústo da Silva JJR, Williams RJP. 2001.. The Biological Chemistry of the Elements. Oxford, UK:: Oxford Univ. Press
    [Google Scholar]
  55. 55.
    Gao F, Dubos C. 2021.. Transcriptional integration of plant responses to iron availability. . J. Exp. Bot. 72::205670
    [Crossref] [Google Scholar]
  56. 56.
    Gao F, Robe K, Bettembourg M, Navarro N, Rofidal V, et al. 2020.. The transcription factor bHLH121 interacts with bHLH105 (ILR3) and its closest homologs to regulate iron homeostasis in Arabidopsis. . Plant Cell 32::50824
    [Crossref] [Google Scholar]
  57. 57.
    García MJ, Angulo M, Romera FJ, Lucena C, Pérez-Vicente R. 2022.. A shoot derived long distance iron signal may act upstream of the IMA peptides in the regulation of Fe deficiency responses in Arabidopsis thaliana roots. . Front. Plant Sci. 13::971773
    [Crossref] [Google Scholar]
  58. 58.
    Gilbert N. 2009.. Environment: the disappearing nutrient. . Nature 461::71618
    [Crossref] [Google Scholar]
  59. 59.
    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::95363
    [Crossref] [Google Scholar]
  60. 60.
    Haas CE, Rodionov DA, Kropat J, Malasarn D, Merchant SS, de Crécy-Lagard V. 2009.. A subset of the diverse COG0523 family of putative metal chaperones is linked to zinc homeostasis in all kingdoms of life. . BMC Genom. 10::470
    [Crossref] [Google Scholar]
  61. 61.
    Hanikenne M, Kroymann J, Trampczynska A, Bernal M, Motte P, et al. 2013.. Hard selective sweep and ectopic gene conversion in a gene cluster affording environmental adaptation. . PLOS Genet. 9::e1003707 61. Provides insights into how natural selection acted on a metal homeostasis gene.
    [Crossref] [Google Scholar]
  62. 62.
    Hanikenne M, Talke IN, Haydon MJ, Lanz C, Nolte A, et al. 2008.. Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. . Nature 453::39195
    [Crossref] [Google Scholar]
  63. 63.
    Harbort CJ, Hashimoto M, Inoue H, Niu Y, Guan R, et al. 2020.. Root-secreted coumarins and the microbiota interact to improve iron nutrition in Arabidopsis. . Cell Host Microbe 28::82537.e6
    [Crossref] [Google Scholar]
  64. 64.
    Hassinen VH, Tervahauta AI, Schat H, Kärenlampi SO. 2011.. Plant metallothioneins—metal chelators with ROS scavenging activity?. Plant Biol. 13::22532
    [Crossref] [Google Scholar]
  65. 65.
    Haydon MJ, Cobbett CS. 2007.. A novel major facilitator superfamily protein at the tonoplast influences zinc tolerance and accumulation in Arabidopsis. . Plant Physiol. 143::170519
    [Crossref] [Google Scholar]
  66. 66.
    Haydon MJ, Kawachi M, Wirtz M, Hillmer S, Hell R, Krämer U. 2012.. Vacuolar nicotianamine has critical and distinct roles under iron deficiency and for zinc sequestration in Arabidopsis. . Plant Cell 24::72437 66. Example of intracellular metal routing through the partitioning of a chelator molecule.
    [Crossref] [Google Scholar]
  67. 67.
    Haynes WM, Lide DR, Bruno TJ. 2016.. CRC Handbook of Chemistry and Physics: A Ready-Reference Book of Chemical and Physical Data. Boca Raton, Florida:: CRC Press
    [Google Scholar]
  68. 68.
    Heim MA, Jakoby M, Werber M, Martin C, Weisshaar B, Bailey PC. 2003.. The basic helix-loop-helix transcription factor family in plants: a genome-wide study of protein structure and functional diversity. . Mol. Biol. Evol. 20::73547
    [Crossref] [Google Scholar]
  69. 69.
    Hider R, Aviles MV, Chen Y-L, Latunde-Dada GO. 2021.. The role of GSH in intracellular iron trafficking. . Int. J. Mol. Sci. 22::1278
    [Crossref] [Google Scholar]
  70. 70.
    Hong S, Kim SA, Guerinot ML, McClung CR. 2013.. Reciprocal interaction of the circadian clock with the iron homeostasis network in Arabidopsis. . Plant Physiol. 161::893903
    [Crossref] [Google Scholar]
  71. 71.
    Horger AC, Fones HN, Preston GM. 2013.. The current status of the elemental defense hypothesis in relation to pathogens. . Front. Plant Sci. 4::395
    [Crossref] [Google Scholar]
  72. 72.
    Hulshof CM, Spasojevic MJ. 2020.. The edaphic control of plant diversity. . Glob. Ecol. Biogeogr. 29::163450
    [Crossref] [Google Scholar]
  73. 73.
    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::132739
    [Crossref] [Google Scholar]
  74. 74.
    Imlay JA. 2006.. Iron-sulphur clusters and the problem with oxygen. . Mol. Microbiol. 59::107382
    [Crossref] [Google Scholar]
  75. 75.
    Irving H, Williams RJP. 1948.. Order of stability of metal complexes. . Nature 162::74647
    [Crossref] [Google Scholar]
  76. 76.
    Jaffe BD, Ketterer ME, Shuster SM. 2018.. Elemental allelopathy by an arsenic hyperaccumulating fern, Pteris vittata L. . J. Plant Ecol. 11::55359
    [Crossref] [Google Scholar]
  77. 77.
