Ceasar, S. A.; InBioS – PhytoSystems, Functional Genomics and Plant Molecular Imaging, University of Liège, Liège, Belgium, InBioS – Center for Protein Engineering, Biological Macromolecules, University of Liège, Liège, Belgium
Lekeux, Gilles ; InBioS – PhytoSystems, Functional Genomics and Plant Molecular Imaging, University of Liège, Liège, Belgium, InBioS – Center for Protein Engineering, Biological Macromolecules, University of Liège, Liège, Belgium
Motte, Patrick ; Université de Liège - ULiège > Département des sciences de la vie > Génomique fonctionnelle et imagerie moléculaire végétale
Xiao, Z.; Melbourne Dementia Research Centre, Florey Institute of Neuroscience and Mental Health, The University of Melbourne, Parkville, VIC, Australia
Galleni, Moreno ; Université de Liège - ULiège > Département des sciences de la vie > Macromolécules biologiques
Hanikenne, Marc ; Université de Liège - ULiège > Département des sciences de la vie > Génomique fonctionnelle et imagerie moléculaire végétale
Language :
English
Title :
di-Cysteine Residues of the Arabidopsis thaliana HMA4 C-Terminus Are Only Partially Required for Cadmium Transport
Publication date :
2020
Journal title :
Frontiers in Plant Science
eISSN :
1664-462X
Publisher :
Frontiers Media S.A.
Volume :
11
Pages :
560
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
FRIA - Fonds pour la Formation à la Recherche dans l'Industrie et dans l'Agriculture [BE] F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE]
Argüello J. M., (2003). Identification of ion-selectivity determinants in heavy-metal transport P1B-type ATPases. J. Membr. Biol. 195 93–108. 10.1007/s00232-003-2048-2 14692449
Argüello J. M., Eren E., González-Guerrero M., (2007). The structure and function of heavy metal transport P1B-ATPases. BioMetals 20 233–234. 10.1007/s10534-006-9055-6 17219055
Assunção A. G. L., Herrero E., Lin Y.-F., Huettel B., Talukdar S., Smaczniak C., et al. (2010). Arabidopsis thaliana transcription factors bZIP19 and bZIP23 regulate the adaptation to zinc deficiency. Proc. Natl. Acad. Sci. U.S.A. 107 10296–10301. 10.1073/pnas.1004788107 20479230
Barberon M., Geldner N., (2014). Radial transport of nutrients: the plant root as a polarized epithelium. Plant Physiol. 166 528–537. 10.1104/pp.114.246124 25136061
Barberon M., Zelazny E., Robert S., Conéjéro G., Curie C., Friml J., et al. (2011). Monoubiquitin-dependent endocytosis of the iron-regulated transporter 1 (IRT1) transporter controls iron uptake in plants. Proc. Natl. Acad. Sci. U.S.A. 108 E450–E458. 10.1073/pnas.1100659108 21628566
Bernard C., Roosens N., Czernic P., Lebrun M., Verbruggen N., (2004). A novel CPx-ATPase from the cadmium hyperaccumulator Thlaspi caerulescens. FEBS Lett. 569 140–148. 10.1016/j.febslet.2004.05.036 15225623
Buckhout T. J., Yang T. J. W., Schmidt W., (2009). Early iron-deficiency-induced transcriptional changes in Arabidopsis roots as revealed by microarray analyses. BMC Genomics 10:147. 10.1186/1471-2164-10-147 19348669
Bækgaard L., Mikkelsen M. D., Sørensen D. M., Hegelund J. N., Persson D. P., Mills R. F., et al. (2010). A combined Zinc/Cadmium sensor and Zinc/Cadmium export regulator in a heavy metal pump. J. Biol. Chem. 285 31243–31252. 10.1074/jbc.M110.111260 20650903
Castro P. H., Lilay G. H., Munoz-Merida A., Schjoerring J. K., Azevedo H., Assuncao A. G. L., (2017). Phylogenetic analysis of F-bZIP transcription factors indicates conservation of the zinc deficiency response across land plants. Sci. Rep. 7:3806. 10.1038/s41598-017-03903-6 28630437
