Home LiteratureArticle Details
PMID: 25941529 Published · epublish English Journal Article Review

Temporal aspects of copper homeostasis and its crosstalk with hormones.

Frontiers in plant science ·Vol. 6 ·2015-00-00 ·Pages 255

Peñarrubia L, Romero P, Carrió-Seguí A, Andrés-Bordería A, Moreno J, Sanz A

Abstract

To cope with the dual nature of copper as being essential and toxic for cells, plants temporarily adapt the expression of copper homeostasis components to assure its delivery to cuproproteins while avoiding the interference of potential oxidative damage derived from both copper uptake and photosynthetic reactions during light hours. The circadian clock participates in the temporal organization of coordination of plant nutrition adapting metabolic responses to the daily oscillations. This timely control improves plant fitness and reproduction and holds biotechnological potential to drive increased crop yields. Hormonal pathways, including those of abscisic acid, gibberellins, ethylene, auxins, and jasmonates are also under direct clock and light control, both in mono and dicotyledons. In this review, we focus on copper transport in Arabidopsis thaliana and Oryza sativa and the presumable role of hormones in metal homeostasis matching nutrient availability to growth requirements and preventing metal toxicity. The presence of putative hormone-dependent regulatory elements in the promoters of copper transporters genes suggests hormonal regulation to match special copper requirements during plant development. Spatial and temporal processes that can be affected by hormones include the regulation of copper uptake into roots, intracellular trafficking and compartmentalization, and long-distance transport to developing vegetative and reproductive tissues. In turn, hormone biosynthesis and signaling are also influenced by copper availability, which suggests reciprocal regulation subjected to temporal control by the central oscillator of the circadian clock. This transcriptional regulatory network, coordinates environmental and hormonal signaling with developmental pathways to allow enhanced micronutrient acquisition efficiency.

Keywords
Arabidopsis thaliana Oryza sativa circadian clock copper homeostasis copper transporters hormone biosynthesis hormone signaling oxidative stress
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Peñarrubia Lola
Laboratory of Plant Molecular Biology, Department of Biochemistry and Molecular Biology, University of Valencia, Valencia Spain.
Romero Paco
Laboratory of Plant Molecular Biology, Department of Biochemistry and Molecular Biology, University of Valencia, Valencia Spain.
Carrió-Seguí Angela
Laboratory of Plant Molecular Biology, Department of Biochemistry and Molecular Biology, University of Valencia, Valencia Spain.
Andrés-Bordería Amparo
Laboratory of Plant Molecular Biology, Department of Biochemistry and Molecular Biology, University of Valencia, Valencia Spain.
Moreno Joaquín
Laboratory of Plant Molecular Biology, Department of Biochemistry and Molecular Biology, University of Valencia, Valencia Spain.
Sanz Amparo
Department of Plant Biology, University of Valencia, Valencia Spain.
References (169)
169 references, click to expand
  1. Sugars, the clock and transition to flowering.
    Front Plant Sci. 2013 Feb 14;4:22 PMID: 23420760
  2. TOC1 functions as a molecular switch connecting the circadian clock with plant responses to drought.
    EMBO J. 2009 Dec 2;28(23 ):3745-57 PMID: 19816401
  3. Possible role of light in the maintenance of EIN3/EIL1 stability in Arabidopsis seedlings.
    Biochem Biophys Res Commun. 2006 Nov 17;350(2):484-91 PMID: 17011517
  4. Molecular and functional analyses of COPT/Ctr-type copper transporter-like gene family in rice.
    BMC Plant Biol. 2011 Apr 21;11:69 PMID: 21510855
  5. Exogenously induced expression of ethylene biosynthesis, ethylene perception, phospholipase D, and Rboh-oxidase genes in broccoli seedlings.
    J Exp Bot. 2010 Jul;61(12):3475-91 PMID: 20581125
  6. Plasma membrane depolarization induced by abscisic acid in Arabidopsis suspension cells involves reduction of proton pumping in addition to anion channel activation, which are both Ca2+ dependent.
    Plant Physiol. 2004 May;135(1):231-43 PMID: 15141069
  7. Analysis of transcription factor HY5 genomic binding sites revealed its hierarchical role in light regulation of development.