    Jang S, Imlay JA. 2007.. Micromolar intracellular hydrogen peroxide disrupts metabolism by damaging iron-sulfur enzymes. . J. Biol. Chem. 282::92937
    [Crossref] [Google Scholar]
  78. 78.
    Jaquinod M, Villiers F, Kieffer-Jaquinod S, Hugouvieux V, Bruley C, et al. 2007.. A proteomics dissection of Arabidopsis thaliana vacuoles isolated from cell culture. . Mol. Cell Proteom. 6::394412
    [Crossref] [Google Scholar]
  79. 79.
    Jiang X, Stockwell BR, Conrad M. 2021.. Ferroptosis: mechanisms, biology and role in disease. . Nat. Rev. Mol. Cell Biol. 22::26682
    [Crossref] [Google Scholar]
  80. 80.
    Kambe T, Taylor KM, Fu D. 2021.. Zinc transporters and their functional integration in mammalian cells. . J. Biol. Chem. 296::100320
    [Crossref] [Google Scholar]
  81. 81.
    Kang HG, Foley RC, Onate-Sanchez L, Lin C, Singh KB. 2003.. Target genes for OBP3, a Dof transcription factor, include novel basic helix-loop-helix domain proteins inducible by salicylic acid. . Plant J. 35::36272
    [Crossref] [Google Scholar]
  82. 82.
    Kazemi-Dinan A, Thomaschky S, Stein RJ, Krämer U, Müller C. 2014.. Zinc and cadmium hyperaccumulation act as deterrents towards specialist herbivores and impede the performance of a generalist herbivore. . New Phytol. 202::62839
    [Crossref] [Google Scholar]
  83. 83.
    Kehrer JP. 2000.. The Haber-Weiss reaction and mechanisms of toxicity. . Toxicology 149::4350
    [Crossref] [Google Scholar]
  84. 84.
    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::226376
    [Crossref] [Google Scholar]
  85. 85.
    Kim SA, LaCroix IS, Gerber SA, Guerinot ML. 2019.. The iron deficiency response in Arabidopsis thaliana requires the phosphorylated transcription factor URI. . PNAS 116::2493342
    [Crossref] [Google Scholar]
  86. 86.
    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::129598
    [Crossref] [Google Scholar]
  87. 87.
    Klaumann S, Nickolaus SD, Furst SH, Starck S, Schneider S, et al. 2011.. The tonoplast copper transporter COPT5 acts as an exporter and is required for interorgan allocation of copper in Arabidopsis thaliana. . New Phytol. 192::393404
    [Crossref] [Google Scholar]
  88. 88.
    Knoll AH, Nowak MA. 2017.. The timetable of evolution. . Sci. Adv. 3::e1603076
    [Crossref] [Google Scholar]
  89. 89.
    Kobayashi T. 2019.. Understanding the complexity of iron sensing and signaling cascades in plants. . Plant Cell Physiol. 60::144046
    [Crossref] [Google Scholar]
  90. 90.
    Kobayashi T, Nagasaka S, Senoura T, Itai RN, Nakanishi H, Nishizawa NK. 2013.. Iron-binding haemerythrin RING ubiquitin ligases regulate plant iron responses and accumulation. . Nat. Commun. 4::2792
    [Crossref] [Google Scholar]
  91. 91.
    Koffler BE, Bloem E, Zellnig G, Zechmann B. 2013.. High resolution imaging of subcellular glutathione concentrations by quantitative immunoelectron microscopy in different leaf areas of Arabidopsis. . Micron 45::11928
    [Crossref] [Google Scholar]
  92. 92.
    Korshunova YO, Eide D, Gregg Clark W, Lou Guerinot M, Pakrasi HB. 1999.. The IRT1 protein from Arabidopsis thaliana is a metal transporter with a broad substrate range. . Plant Mol. Biol. 40::3744
    [Crossref] [Google Scholar]
  93. 93.
    Kozhevnikova AD, Seregin IV, Erlikh NT, Shevyreva TA, Andreev IM, et al. 2014.. Histidine-mediated xylem loading of zinc is a species-wide character in Noccaea caerulescens. . New Phytol. 203::50819
    [Crossref] [Google Scholar]
  94. 94.
    Krämer U. 2010.. Metal hyperaccumulation in plants. . Annu. Rev. Plant Biol. 61::51734
    [Crossref] [Google Scholar]
  95. 95.
    Krämer U. 2018.. Conceptualizing plant systems evolution. . Curr. Opin. Plant Biol. 42::6675
    [Crossref] [Google Scholar]
  96. 96.
    Krämer U, Clemens S. 2005.. Functions and homeostasis of zinc, copper, and nickel in plants. . In Molecular Biology of Metal Homeostasis and Detoxification, ed. MJ Tamás, E Martinoia , 21671. Heidelberg, Ger:.: Springer
    [Google Scholar]
  97. 97.
    Krämer U, Cotter-Howells JD, Charnock JM, Baker AJM, Smith JAC. 1996.. Free histidine as a metal chelator in plants that accumulate nickel. . Nature 379::63538
    [Crossref] [Google Scholar]
  98. 98.
    Kropat J, Tottey S, Birkenbihl RP, Depege N, Huijser P, Merchant SS. 2005.. A regulator of nutritional copper signaling in Chlamydomonas is an SBP domain protein that recognizes the GTAC core of copper response element. . PNAS 102::1873035
    [Crossref] [Google Scholar]
  99. 99.
    Kumar RK, Chu H-H, Abundis C, Vasques K, Rodriguez DC, et al. 2017.. Iron-nicotianamine transporters are required for proper long distance iron signaling. . Plant Physiol. 175::125468
    [Crossref] [Google Scholar]
  100. 100.