Charlier J.-B., Polese C., Nouet C., Carnol M., Bosman B., Krämer U., et al. (2015). Zinc triggers a complex transcriptional and post-transcriptional regulation of the metal homeostasis gene FRD3 in Arabidopsis relatives. J. Exp. Bot. 66 3865–3878. 10.1093/jxb/erv188 25900619
Clemens S., Aarts M. G. M., Thomine S., Verbruggen N., (2013). Plant science: the key to preventing slow cadmium poisoning. Trends Plant Sci. 18 92–99. 10.1016/j.tplants.2012.08.003 22981394
Colangelo E. P., Guerinot M. L., (2004). The essential basic helix-loop-helix protein FIT1 is required for the iron deficiency response. Plant Cell 16 3400–3412. 10.1105/tpc.104.024315 15539473
Connolly E. L., Fett J. P., Guerinot M. L., (2002). Expression of the IRT1 metal transporter is controlled by metals at the levels of transcript and protein accumulation. Plant Cell 14 1347–1357. 10.1105/tpc.001263 12084831
Corso M., Schvartzman M. S., Guzzo F., Souard F., Malkowski E., Hanikenne M., et al. (2018). Contrasting cadmium resistance strategies in two metallicolous populations of Arabidopsis halleri. New Phytol. 218 283–297. 10.1111/nph.14948 29292826
Courbot M., Willems G., Motte P., Arvidsson S., Roosens N., Saumitou-Laprade P., et al. (2007). A major quantitative trait locus for cadmium tolerance in Arabidopsis halleri colocalizes with HMA4, a gene encoding a heavy metal ATPase. Plant Physiol. 144 1052–1065. 10.1104/pp.106.095133 17434989
Cun P., Sarrobert C., Richaud P., Chevalier A., Soreau P., Auroy P., et al. (2014). Modulation of Zn/Cd P1B2-ATPase activities in Arabidopsis impacts differently on Zn and Cd contents in shoots and seeds. Metallomics 6 2109–2116. 10.1039/c4mt00182f
Czechowski T., Stitt M., Altmann T., Udvardi M. K., Scheible W.-R., (2005). Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol. 139 5–17. 10.1104/pp.105.063743 16166256
de Seny D., Heinz U., Wommer S., Kiefer M., Meyer-Klaucke W., Galleni M., et al. (2001). Metal ion binding and coordination geometry for wild type and mutants of metallo-β-lactamase from Bacillus cereus 569/H/9 (BcII): a combined thermodynamic, kinetic, and spectroscopic approach. J. Biol. Chem. 276 45065–45078. 10.1074/jbc.M106447200
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.e5–964.e5. 10.1016/j.molcel.2018.02.009 29547723
Halimaa P., Blande D., Baltzi E., Aarts M. G. M., Granlund L., Keinänen M., et al. (2019). Transcriptional effects of cadmium on iron homeostasis differ in calamine accessions of Noccaea caerulescens. Plant J. 97 306–320. 10.1111/tpj.14121 30288820
Hanikenne M., Talke I. N., Haydon M. J., Lanz C., Nolte A., Motte P., et al. (2008). Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 453 391–395. 10.1038/nature06877 18425111
Hellemans J., Mortier G., De Paepe A., Speleman F., Vandesompele J., (2007). qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol. 8:R19. 10.1186/gb-2007-8-2-r19 17291332
Hussain D., Haydon M. J., Wang Y., Wong E., Sherson S. M., Young J., et al. (2004). P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis. Plant Cell 16 1327–1339. 10.1105/tpc.020487 15100400
Inaba S., Kurata R., Kobayashi M., Yamagishi Y., Mori I., Ogata Y., et al. (2015). Identification of putative target genes of bZIP19, a transcription factor essential for Arabidopsis adaptation to Zn deficiency in roots. Plant J. 84 323–334. 10.1111/tpj.12996 26306426
Kocyła A., Pomorski A., Krêżel A., (2015). Molar absorption coefficients and stability constants of metal complexes of 4-(2-pyridylazo)resorcinol (PAR): revisiting common chelating probe for the study of metalloproteins. J. Inorg. Biochem. 152 82–92. 10.1016/j.jinorgbio.2015.08.024 26364130