    Plant Cell. 2007 Mar;19(3):731-49 PMID: 17337630
  8. Cytosolic zinc buffering and muffling: their role in intracellular zinc homeostasis.
    Metallomics. 2010 May;2(5):306-17 PMID: 21069178
  9. Do PFT1 and HY5 interact in regulation of sulfate assimilation by light in Arabidopsis?
    FEBS Lett. 2014 Apr 2;588(7):1116-21 PMID: 24583010
  10. HY5 is a point of convergence between cryptochrome and cytokinin signalling pathways in Arabidopsis thaliana.
    Plant J. 2007 Feb;49(3):428-41 PMID: 17217468
  11. Stable isotopes of Cu and Zn in higher plants: evidence for Cu reduction at the root surface and two conceptual models for isotopic fractionation processes.
    Environ Sci Technol. 2012 Mar 6;46(5):2652-60 PMID: 22296233
  12. Sulfate availability affects ABA levels and germination response to ABA and salt stress in Arabidopsis thaliana.
    Plant J. 2014 Feb;77(4):604-15 PMID: 24330104
  13. RESPONSIVE-TO-ANTAGONIST1, a Menkes/Wilson disease-related copper transporter, is required for ethylene signaling in Arabidopsis.
    Cell. 1999 Apr 30;97(3):383-93 PMID: 10319818
  14. Circadian regulation of ion channels and their functions.
    J Neurochem. 2009 Aug;110(4):1150-69 PMID: 19549279
  15. Subcellular metal imaging identifies dynamic sites of Cu accumulation in Chlamydomonas.
    Nat Chem Biol. 2014 Dec;10(12):1034-42 PMID: 25344811
  16. Cell biology of molybdenum in plants and humans.
    Biochim Biophys Acta. 2012 Sep;1823(9):1568-79 PMID: 22370186
  17. Annotations and functional analyses of the rice WRKY gene superfamily reveal positive and negative regulators of abscisic acid signaling in aleurone cells.
    Plant Physiol. 2005 Jan;137(1):176-89 PMID: 15618416
  18. Undetectable intracellular free copper: the requirement of a copper chaperone for superoxide dismutase.
    Science. 1999 Apr 30;284(5415):805-8 PMID: 10221913
  19. Interactions between circadian and hormonal signalling in plants.
    Plant Mol Biol. 2009 Mar;69(4):419-27 PMID: 18855103
  20. The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid.
    Cell Rep. 2012 Jun 28;1(6):639-47 PMID: 22813739
  21. Iron is involved in the maintenance of circadian period length in Arabidopsis.
    Plant Physiol. 2013 Mar;161(3):1409-20 PMID: 23307650
  22. Response to copper excess in Arabidopsis thaliana: Impact on the root system architecture, hormone distribution, lignin accumulation and mineral profile.
    Plant Physiol Biochem. 2010 Aug;48(8):673-82 PMID: 20542443
  23. Differential regulation of EIN3 stability by glucose and ethylene signalling in plants.
    Nature. 2003 Oct 2;425(6957):521-5 PMID: 14523448
  24. Functional characterisation of Arabidopsis SPL7 conserved protein domains suggests novel regulatory mechanisms in the Cu deficiency response.
    BMC Plant Biol. 2014 Aug 30;14:231 PMID: 25207797
  25. The Arabidopsis transcription factor HY5 integrates light and hormone signaling pathways.
    Plant J. 2004 Apr;38(2):332-47 PMID: 15078335
  26. Multiple phytohormones influence distinct parameters of the plant circadian clock.
    Genes Cells. 2006 Dec;11(12):1381-92 PMID: 17121545
  27. Circadian clock control of endocrine factors.
    Nat Rev Endocrinol. 2014 Aug;10(8):466-75 PMID: 24863387
  28. The CRR1 nutritional copper sensor in Chlamydomonas contains two distinct metal-responsive domains.
    Plant Cell. 2010 Dec;22(12):4098-113 PMID: 21131558
  29. Identification of genes of the plant-specific transcription-factor families cooperatively regulated by ethylene and jasmonate in Arabidopsis thaliana.
    J Plant Res. 2006 Jul;119(4):407-13 PMID: 16820983
  30. Functions of amine oxidases in plant development and defence.
    Trends Plant Sci. 2006 Feb;11(2):80-8 PMID: 16406305
  31. Ethylene modulates the role of NONEXPRESSOR OF PATHOGENESIS-RELATED GENES1 in cross talk between salicylate and jasmonate signaling.