    Kuo W-Y, Huang C-H, Jinn T-L. 2013.. Chaperonin 20 might be an iron chaperone for superoxide dismutase in activating iron superoxide dismutase (FeSOD). . Plant Signal. Behav. 8::e23074
    [Crossref] [Google Scholar]
  101. 101.
    Langridge P. 2022.. Micronutrient toxicity and deficiency. . In Wheat Improvement: Food Security in a Changing Climate, ed. MP Reynolds, H-J Braun , pp. 43349. Cham, Switz.:: Springer Intern.
    [Google Scholar]
  102. 102.
    Lanquar V, Grossmann G, Vinkenborg JL, Merkx M, Thomine S, Frommer WB. 2014.. Dynamic imaging of cytosolic zinc in Arabidopsis roots combining FRET sensors and RootChip technology. . New Phytol. 202::198208
    [Crossref] [Google Scholar]
  103. 103.
    Lanquar V, Ramos MS, Lelievre 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::198699
    [Crossref] [Google Scholar]
  104. 104.
    Lay-Pruitt KS, Wang W, Prom UTC, Pandey A, Zheng L, Rouached H. 2022.. A tale of two players: the role of phosphate in iron and zinc homeostatic interactions. . Planta 256::23
    [Crossref] [Google Scholar]
  105. 105.
    Lee G, Ahmadi H, Quintana J, Syllwasschy L, Janina N, et al. 2021.. Constitutively enhanced genome integrity maintenance and direct stress mitigation characterize transcriptome of extreme stress-adapted Arabidopsis halleri. . Plant J. 108::896911
    [Crossref] [Google Scholar]
  106. 106.
    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::116273
    [Crossref] [Google Scholar]
  107. 107.
    Lekeux G, Laurent C, Joris M, Jadoul A, Jiang D, et al. 2018.. di-Cysteine motifs in the C-terminus of plant HMA4 proteins confer nanomolar affinity for zinc and are essential for HMA4 function in vivo. . J. Exp. Bot. 69::554760
    [Google Scholar]
  108. 108.
    Lešková A, Giehl RFH, Hartmann A, Fargašová A, von Wirén N. 2017.. Heavy metals induce iron deficiency responses at different hierarchic and regulatory levels. . Plant Physiol. 174::164868
    [Crossref] [Google Scholar]
  109. 109.
    Li M, Cao L, Mwimba M, Zhou Y, Li L, et al. 2019.. Comprehensive mapping of abiotic stress inputs into the soybean circadian clock. . PNAS 116::2384049
    [Crossref] [Google Scholar]
  110. 110.
    Li Y, Lu CK, Li CY, Lei RH, Pu MN, et al. 2021.. IRON MAN interacts with BRUTUS to maintain iron homeostasis in Arabidopsis. . PNAS 118::e2109063118 110. Describes how possible Fe sensors and IMA/FEP peptides may act to regulate transcriptional Fe deficiency responses.
    [Crossref] [Google Scholar]
  111. 111.
    Lichtblau DM, Schwarz B, Baby D, Endres C, Sieberg C, Bauer P. 2022.. The iron deficiency-regulated small protein effector FEP3/IRON MAN1 modulates interaction of BRUTUS-LIKE1 with bHLH subgroup IVc and POPEYE transcription factors. . Front. Plant Sci. 13::930049
    [Crossref] [Google Scholar]
  112. 112.
    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::13743 112. Provides evidence for Zn sensor functions of two transcription factors regulating Zn deficiency responses.
    [Crossref] [Google Scholar]
  113. 113.
    Lindsay WL, Schwab AP. 1982.. The chemistry of iron in soils and its availability to plants. . J. Plant Nutr. 5::82140
    [Crossref] [Google Scholar]
  114. 114.
    Loladze I. 2014.. Hidden shift of the ionome of plants exposed to elevated CO2 depletes minerals at the base of human nutrition. . eLife 3::e02245
    [Crossref] [Google Scholar]
  115. 115.
    Long TA, Tsukagoshi H, Busch W, Lahner B, Salt DE, Benfey PN. 2010.. The bHLH transcription factor POPEYE regulates response to iron deficiency in Arabidopsis roots. . Plant Cell 22::221936
    [Crossref] [Google Scholar]
  116. 116.
    Ma Z, Jacobsen FE, Giedroc DP. 2009.. Coordination chemistry of bacterial metal transport and sensing. . Chem. Rev. 109::464481
    [Crossref] [Google Scholar]
  117. 117.
    Macomber L, Imlay JA. 2009.. The iron-sulfur clusters of dehydratases are primary intracellular targets of copper toxicity. . PNAS 106::834449
    [Crossref] [Google Scholar]
  118. 118.
    Maio N, Lafont BAP, Sil D, Li Y, Bollinger JM Jr., et al. 2021.. Fe-S cofactors in the SARS-CoV-2 RNA-dependent RNA polymerase are potential antiviral targets. . Science 373::23641
    [Crossref] [Google Scholar]
  119. 119.
    Maliandi MV, Busi MV, Turowski VR, Leaden L, Araya A, Gomez-Casati DF. 2011.. The mitochondrial protein frataxin is essential for heme biosynthesis in plants. . FEBS J. 278::47081
    [Crossref] [Google Scholar]
  120. 120.
    Mankotia S, Singh D, Monika K, Kalra M, Meena H, et al. 2023.. ELONGATED HYPOCOTYL 5 regulates BRUTUS and affects iron acquisition and homeostasis in Arabidopsis thaliana. . Plant J. 114::126784
    [Crossref] [Google Scholar]
  121. 121.