Krämer U., (2010). Metal hyperaccumulation in plants. Annu. Rev. Plant Biol. 61 517–534. 10.1146/annurev-arplant-042809-112156 20192749
Lane T. W., Morel F. M., (2000). A biological function for cadmium in marine diatoms. Proc. Natl. Acad. Sci. U.S.A. 97 4627–4631. 10.1073/pnas.090091397 10781068
Laurent C., Lekeux G., Ukuwela A. A., Xiao Z., Charlier J.-B., Bosman B., et al. (2016). Metal binding to the N-terminal cytoplasmic domain of the PIB ATPase HMA4 is required for metal transport in Arabidopsis. Plant Mol. Biol. 90 453–466. 10.1007/s11103-016-0429-z 26797794
Lekeux G., Crowet J.-M., Nouet C., Joris M., Jadoul A., Bosman B., et al. (2019). Homology modeling and in vivo functional characterization of the zinc permeation pathway in a heavy metal P-type ATPase. J. Exp. Bot. 70 329–341. 10.1093/jxb/ery353 30418580
Lekeux G., Laurent C., Joris M., Jadoul A., Jiang D., Bosman B., 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 5547–5560. 10.1093/jxb/ery311 30137564
Liedschulte V., Laparra H., Battey J. N. D., Schwaar J. D., Broye H., Mark R., et al. (2017). Impairing both HMA4 homeologs is required for cadmium reduction in tobacco. Plant. Cell Environ. 40 364–377. 10.1111/pce.12870 27880006
Lin Y.-F., Liang H.-M., Yang S.-Y., Boch A., Clemens S., Chen C.-C., et al. (2009). Arabidopsis IRT3 is a zinc-regulated and plasma membrane localized zinc/iron transporter. New Phytol. 182 392–404. 10.1111/j.1469-8137.2009.02766.x 19210716
Merlot S., de la Torre V. S. G., Hanikenne M., (2018). “Physiology and molecular biology of trace element hyperaccumulation,” in Agromining: Farming for Metals, eds Van der Ent A., Echevarria G., Baker A. J. M., Morel J. L., (Cham: Springer International Publishing), 93–116.
Mills R. F., Krijger G. C., Baccarini P. J., Hall J. L., Williams L. E., (2003). Functional expression of AtHMA4, a P1B-type ATPase of the Zn/Co/Cd/Pb subclass. Plant J. 35 164–176. 10.1046/j.1365-313x.2003.01790.x 12848823
Nouet C., Charlier J.-B., Carnol M., Bosman B., Farnir F., Motte P., et al. (2015). Functional analysis of the three HMA4 copies of the metal hyperaccumulator Arabidopsis halleri. J. Exp. Bot. 66 5783–5795. 10.1093/jxb/erv280 26044091
Nriagu J. O., (1988). A silent epidemic of environmental metal poisoning? Environ. Pollut. 50 139–161. 10.1016/0269-7491(88)90189-3 15092656
Pottier M., Oomen R., Picco C., Giraudat J., Scholz-Starke J., Richaud P., et al. (2015). Identification of mutations allowing Natural Resistance associated macrophage proteins (NRAMP) to discriminate against cadmium. Plant J. 83 625–637. 10.1111/tpj.12914 26088788
Rogers E. E., Eide D. J., Guerinot M. L., (2000). Altered selectivity in an Arabidopsis metal transporter. Proc. Natl. Acad. Sci. U.S.A. 97 12356–12360. 10.1073/pnas.210214197 11035780
Rosenzweig A. C., Argüello J. M., (2012). Toward a molecular understanding of metal transport by P1B-Type ATPases. Curr. Top. Membr. 69 113–136. 10.1016/B978-0-12-394390-3.00005-7
Ruijter J. M., Ramakers C., Hoogaars W. M. H., Karlen Y., Bakker O., van den Hoff M. J. B., et al. (2009). Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res. 37:e45. 10.1093/nar/gkp045 19237396
Satarug S., Baker J. R., Urbenjapol S., Haswell-Elkins M., Reilly P. E. B., Williams D. J., et al. (2003). A global perspective on cadmium pollution and toxicity in non-occupationally exposed population. Toxicol. Lett. 137 65–83. 10.1016/S0378-4274(02)00381-8 12505433
Satarug S., Garrett S. H., Sens M. A., Sens D. A., (2010). Cadmium, environmental exposure, and health outcomes. Environ. Health Perspect. 118 182–190. 10.1289/ehp.0901234