    Plant Physiol. 2009 Apr;149(4):1797-809 PMID: 19176718
  32. Two different novel cis-acting elements of erd1, a clpA homologous Arabidopsis gene function in induction by dehydration stress and dark-induced senescence.
    Plant J. 2003 Jan;33(2):259-70 PMID: 12535340
  33. 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. 2012 Sep 28;287(40):33252-67 PMID: 22865877
  34. A copper cofactor for the ethylene receptor ETR1 from Arabidopsis.
    Science. 1999 Feb 12;283(5404):996-8 PMID: 9974395
  35. XAP5 CIRCADIAN TIMEKEEPER regulates ethylene responses in aerial tissues of Arabidopsis.
    Plant Physiol. 2011 Feb;155(2):988-99 PMID: 21163961
  36. SQUAMOSA promoter binding protein-like7 regulated microRNA408 is required for vegetative development in Arabidopsis.
    Plant J. 2013 Apr;74(1):98-109 PMID: 23289771
  37. Increasing CO2 threatens human nutrition.
    Nature. 2014 Jun 5;510(7503):139-42 PMID: 24805231
  38. Copper amine oxidase expression in defense responses to wounding and Ascochyta rabiei invasion.
    Plant Physiol. 2002 Mar;128(3):865-75 PMID: 11891243
  39. Deregulated copper transport affects Arabidopsis development especially in the absence of environmental cycles.
    Plant Physiol. 2010 May;153(1):170-84 PMID: 20335405
  40. Function of PPR proteins in plastid gene expression.
    RNA Biol. 2013;10(9):1446-56 PMID: 23771106
  41. A member of the heavy metal P-type ATPase OsHMA5 is involved in xylem loading of copper in rice.
    Plant Physiol. 2013 Nov;163(3):1353-62 PMID: 24064929
  42. Multiple layers of posttranslational regulation refine circadian clock activity in Arabidopsis.
    Plant Cell. 2014 Jan;26(1):79-87 PMID: 24481076
  43. Sequential expression of two 1-aminocyclopropane-1-carboxylate synthase genes in response to biotic and abiotic stresses in potato (Solanum tuberosum L.) leaves.
    Plant Mol Biol. 1997 Dec;35(6):683-8 PMID: 9426590
  44. Enhancing crop yield with the use of N-based fertilizers co-applied with plant hormones or growth regulators.
    J Sci Food Agric. 2015 Jul;95(9):1777-85 PMID: 25267003
  45. Transcriptome sequencing identifies SPL7-regulated copper acquisition genes FRO4/FRO5 and the copper dependence of iron homeostasis in Arabidopsis.
    Plant Cell. 2012 Feb;24(2):738-61 PMID: 22374396
  46. Iron around the clock.
    Plant Sci. 2014 Jul;224:112-9 PMID: 24908512
  47. Auxin and the integration of environmental signals into plant root development.
    Ann Bot. 2013 Dec;112(9):1655-65 PMID: 24136877
  48. Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks.
    Curr Opin Plant Biol. 2006 Aug;9(4):436-42 PMID: 16759898
  49. Functional dissection of a sugar-repressed alpha-amylase gene (RAmy1 A) promoter in rice embryos.
    FEBS Lett. 1998 Feb 13;423(1):81-5 PMID: 9506846
  50. Different stresses, similar morphogenic responses: integrating a plethora of pathways.
    Plant Cell Environ. 2009 Feb;32(2):158-69 PMID: 19021890
  51. The final split: the regulation of anther dehiscence.
    J Exp Bot. 2011 Mar;62(5):1633-49 PMID: 21325605
  52. The Arabidopsis heavy metal P-type ATPase HMA5 interacts with metallochaperones and functions in copper detoxification of roots.
    Plant J. 2006 Jan;45(2):225-36 PMID: 16367966
  53. COPPER AMINE OXIDASE1 (CuAO1) of Arabidopsis thaliana contributes to abscisic acid- and polyamine-induced nitric oxide biosynthesis and abscisic acid signal transduction.
    Mol Plant. 2011 Jul;4(4):663-78 PMID: 21471330
  54. The intracellular Arabidopsis COPT5 transport protein is required for photosynthetic electron transport under severe copper deficiency.