    Maret W. 2009.. Molecular aspects of human cellular zinc homeostasis: redox control of zinc potentials and zinc signals. . Biometals 22::14957
    [Crossref] [Google Scholar]
  122. 122.
    Marschner H, Marschner P. 2012.. Marschner's Mineral Nutrition of Higher Plants. Waltham, MA:: Elsevier/Academic
    [Google Scholar]
  123. 123.
    Martin-Barranco A, Spielmann J, Dubeaux G, Vert G, Zelazny E. 2020.. Dynamic control of the high-affinity iron uptake complex in root epidermal cells. . Plant Physiol. 184::123650
    [Crossref] [Google Scholar]
  124. 124.
    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::74859
    [Crossref] [Google Scholar]
  125. 125.
    Maurer F, Naranjo Arcos MA, Bauer P. 2014.. Responses of a triple mutant defective in three iron deficiency-induced BASIC HELIX-LOOP-HELIX genes of the subgroup Ib(2) to iron deficiency and salicylic acid. . PLOS ONE 9::e99234
    [Crossref] [Google Scholar]
  126. 126.
    Mendoza-Cozatl DG, Xie Q, Akmakjian GZ, Jobe TO, Patel A, et al. 2014.. OPT3 is a component of the iron-signaling network between leaves and roots and misregulation of OPT3 leads to an over-accumulation of cadmium in seeds. . Mol. Plant 7::145569
    [Crossref] [Google Scholar]
  127. 127.
    Merchant SS, Allen MD, Kropat J, Moseley JL, Long JC, et al. 2006.. Between a rock and a hard place: trace element nutrition in Chlamydomonas. . Biochim. Biophys. Acta Mol. Cell Res. 1763::57894
    [Crossref] [Google Scholar]
  128. 128.
    Mohiley A, Tielbörger K, Seifan M, Gruntman M. 2020.. The role of biotic interactions in determining metal hyperaccumulation in plants. . Funct. Ecol. 34::65868
    [Crossref] [Google Scholar]
  129. 129.
    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::894904
    [Crossref] [Google Scholar]
  130. 130.
    Moreno-Jiménez E, Maestre FT, Flagmeier M, Guirado E, Berdugo M, et al. 2023.. Soils in warmer and less developed countries have less micronutrients globally. . Glob. Chang. Biol. 29::52232
    [Crossref] [Google Scholar]
  131. 131.
    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::332638
    [Crossref] [Google Scholar]
  132. 132.
    Myrach T, Zhu A, Witte C-P. 2017.. The assembly of the plant urease activation complex and the essential role of the urease accessory protein G (UreG) in delivery of nickel to urease. . J. Biol. Chem. 292::1455665
    [Crossref] [Google Scholar]
  133. 133.
    Netz DJA, Stith CM, Stümpfig M, Köpf G, Vogel D, et al. 2011.. Eukaryotic DNA polymerases require an iron-sulfur cluster for the formation of active complexes. . Nat. Chem. Biol. 8::12532
    [Crossref] [Google Scholar]
  134. 134.
    Nieboer E, Richardson DHS. 1980.. The replacement of the nondescript term ‘heavy metals’ by a biologically and chemically significant classification of metal ions. . Environ. Pollut. Ser. B Chem. Phys. 1::326
    [Crossref] [Google Scholar]
  135. 135.
    Nozoye T, Nagasaka S, Kobayashi T, Takahashi M, Sato Y, et al. 2011.. Phytosiderophore efflux transporters are crucial for iron acquisition in graminaceous plants. . J. Biol. Chem. 286::544654
    [Crossref] [Google Scholar]
  136. 136.
    O'Halloran TV, Culotta VC. 2000.. Metallochaperones, an intracellular shuttle service for metal ions. . J. Biol. Chem. 275::2505760
    [Crossref] [Google Scholar]
  137. 137.
    Okada S, Lei GJ, Yamaji N, Huang S, Ma JF, et al. 2022.. FE UPTAKE-INDUCING PEPTIDE1 maintains Fe translocation by controlling Fe deficiency response genes in the vascular tissue of Arabidopsis. . Plant Cell Environ. 45::332237
    [Crossref] [Google Scholar]
  138. 138.
    Olsen LI, Hansen TH, Larue C, Osterberg JT, Hoffmann RD, et al. 2016.. Mother-plant-mediated pumping of zinc into the developing seed. . Nat. Plants 2::16036
    [Crossref] [Google Scholar]
  139. 139.
    Osman D, Cooke A, Young TR, Deery E, Robinson NJ, Warren MJ. 2021.. The requirement for cobalt in vitamin B12: a paradigm for protein metalation. . Biochim. Biophys. Acta Mol. Cell Res. 1868::118896
    [Crossref] [Google Scholar]
  140. 140.
    Osman D, Martini MA, Foster AW, Chen J, Scott AJP, et al. 2019.. Bacterial sensors define intracellular free energies for correct enzyme metalation. . Nat. Chem. Biol. 15::24149
    [Crossref] [Google Scholar]
  141. 141.
    Osman D, Robinson NJ. 2023.. Protein metalation in a nutshell. . FEBS Lett. 597::14150
    [Crossref] [Google Scholar]
  142. 142.
    Palmer CM, Guerinot ML. 2009.. Facing the challenges of Cu, Fe and Zn homeostasis in plants. . Nat. Chem. Biol. 5::33340
    [Crossref] [Google Scholar]
  143. 143.
    Pasquini M, Grosjean N, Hixson KK, Nicora CD, Yee EF, et al. 2022.. Zng1 is a GTP-dependent zinc transferase needed for activation of methionine aminopeptidase. . Cell Rep. 39::110834
    [Crossref] [Google Scholar]
  144. 144.