Schvartzman M. S., Corso M., Fataftah N., Scheepers M., Nouet C., Bosman B., et al. (2018). Adaptation to high zinc depends on distinct mechanisms in metallicolous populations of Arabidopsis halleri. New Phytol. 218 269–282. 10.1111/nph.14949 29292833
Smith A. T., Smith K. P., Rosenzweig A. C., (2014). Diversity of the metal-transporting P1B-type ATPases. J. Biol. Inorg. Chem. 19 947–960. 10.1007/s00775-014-1129-2 24729073
Talke I. N., 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. 142 148–167. 10.1104/pp.105.076232 16844841
Thomine S., Vert G., (2013). Iron transport in plants: better be safe than sorry. Curr. Opin. Plant Biol. 16 322–327. 10.1016/j.pbi.2013.01.003 23415557
Tocquin P., Corbesier L., Havelange A., Pieltain A., Kurtem E., Bernier G., et al. (2003). A novel high efficiency, low maintenance, hydroponic system for synchronous growth and flowering of Arabidopsis thaliana. BMC Plant Biol. 3:2. 10.1186/1471-2229-3-2 12556248
Tóth G., Hermann T., Da Silva M. R., Montanarella L., (2016). Heavy metals in agricultural soils of the European Union with implications for food safety. Environ. Int. 88 299–309. 10.1016/j.envint.2015.12.017 26851498
van de Mortel J. E., Almar Villanueva L., Schat H., Kwekkeboom J., Coughlan S., Moerland P. D., et al. (2006). Large expression differences in genes for iron and zinc homeostasis, stress response, and lignin biosynthesis distinguish roots of Arabidopsis thaliana and the related metal hyperaccumulator Thlaspi caerulescens. Plant Physiol. 142 1127–1147. 10.1104/pp.106.082073 16998091
Vandesompele J., De Preter K., Pattyn F., Poppe B., Van Roy N., De Paepe A., et al. (2002). Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3:research0034.1. 10.1186/gb-2002-3-7-research0034 12184808
Verret F., Gravot A., Auroy P., Leonhardt N., David P., Nussaume L., et al. (2004). Overexpression of AtHMA4 enhances root-to-shoot translocation of zinc and cadmium and plant metal tolerance. FEBS Lett. 576 306–312. 10.1016/j.febslet.2004.09.023 15498553
Verret F., Gravot A., Auroy P., Preveral S., Forestier C., Vavasseur A., et al. (2005). Heavy metal transport by AtHMA4 involves the N-terminal degenerated metal binding domain and the C-terminal His11 stretch. FEBS Lett. 579 1515–1522. 10.1016/j.febslet.2005.01.065 15733866
Vert G., Grotz N., Dédaldéchamp F., Gaymard F., Guerinot M. L., Briat J.-F., et al. (2002). IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell 14 1223–1233. 10.1105/tpc.001388
Wang K., Sitsel O., Meloni G., Autzen H. E., Andersson M., Klymchuk T., et al. (2014). Structure and mechanism of Zn2+-transporting P-type ATPases. Nature 514 518–522. 10.1038/nature13618 25132545
Williams L. E., Mills R. F., (2005). P1B-ATPases; an ancient family of transition metal pumps with diverse functions in plants. Trends Plant Sci. 10 491–502. 10.1016/j.tplants.2005.08.008 16154798
Wong C. K., Cobbett C. S., (2009). HMA P-type ATPases are the major mechanism for root-to-shoot Cd translocation in Arabidopsis thaliana. New Phytol. 181 71–78. 10.1111/j.1469-8137.2008.02638.x 19076718
Yang T. J. W., Lin W.-D., Schmidt W., (2010). Transcriptional profiling of the Arabidopsis iron deficiency response reveals conserved transition metal homeostasis networks. Plant Physiol. 152 2130–2141. 10.1104/pp.109.152728 20181752
Zimmermann M., Clarke O., Gulbis J. M., Keizer D. W., Jarvis R. S., Cobbett C. S., et al. (2009). Metal binding affinities of Arabidopsis zinc and copper transporters: selectivities match the relative, but not the absolute, affinities of their amino-terminal domains. Biochemistry 48 11640–11654. 10.1021/bi901573b 19883117