    Plant J. 2011 Mar;65(6):848-60 PMID: 21281364
  55. Analysis of Arabidopsis glucose insensitive growth mutants reveals the involvement of the plastidial copper transporter PAA1 in glucose-induced intracellular signaling.
    Plant Physiol. 2012 Jul;159(3):1001-12 PMID: 22582133
  56. Transition metals in plant photosynthesis.
    Metallomics. 2013 Sep;5(9):1090-109 PMID: 23739807
  57. A tidal wave of signals: calcium and ROS at the forefront of rapid systemic signaling.
    Trends Plant Sci. 2014 Oct;19(10):623-30 PMID: 25088679
  58. AtCCS is a functional homolog of the yeast copper chaperone Ccs1/Lys7.
    FEBS Lett. 2005 Apr 25;579(11):2307-12 PMID: 15848163
  59. Calcium- and potassium-permeable plasma membrane transporters are activated by copper in Arabidopsis root tips: linking copper transport with cytosolic hydroxyl radical production.
    Plant Cell Environ. 2013 Apr;36(4):844-55 PMID: 23046313
  60. Structure and function of copper uptake transporters.
    Curr Top Membr. 2012;69:97-112 PMID: 23046648
  61. Roles of nitric oxide in alleviating heavy metal toxicity in plants.
    Arch Biochem Biophys. 2010 May;497(1-2):13-20 PMID: 20193657
  62. Metabolic regulation of circadian clocks.
    Semin Cell Dev Biol. 2013 May;24(5):414-21 PMID: 23538134
  63. Copper homeostasis influences the circadian clock in Arabidopsis.
    Plant Signal Behav. 2010 Oct;5(10):1237-40 PMID: 20861682
  64. Plant hormone signaling lightens up: integrators of light and hormones.
    Curr Opin Plant Biol. 2010 Oct;13(5):571-7 PMID: 20739215
  65. A role for the GCC-box in jasmonate-mediated activation of the PDF1.2 gene of Arabidopsis.
    Plant Physiol. 2003 Jun;132(2):1020-32 PMID: 12805630
  66. Emerging roles of microRNAs in the mediation of drought stress response in plants.
    J Exp Bot. 2013 Aug;64(11):3077-86 PMID: 23814278
  67. COPASI--a COmplex PAthway SImulator.
    Bioinformatics. 2006 Dec 15;22(24):3067-74 PMID: 17032683
  68. Placing metal micronutrients in context: transport and distribution in plants.
    Curr Opin Plant Biol. 2009 Jun;12(3):299-306 PMID: 19481498
  69. Inhibition of blue light-dependent H+ pumping by abscisic acid through hydrogen peroxide-induced dephosphorylation of the plasma membrane H+-ATPase in guard cell protoplasts.
    Plant Physiol. 2004 Dec;136(4):4150-8 PMID: 15563626
  70. Mechanisms of cross talk between gibberellin and other hormones.
    Plant Physiol. 2007 Jul;144(3):1240-6 PMID: 17616507
  71. Molecular mechanisms of copper uptake and distribution.
    Curr Opin Chem Biol. 2002 Apr;6(2):171-80 PMID: 12039001
  72. ABA-mediated transcriptional regulation in response to osmotic stress in plants.
    J Plant Res. 2011 Jul;124(4):509-25 PMID: 21416314
  73. Lysosome-related organelles as mediators of metal homeostasis.
    J Biol Chem. 2014 Oct 10;289(41):28129-36 PMID: 25160625
  74. Network discovery pipeline elucidates conserved time-of-day-specific cis-regulatory modules.
    PLoS Genet. 2008 Feb;4(2):e14 PMID: 18248097
  75. EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis.
    Science. 1999 Jun 25;284(5423):2148-52 PMID: 10381874
  76. Interaction with Cu²⁺ disrupts the RNA binding affinities of RNA recognition motif containing protein.
    Biochem Biophys Res Commun. 2014 Feb 7;444(2):116-20 PMID: 24434156
  77. Comparative transcriptome of diurnally oscillating genes and hormone-responsive genes in Arabidopsis thaliana: insight into circadian clock-controlled daily responses to common ambient stresses in plants.