    Perea-Garcia A, Andres-Borderia A, Mayo de Andres S, Sanz A, Davis AM, et al. 2016.. Modulation of copper deficiency responses by diurnal and circadian rhythms in Arabidopsis thaliana. . J. Exp. Bot. 67::391403
    [Crossref] [Google Scholar]
  145. 145.
    Philpott CC. 2012.. Coming into view: eukaryotic iron chaperones and intracellular iron delivery. . J. Biol. Chem. 287::1351823
    [Crossref] [Google Scholar]
  146. 146.
    Pottier M, Dumont J, Masclaux-Daubresse C, Thomine S. 2019.. Autophagy is essential for optimal translocation of iron to seeds in Arabidopsis. . J. Exp. Bot. 70::85969
    [Google Scholar]
  147. 147.
    Przybyla-Toscano J, Boussardon C, Law SR, Rouhier N, Keech O. 2021.. Gene atlas of iron-containing proteins in Arabidopsis thaliana. . Plant J. 106::25874
    [Crossref] [Google Scholar]
  148. 148.
    Quintana J, Bernal M, Scholle M, Holländer-Czytko H, Nguyen NT, et al. 2022.. Root-to-shoot iron partitioning in Arabidopsis requires IRON-REGULATED TRANSPORTER1 (IRT1) protein but not its iron(II) transport function. . Plant J. 109::9921013
    [Crossref] [Google Scholar]
  149. 149.
    Rae TD, Schmidt PJ, Pufahl RA, Culotta VC, O'Halloran TV. 1999.. Undetectable intracellular free copper: the requirement of a copper chaperone for superoxide dismutase. . Science 284::8058
    [Crossref] [Google Scholar]
  150. 150.
    Rajniak J, Giehl RFH, Chang E, Murgia I, von Wirén N, Sattely ES. 2018.. Biosynthesis of redox-active metabolites in response to iron deficiency in plants. . Nat. Chem. Biol. 14::44250
    [Crossref] [Google Scholar]
  151. 151.
    Remy E, Cabrito TR, Batista RA, Hussein MA, Teixeira MC, et al. 2014.. Intron retention in the 5′UTR of the novel ZIF2 transporter enhances translation to promote zinc tolerance in Arabidopsis. . PLOS Genet. 10::e1004375
    [Crossref] [Google Scholar]
  152. 152.
    Richau KH, Kozhevnikova AD, Seregin IV, Vooijs R, Koevoets PL, et al. 2009.. Chelation by histidine inhibits the vacuolar sequestration of nickel in roots of the hyperaccumulator Thlaspi caerulescens. . New Phytol. 183::10616
    [Crossref] [Google Scholar]
  153. 153.
    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::206279
    [Crossref] [Google Scholar]
  154. 154.
    Robinson NJ, Procter CM, Connolly EL, Guerinot ML. 1999.. A ferric-chelate reductase for iron uptake from soils. . Nature 397::69497
    [Crossref] [Google Scholar]
  155. 155.
    Rodríguez-Celma J, Connorton JM, Kruse I, Green RT, Franceschetti M, et al. 2019.. Arabidopsis BRUTUS-LIKE E3 ligases negatively regulate iron uptake by targeting transcription factor FIT for recycling. . PNAS 116::1758491
    [Crossref] [Google Scholar]
  156. 156.
    Rodríguez-Celma J, Lin WD, Fu GM, Abadia J, Lopez-Millan AF, Schmidt W. 2013.. Mutually exclusive alterations in secondary metabolism are critical for the uptake of insoluble iron compounds by Arabidopsis and Medicago truncatula. . Plant Physiol. 162::147385
    [Crossref] [Google Scholar]
  157. 157.
    Rodríguez-Celma J, Tsai YH, Wen TN, Wu YC, Curie C, Schmidt W. 2016.. Systems-wide analysis of manganese deficiency-induced changes in gene activity of Arabidopsis roots. . Sci. Rep. 6::35846
    [Crossref] [Google Scholar]
  158. 158.
    Roschzttardtz H, Séguéla-Arnaud M, Briat J-F, Vert G, Curie C. 2011.. The FRD3 citrate effluxer promotes iron nutrition between symplastically disconnected tissues throughout Arabidopsis development. . Plant Cell 23::272537
    [Crossref] [Google Scholar]
  159. 159.
    Safiri S, Kolahi A-A, Noori M, Nejadghaderi SA, Karamzad N, et al. 2021.. Burden of anemia and its underlying causes in 204 countries and territories, 1990–2019: results from the Global Burden of Disease Study 2019. . J. Hematol. Oncol. 14::185
    [Crossref] [Google Scholar]
  160. 160.
    Salomé PA, Oliva M, Weigel D, Krämer U. 2013.. Circadian clock adjustment to plant iron status depends on chloroplast and phytochrome function. . EMBO J. 32::51123
    [Crossref] [Google Scholar]
  161. 161.
    Salt DE, Baxter I, Lahner B. 2008.. Ionomics and the study of the plant ionome. . Annu. Rev. Plant Biol. 59::70933
    [Crossref] [Google Scholar]
  162. 162.
    Sancenón V, Puig S, Mateu-Andrés I, Dorcey E, Thiele DJ, Peñarrubia L. 2004.. The Arabidopsis copper transporter COPT1 functions in root elongation and pollen development. . J. Biol. Chem. 279::1534855
    [Crossref] [Google Scholar]
  163. 163.
    Sancenon V, Puig S, Mira H, Thiele DJ, Peñarrubia L. 2003.. Identification of a copper transporter family in Arabidopsis thaliana. . Plant Mol. Biol. 51::57787
    [Crossref] [Google Scholar]
  164. 164.