    Plant Cell Physiol. 2008 Mar;49(3):481-7 PMID: 18202002
  78. Regulation of ribonucleotide reductase in response to iron deficiency.
    Mol Cell. 2011 Dec 9;44(5):759-69 PMID: 22152479
  79. MicroRNA408 is critical for the HY5-SPL7 gene network that mediates the coordinated response to light and copper.
    Plant Cell. 2014 Dec;26(12):4933-53 PMID: 25516599
  80. Diurnal variation of cytokinin, auxin and abscisic acid levels in tobacco leaves.
    J Exp Bot. 2005 Nov;56(421):2877-83 PMID: 16157652
  81. Current understanding on ethylene signaling in plants: the influence of nutrient availability.
    Plant Physiol Biochem. 2013 Dec;73:128-38 PMID: 24095919
  82. Regulation of copper homeostasis by micro-RNA in Arabidopsis.
    J Biol Chem. 2007 Jun 1;282(22):16369-78 PMID: 17405879
  83. The WRKY superfamily of plant transcription factors.
    Trends Plant Sci. 2000 May;5(5):199-206 PMID: 10785665
  84. Molybdenum cofactor biosynthesis and molybdenum enzymes.
    Annu Rev Plant Biol. 2006;57:623-47 PMID: 16669776
  85. Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development.
    Genome Biol. 2008;9(8):R130 PMID: 18710561
  86. Early transcriptomic changes induced by magnesium deficiency in Arabidopsis thaliana reveal the alteration of circadian clock gene expression in roots and the triggering of abscisic acid-responsive genes.
    New Phytol. 2010 Jul;187(1):119-31 PMID: 20406411
  87. The transcriptional regulatory network in the drought response and its crosstalk in abiotic stress responses including drought, cold, and heat.
    Front Plant Sci. 2014 May 16;5:170 PMID: 24904597
  88. MicroRNA-mediated systemic down-regulation of copper protein expression in response to low copper availability in Arabidopsis.
    J Biol Chem. 2008 Jun 6;283(23):15932-45 PMID: 18408011
  89. MiR398 and plant stress responses.
    Physiol Plant. 2011 Sep;143(1):1-9 PMID: 21496029
  90. Plant immunity requires conformational changes [corrected] of NPR1 via S-nitrosylation and thioredoxins.
    Science. 2008 Aug 15;321(5891):952-6 PMID: 18635760
  91. Characterization of Arabidopsis thaliana genes encoding functional homologues of the yeast metal chaperone Cox19p, involved in cytochrome c oxidase biogenesis.
    Plant Mol Biol. 2007 Oct;65(3):343-55 PMID: 17712601
  92. A review of metal-catalyzed molecular damage: protection by melatonin.
    J Pineal Res. 2014 May;56(4):343-70 PMID: 24628077
  93. Interaction of light and hormone signals in germinating seeds.
    Plant Mol Biol. 2009 Mar;69(4):463-72 PMID: 19031046
  94. The Arabidopsis abscisic acid response locus ABI4 encodes an APETALA 2 domain protein.
    Plant Cell. 1998 Jun;10(6):1043-54 PMID: 9634591
  95. Plant hormones and nutrient signaling.
    Plant Mol Biol. 2009 Mar;69(4):361-73 PMID: 18688730
  96. Structure of the molybdopterin-bound Cnx1G domain links molybdenum and copper metabolism.
    Nature. 2004 Aug 12;430(7001):803-6 PMID: 15306815
  97. AtCOX17, an Arabidopsis homolog of the yeast copper chaperone COX17.
    Plant Physiol. 2002 Aug;129(4):1852-7 PMID: 12177498
  98. Copper and iron homeostasis in Arabidopsis: responses to metal deficiencies, interactions and biotechnological applications.
    Plant Cell Environ. 2007 Mar;30(3):271-90 PMID: 17263774
  99. Circadian clock adjustment to plant iron status depends on chloroplast and phytochrome function.
    EMBO J. 2013 Feb 20;32(4):511-23 PMID: 23241948
  100. Transcriptional regulation of secondary growth in Arabidopsis thaliana.
    J Exp Bot. 2003 Dec;54(393):2709-22 PMID: 14585825
  101. Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany.
    Ann Bot. 2013 Jun;111(6):1021-58 PMID: 23558912
  102. The Jasmonate-ZIM domain proteins interact with the R2R3-MYB transcription factors MYB21 and MYB24 to affect Jasmonate-regulated stamen development in Arabidopsis.