    Santi S, Schmidt W. 2009.. Dissecting iron deficiency-induced proton extrusion in Arabidopsis roots. . New Phytol. 183::107284
    [Crossref] [Google Scholar]
  165. 165.
    Schaaf G, Honsbein A, Meda AR, Kirchner S, Wipf D, von Wirén N. 2006.. AtIREG2 encodes a tonoplast transport protein involved in iron-dependent nickel detoxification in Arabidopsis thaliana roots. . J. Biol. Chem. 281::2553240
    [Crossref] [Google Scholar]
  166. 166.
    Schaedler TA, Thornton JD, Kruse I, Schwarzländer M, Meyer AJ, et al. 2014.. A conserved mitochondrial ATP-binding cassette transporter exports glutathione polysulfide for cytosolic metal cofactor assembly. . J. Biol. Chem. 289::2326474
    [Crossref] [Google Scholar]
  167. 167.
    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::892910
    [Google Scholar]
  168. 168.
    Schuler M, Rellán-Álvarez R, Fink-Straube C, Abadía J, Bauer P. 2012.. Nicotianamine functions in the phloem-based transport of iron to sink organs, in pollen development and pollen tube growth in Arabidopsis. . Plant Cell 24::2380400
    [Crossref] [Google Scholar]
  169. 169.
    Schulten A, Krämer U. 2017.. Interactions between copper homeostasis and metabolism in plants. . In Progress in Botany Vol. 79, ed. FM Cánovas, U Lüttge, R Matyssek , pp. 11146. Cham, Switz.:: Springer Intern.
    [Google Scholar]
  170. 170.
    Schulten A, Pietzenuk B, Quintana J, Scholle M, Feil R, et al. 2021.. Energy status-promoted growth and development of Arabidopsis require copper deficiency response transcriptional regulator SPL7. . Plant Cell 34::387398
    [Crossref] [Google Scholar]
  171. 171.
    Seebach H, Radow G, Brunek M, Schulz F, Piotrowski M, Krämer U. 2023.. Arabidopsis nicotianamine synthases comprise a common core-NAS domain fused to a variable autoinhibitory C terminus. . J. Biol. Chem. 299::104732
    [Crossref] [Google Scholar]
  172. 172.
    Shaul O, Hilgemann DW, de-Almeida-Engler J, Van Montagu M, Inzé D, Galili G. 1999.. Cloning and characterization of a novel Mg2+/H+ exchanger. . EMBO J. 18::397380
    [Crossref] [Google Scholar]
  173. 173.
    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::133346
    [Crossref] [Google Scholar]
  174. 174.
    Sinclair SA, Larue C, Bonk L, Khan A, Castillo-Michel H, et al. 2017.. Etiolated seedling development requires repression of photomorphogenesis by a small cell-wall-derived dark signal. . Curr. Biol. 27::340318.e7
    [Crossref] [Google Scholar]
  175. 175.
    Sinclair SA, Senger T, Talke IN, Cobbett CS, Haydon MJ, Krämer U. 2018.. Systemic upregulation of MTP2- and HMA2-mediated Zn partitioning to the shoot supplements local Zn deficiency responses. . Plant Cell 30::246379
    [Crossref] [Google Scholar]
  176. 176.
    Sivitz AB, Hermand V, Curie C, Vert G. 2012.. Arabidopsis bHLH100 and bHLH101 control iron homeostasis via a FIT-independent pathway. . PLOS ONE 7::e44843
    [Crossref] [Google Scholar]
  177. 177.
    Slessarev EW, Lin Y, Bingham NL, Johnson JE, Dai Y, et al. 2016.. Water balance creates a threshold in soil pH at the global scale. . Nature 540::56769
    [Crossref] [Google Scholar]
  178. 178.
    Smethurst DGJ, Shcherbik N. 2021.. Interchangeable utilization of metals: new perspectives on the impacts of metal ions employed in ancient and extant biomolecules. . J. Biol. Chem. 297::101374
    [Crossref] [Google Scholar]
  179. 179.
    Sommer F, Kropat J, Malasarn D, Grossoehme NE, Chen X, et al. 2010.. The CRR1 nutritional copper sensor in Chlamydomonas contains two distinct metal-responsive domains. . Plant Cell 22::4098113 179. Characterizes possible Cu sensor functions of Cu deficiency response–regulating transcription factors in photosynthetic organisms.
    [Crossref] [Google Scholar]
  180. 180.
    Song W-Y, Choi KS, Kim DY, Geisler M, Park J, et al. 2010.. Arabidopsis PCR2 is a zinc exporter involved in both zinc extrusion and long-distance zinc transport. . Plant Cell 22::223752
    [Crossref] [Google Scholar]
  181. 181.
    Song WY, Mendoza-Cozatl DG, Lee Y, Schroeder JI, Ahn SN, et al. 2014.. Phytochelatin–metal(loid) transport into vacuoles shows different substrate preferences in barley and Arabidopsis. . Plant Cell Environ. 37::1192201
    [Crossref] [Google Scholar]
  182. 182.
    Song WY, Park J, Mendoza-Cozatl DG, Suter-Grotemeyer M, Shim D, et al. 2010.. Arsenic tolerance in Arabidopsis is mediated by two ABCC-type phytochelatin transporters. . PNAS 107::2118792
    [Crossref] [Google Scholar]
  183. 183.
    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::125265
    [Crossref] [Google Scholar]
  184. 184.
    Stacey MG, Koh S, Becker J, Stacey G. 2002.. AtOPT3, a member of the oligopeptide transporter family, is essential for embryo development in Arabidopsis. . Plant Cell 14::2799811
    [Crossref] [Google Scholar]
  185. 185.
    Stacey MG, Patel A, McClain WE, Mathieu M, Remley M, et al. 2008.. The Arabidopsis AtOPT3 protein functions in metal homeostasis and movement of iron to developing seeds. . Plant Physiol. 146::589601
    [Crossref] [Google Scholar]
  186. 186.
    Stanton C, Sanders D, Krämer U, Podar D. 2022.. Zinc in plants: integrating homeostasis and biofortification. . Mol. Plant 15::6585
    [Crossref] [Google Scholar]
  187. 187.
    Stark JM. 1994.. Causes of soil nutrient heterogeneity at different scales. . In Exploitation of Environmental Heterogeneity by Plants: Ecophysical Processes Above- and Belowground, ed. MM Caldwell, RW Pearcy , pp. 25584. Boston:: Academic
    [Google Scholar]
  188. 188.
    Stein RJ, Höreth S, de Melo JRF, Syllwasschy L, Lee G, et al. 2017.. Relationships between soil and leaf mineral composition are element-specific, environment-dependent and geographically structured in the emerging model Arabidopsis halleri. . New Phytol. 213::127486 188. A field survey of both leaf and rhizosphere composition; establishes a comprehensive collection of genotypes.
    [Crossref] [Google Scholar]
  189. 189.
    Stringlis IA, de Jonge R, Pieterse CMJ. 2019.. The age of coumarins in plant–microbe interactions. . Plant Cell Physiol. 60::140519
    [Crossref] [Google Scholar]
  190. 190.
    Stringlis IA, Yu K, Feussner K, de Jonge R, Van Bentum S, et al. 2018.. MYB72-dependent coumarin exudation shapes root microbiome assembly to promote plant health. . PNAS 115::E521322 190. Mechanistic insights into the functioning and roles of root Fe deficiency responses induced by microbes.
    [Crossref] [Google Scholar]
  191. 191.
    Talke IN, Hanikenne M, Krämer U. 2006.. Zinc-dependent global transcriptional control, transcriptional deregulation, and higher gene copy number for genes in metal homeostasis of the hyperaccumulator Arabidopsis halleri. . Plant Physiol. 142::14867
    [Crossref] [Google Scholar]
  192. 192.
    Tanaka N, Fujiwara T, Tomioka R, Krämer U, Kawachi M, Maeshima M. 2015.. Characterization of the histidine-rich loop of Arabidopsis vacuolar membrane zinc transporter AtMTP1 as a sensor of zinc level in the cytosol. . Plant Cell Physiol. 56::51019
    [Crossref] [Google Scholar]
  193. 193.
    Tennstedt P, Peisker D, Bottcher C, Trampczynska A, Clemens S. 2009.. Phytochelatin synthesis is essential for the detoxification of excess zinc and contributes significantly to the accumulation of zinc. . Plant Physiol. 149::93848
    [Crossref] [Google Scholar]
  194. 194.
    Thomine S, Wang R, Ward JM, Crawford NM, Schroeder JI. 2000.. Cadmium and iron transport by members of a plant metal transporter family in Arabidopsis with homology to Nramp genes. . PNAS 97::499196
    [Crossref] [Google Scholar]
  195. 195.
    Tissot N, Robe K, Gao F, Grant-Grant S, Boucherez J, et al. 2019.. Transcriptional integration of the responses to iron availability by the bHLH factor ILR3. . New Phytol. 223::143346
    [Crossref] [Google Scholar]
  196. 196.
    Tottey S, Waldron KJ, Firbank SJ, Reale B, Bessant C, et al. 2008.. Protein-folding location can regulate manganese-binding versus copper- or zinc-binding. . Nature 455::113842
    [Crossref] [Google Scholar]
  197. 197.
    Tsang T, Davis CI, Brady DC. 2021.. Copper biology. . Curr. Biol. 31::R42127
    [Crossref] [Google Scholar]
  198. 198.
    Tsvetkov P, Coy S, Petrova B, Dreishpoon M, Verma A, et al. 2022.. Copper induces cell death by targeting lipoylated TCA cycle proteins. . Science 375::125461
    [Crossref] [Google Scholar]
  199. 199.
    Turowski VR, Aknin C, Maliandi MV, Buchensky C, Leaden L, et al. 2015.. Frataxin is localized to both the chloroplast and mitochondrion and is involved in chloroplast Fe-S protein function in Arabidopsis. . PLOS ONE 10::e0141443
    [Crossref] [Google Scholar]
  200. 200.
    van de Mortel JE, Schat H, Moerland PD, Ver Loren van Themaat E, van der Ent S, et al. 2008.. Expression differences for genes involved in lignin, glutathione and sulphate metabolism in response to cadmium in Arabidopsis thaliana and the related Zn/Cd-hyperaccumulator Thlaspi caerulescens. . Plant Cell Environ. 31::30124
    [Crossref] [Google Scholar]
  201. 201.
    Vélez-Bermúdez IC, Schmidt W. 2022.. How plants recalibrate cellular iron homeostasis. . Plant Cell Physiol. 63::15462
    [Crossref] [Google Scholar]
  202. 202.
    Vert GA, Briat JF, Curie C. 2003.. Dual regulation of the Arabidopsis high-affinity root iron uptake system by local and long-distance signals. . Plant Physiol. 132::796804
    [Crossref] [Google Scholar]
  203. 203.
    Vert GA, Grotz N, Dedaldechamp 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::122333
    [Crossref] [Google Scholar]
  204. 204.
    von Wirén N, Klair S, Bansal S, Briat J-F, Khodr H, et al. 1999.. Nicotianamine chelates both FeIII and FeII. Implications for metal transport in plants. . Plant Physiol. 119::110714
    [Crossref] [Google Scholar]
  205. 205.