    Plant Cell. 2011 Mar;23(3):1000-13 PMID: 21447791
  103. Tell me more: roles of NPRs in plant immunity.
    Trends Plant Sci. 2013 Jul;18(7):402-11 PMID: 23683896
  104. A rice WRKY gene encodes a transcriptional repressor of the gibberellin signaling pathway in aleurone cells.
    Plant Physiol. 2004 Apr;134(4):1500-13 PMID: 15047897
  105. Copper-deficiency in Brassica napus induces copper remobilization, molybdenum accumulation and modification of the expression of chloroplastic proteins.
    PLoS One. 2014 Oct 15;9(10):e109889 PMID: 25333918
  106. The bacterial pathogen Xanthomonas oryzae overcomes rice defenses by regulating host copper redistribution.
    Plant Cell. 2010 Sep;22(9):3164-76 PMID: 20852017
  107. Copper and iron homeostasis in plants: the challenges of oxidative stress.
    Antioxid Redox Signal. 2013 Sep 20;19(9):919-32 PMID: 23199018
  108. Shaping a root system: regulating lateral versus primary root growth.
    Trends Plant Sci. 2014 Jul;19(7):426-31 PMID: 24513255
  109. Copper speciation and isotopic fractionation in plants: uptake and translocation mechanisms.
    New Phytol. 2013 Jul;199(2):367-78 PMID: 23600562
  110. SQUAMOSA Promoter Binding Protein-Like7 Is a Central Regulator for Copper Homeostasis in Arabidopsis.
    Plant Cell. 2009 Jan;21(1):347-61 PMID: 19122104
  111. Hidden shift of the ionome of plants exposed to elevated CO₂depletes minerals at the base of human nutrition.
    Elife. 2014 May 07;3:e02245 PMID: 24867639
  112. A dynamic interface between vacuoles and mitochondria in yeast.
    Dev Cell. 2014 Jul 14;30(1):95-102 PMID: 25026036
  113. Copper metallochaperones.
    Annu Rev Biochem. 2010;79:537-62 PMID: 20205585
  114. Molybdenum metabolism in plants.
    Metallomics. 2013 Sep;5(9):1191-203 PMID: 23800757
  115. The Clp protease system is required for copper ion-dependent turnover of the PAA2/HMA8 copper transporter in chloroplasts.
    New Phytol. 2015 Jan;205(2):511-7 PMID: 25262970
  116. SOMNUS, a CCCH-type zinc finger protein in Arabidopsis, negatively regulates light-dependent seed germination downstream of PIL5.
    Plant Cell. 2008 May;20(5):1260-77 PMID: 18487351
  117. 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. 2008 Oct;148(2):969-80 PMID: 18701674
  118. Copper regulates primary root elongation through PIN1-mediated auxin redistribution.
    Plant Cell Physiol. 2013 May;54(5):766-78 PMID: 23396597
  119. Mitochondria and copper homeostasis in plants.
    Mitochondrion. 2014 Nov;19 Pt B:269-74 PMID: 24582977
  120. The tonoplast copper transporter COPT5 acts as an exporter and is required for interorgan allocation of copper in Arabidopsis thaliana.
    New Phytol. 2011 Oct;192(2):393-404 PMID: 21692805
  121. Perception of the plant immune signal salicylic acid.
    Curr Opin Plant Biol. 2014 Aug;20:64-8 PMID: 24840293
  122. The Arabidopsis COPT6 transport protein functions in copper distribution under copper-deficient conditions.
    Plant Cell Physiol. 2013 Aug;54(8):1378-90 PMID: 23766354
  123. Dissecting iron deficiency-induced proton extrusion in Arabidopsis roots.
    New Phytol. 2009;183(4):1072-84 PMID: 19549134
  124. Modelling the widespread effects of TOC1 signalling on the plant circadian clock and its outputs.
    BMC Syst Biol. 2013 Mar 19;7:23 PMID: 23506153
  125. The clock protein CCA1 and the bZIP transcription factor HY5 physically interact to regulate gene expression in Arabidopsis.
    Mol Plant. 2008 Jan;1(1):58-67 PMID: 20031914
  126. Copper chelation and exogenous copper affect circadian clock phase resetting in the suprachiasmatic nucleus in vitro.
    Neuroscience. 2014 Jan 3;256:252-61 PMID: 24161278
  127. Gibberellin biosynthesis and response during Arabidopsis seed germination.
    Plant Cell. 2003 Jul;15(7):1591-604 PMID: 12837949
  128. Phloem small RNAs, nutrient stress responses, and systemic mobility.
    BMC Plant Biol. 2010 Apr 13;10:64 PMID: 20388194
  129. Unravelling molecular responses to moderate dehydration in harvested fruit of sweet orange (Citrus sinensis L. Osbeck) using a fruit-specific ABA-deficient mutant.
    J Exp Bot. 2012 Apr;63(7):2753-67 PMID: 22315241
  130. Reciprocal interaction of the circadian clock with the iron homeostasis network in Arabidopsis.
    Plant Physiol. 2013 Feb;161(2):893-903 PMID: 23250624
  131. Heavy-metal-induced ethylene production in Arabidopsis thaliana.
    J Plant Physiol. 2007 Nov;164(11):1480-8 PMID: 17215058
  132. A null mutation in a bZIP factor confers ABA-insensitivity in Arabidopsis thaliana.
    Plant Cell Physiol. 2000 May;41(5):541-7 PMID: 10929936
  133. Rapid and transient activation of transcription of the ERF3 gene by wounding in tobacco leaves: possible involvement of NtWRKYs and autorepression.
    J Biol Chem. 2004 Dec 31;279(53):55355-61 PMID: 15509567
  134. Light activates the degradation of PIL5 protein to promote seed germination through gibberellin in Arabidopsis.
    Plant J. 2006 Jul;47(1):124-39 PMID: 16740147
  135. CIRCADIAN CLOCK-ASSOCIATED 1 regulates ROS homeostasis and oxidative stress responses.
    Proc Natl Acad Sci U S A. 2012 Oct 16;109(42):17129-34 PMID: 23027948
  136. Circadian clock-dependent gating in ABA signalling networks.
    Protoplasma. 2012 Jul;249(3):445-57 PMID: 21773710
  137. Interactions of the developmental regulator ABI3 with proteins identified from developing Arabidopsis seeds.
    Plant J. 2000 Jan;21(2):143-55 PMID: 10743655
  138. ABI4: versatile activator and repressor.
    Trends Plant Sci. 2013 Mar;18(3):125-32 PMID: 23182343
  139. The Arabidopsis copper transporter COPT1 functions in root elongation and pollen development.
    J Biol Chem. 2004 Apr 9;279(15):15348-55 PMID: 14726516
  140. Interactions between plant circadian clocks and solute transport.
    J Exp Bot. 2011 Apr;62(7):2333-48 PMID: 21378117
  141. The CTR/COPT-dependent copper uptake and SPL7-dependent copper deficiency responses are required for basal cadmium tolerance in A. thaliana.
    Metallomics. 2013 Sep;5(9):1262-75 PMID: 23835944
  142. Structural metal sites in nonclassical zinc finger proteins involved in transcriptional and translational regulation.
    Acc Chem Res. 2014 Aug 19;47(8):2643-50 PMID: 25098749
  143. Identification of a novel cis-acting element conferring sulfur deficiency response in Arabidopsis roots.
    Plant J. 2005 May;42(3):305-14 PMID: 15842617
  144. Transcriptional regulation of Arabidopsis MIR168a and argonaute1 homeostasis in abscisic acid and abiotic stress responses.
    Plant Physiol. 2012 Mar;158(3):1279-92 PMID: 22247272
  145. Evolution of a plant-specific copper chaperone family for chloroplast copper homeostasis.
    Proc Natl Acad Sci U S A. 2014 Dec 16;111(50):E5480-7 PMID: 25468978
  146. Abiotic stress and the plant circadian clock.
    Plant Signal Behav. 2011 Feb;6(2):223-31 PMID: 21325898
  147. A conserved KIN17 curved DNA-binding domain protein assembles with SQUAMOSA PROMOTER-BINDING PROTEIN-LIKE7 to adapt Arabidopsis growth and development to limiting copper availability.
    Plant Physiol. 2014 Feb;164(2):828-40 PMID: 24335506
  148. Involvement of nitric oxide and auxin in signal transduction of copper-induced morphological responses in Arabidopsis seedlings.