    Vose PB. 1982.. Iron nutrition in plants: a world overview. . J. Plant Nutr. 5::23349
    [Crossref] [Google Scholar]
  206. 206.
    Watanabe T, Broadley MR, Jansen S, White PJ, Takada J, et al. 2007.. Evolutionary control of leaf element composition in plants. . New Phytol. 174::51623
    [Crossref] [Google Scholar]
  207. 207.
    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::144658
    [Crossref] [Google Scholar]
  208. 208.
    Waters BM, McInturf SA, Stein RJ. 2012.. Rosette iron deficiency transcript and microRNA profiling reveals links between copper and iron homeostasis in Arabidopsis thaliana. . J. Exp. Bot. 63::590318
    [Crossref] [Google Scholar]
  209. 209.
    Wątły J, Łuczkowski M, Padjasek M, Krężel A. 2021.. Phytochelatins as a dynamic system for Cd(II) buffering from the micro- to femtomolar range. . Inorg. Chem. 60::465775
    [Crossref] [Google Scholar]
  210. 210.
    Weber M, Trampczynska A, Clemens S. 2006.. Comparative transcriptome analysis of toxic metal responses in Arabidopsis thaliana and the Cd2+-hypertolerant facultative metallophyte Arabidopsis halleri. . Plant Cell Environ. 29::95063
    [Crossref] [Google Scholar]
  211. 211.
    Weiss A, Murdoch CC, Edmonds KA, Jordan MR, Monteith AJ, et al. 2022.. Zn-regulated GTPase metalloprotein activator 1 modulates vertebrate zinc homeostasis. . Cell 185::214863.e27
    [Crossref] [Google Scholar]
  212. 212.
    Wessells KR, Brown KH. 2012.. Estimating the global prevalence of zinc deficiency: results based on zinc availability in national food supplies and the prevalence of stunting. . PLOS ONE 7::e50568
    [Crossref] [Google Scholar]
  213. 213.
    Wintz H, Fox T, Wu YY, Feng V, Chen W, et al. 2003.. Expression profiles of Arabidopsis thaliana in mineral deficiencies reveal novel transporters involved in metal homeostasis. . J. Biol. Chem. 278::4764453
    [Crossref] [Google Scholar]
  214. 214.
    Wu Y, Zhang D, Chu JY, Boyle P, Wang Y, et al. 2012.. The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid. . Cell Rep. 1::63947
    [Crossref] [Google Scholar]
  215. 215.
    Xu FF, Imlay JA. 2012.. Silver(I), mercury(II), cadmium(II), and zinc(II) target exposed enzymic iron-sulfur clusters when they toxify Escherichia coli. . Appl. Environ. Microbiol. 78::361421
    [Crossref] [Google Scholar]
  216. 216.
    Xu Z-R, Cai M-L, Yang Y, You T-T, Ma JF, et al. 2022.. The ferroxidases LPR1 and LPR2 control iron translocation in the xylem of Arabidopsis plants. . Mol. Plant 15::196275
    [Crossref] [Google Scholar]
  217. 217.
    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::34761
    [Crossref] [Google Scholar]
  218. 218.
    Yamasaki K, Kigawa T, Inoue M, Tateno M, Yamasaki T, et al. 2004.. A novel zinc-binding motif revealed by solution structures of DNA-binding domains of Arabidopsis SBP-family transcription factors. . J. Mol. Biol. 337::4963
    [Crossref] [Google Scholar]
  219. 219.
    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::301229
    [Crossref] [Google Scholar]
  220. 220.
    Young TR, Martini MA, Foster AW, Glasfeld A, Osman D, et al. 2021.. Calculating metalation in cells reveals CobW acquires CoII for vitamin B12 biosynthesis while related proteins prefer ZnII. . Nat. Commun. 12::1195
    [Crossref] [Google Scholar]
  221. 221.
    Zamioudis C, Korteland J, Van Pelt JA, van Hamersveld M, Dombrowski N, et al. 2015.. Rhizobacterial volatiles and photosynthesis-related signals coordinate MYB72 expression in Arabidopsis roots during onset of induced systemic resistance and iron-deficiency responses. . Plant J. 84::30922
    [Crossref] [Google Scholar]
  222. 222.
    Zhai Z, Gayomba SR, Jung HI, Vimalakumari NK, Piñeros 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::224964
    [Crossref] [Google Scholar]
  223. 223.
    Zhang H, Krämer U. 2018.. Differential diel translation of transcripts with roles in the transfer and utilization of iron-sulfur clusters in Arabidopsis. . Front. Plant Sci. 9::1641
    [Crossref] [Google Scholar]
  224. 224.
    Zhang H, Quintana J, Ütkür K, Adrian L, Hawer H, et al. 2022.. Translational fidelity and growth of Arabidopsis require stress-sensitive diphthamide biosynthesis. . Nat. Commun. 13::4009
    [Crossref] [Google Scholar]
  225. 225.
    Zhang H, Zhao X, Li J, Cai H, Deng XW, Li L. 2014.. MicroRNA408 is critical for the HY5-SPL7 gene network that mediates the coordinated response to light and copper. . Plant Cell 26::493353
    [Crossref] [Google Scholar]
  226. 226.
    Zhao CR, Ikka T, Sawaki Y, Kobayashi Y, Suzuki Y, et al. 2009.. Comparative transcriptomic characterization of aluminum, sodium chloride, cadmium and copper rhizotoxicities in Arabidopsis thaliana. . BMC Plant Biol. 9::32
    [Crossref] [Google Scholar]
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  • Article Type: Review Article