    Ann Bot. 2011 Sep;108(3):449-57 PMID: 21856638
  149. Peroxiredoxins are conserved markers of circadian rhythms.
    Nature. 2012 May 16;485(7399):459-64 PMID: 22622569
  150. Signals from chloroplasts converge to regulate nuclear gene expression.
    Science. 2007 May 4;316(5825):715-9 PMID: 17395793
  151. Zinc finger proteins as potential targets for toxic metal ions: differential effects on structure and function.
    Antioxid Redox Signal. 2001 Aug;3(4):625-34 PMID: 11554449
  152. Genome-wide mapping of the HY5-mediated gene networks in Arabidopsis that involve both transcriptional and post-transcriptional regulation.
    Plant J. 2011 Feb;65(3):346-58 PMID: 21265889
  153. Interaction between sugar and abscisic acid signalling during early seedling development in Arabidopsis.
    Plant Mol Biol. 2008 May;67(1-2):151-67 PMID: 18278579
  154. Drought, ozone, ABA and ethylene: new insights from cell to plant to community.
    Plant Cell Environ. 2010 Apr;33(4):510-25 PMID: 19843256
  155. The transcription factor ABI4 is a regulator of mitochondrial retrograde expression of ALTERNATIVE OXIDASE1a.
    Plant Physiol. 2009 Jul;150(3):1286-96 PMID: 19482916
  156. An endogenous F-box protein regulates ARGONAUTE1 in Arabidopsis thaliana.
    Silence. 2010 Jul 12;1(1):15 PMID: 20624295
  157. Facing the challenges of Cu, Fe and Zn homeostasis in plants.
    Nat Chem Biol. 2009 May;5(5):333-40 PMID: 19377460
  158. Arabidopsis copper transport protein COPT2 participates in the cross talk between iron deficiency responses and low-phosphate signaling.
    Plant Physiol. 2013 May;162(1):180-94 PMID: 23487432
  159. Identification of a copper transporter family in Arabidopsis thaliana.
    Plant Mol Biol. 2003 Mar;51(4):577-87 PMID: 12650623
  160. Modulation of environmental responses of plants by circadian clocks.
    Plant Cell Environ. 2007 Mar;30(3):333-49 PMID: 17263778
  161. Mapping the core of the Arabidopsis circadian clock defines the network structure of the oscillator.
    Science. 2012 Apr 6;336(6077):75-9 PMID: 22403178
  162. Expression profiles of Arabidopsis thaliana in mineral deficiencies reveal novel transporters involved in metal homeostasis.
    J Biol Chem. 2003 Nov 28;278(48):47644-53 PMID: 13129917
  163. Copper homeostasis in grapevine: functional characterization of the Vitis vinifera copper transporter 1.
    Planta. 2014 Jul;240(1):91-101 PMID: 24691572
  164. Melatonin: plant growth regulator and/or biostimulator during stress?
    Trends Plant Sci. 2014 Dec;19(12):789-97 PMID: 25156541
  165. Regulation of copper transport in Arabidopsis thaliana: a biochemical oscillator?
    J Biol Inorg Chem. 2010 Jan;15(1):29-36 PMID: 19798519
  166. The role of nutrient availability in regulating root architecture.
    Curr Opin Plant Biol. 2003 Jun;6(3):280-7 PMID: 12753979
  167. Spatiotemporal asymmetric auxin distribution: a means to coordinate plant development.
    Cell Mol Life Sci. 2006 Dec;63(23):2738-54 PMID: 17013565
  168. Social Network: JAZ Protein Interactions Expand Our Knowledge of Jasmonate Signaling.
    Front Plant Sci. 2012 Mar 08;3:41 PMID: 22629274
  169. Circadian rhythms of ethylene emission in Arabidopsis.
    Plant Physiol. 2004 Nov;136(3):3751-61 PMID: 15516515
Article Info
Journal
Frontiers in plant science
Abbr.
Front Plant Sci
ISSN
1664-462X
DOI
10.3389/fpls.2015.00255
Published
2015-00-00
Epub
2015-00-17
Pages
255
Language
English
Region
Switzerland
NLM ID
101568200
PMCID
PMC4400860
External Links
PubMed source DOI: 10.3389/fpls.2015.00255 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2