Protein Biochemistry and Expression Regulation of Cadmium/Zinc Pumping ATPases in the Hyperaccumulator Plants Arabidopsis halleri and Noccaea caerulescens
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
28588597
PubMed Central
PMC5438989
DOI
10.3389/fpls.2017.00835
Knihovny.cz E-zdroje
- Klíčová slova
- QISH, RT-qPCR, cadmium, heavy metal ATPase, metal hyperaccumulator plants, zinc,
- Publikační typ
- časopisecké články MeSH
P1B-ATPases are decisive for metal accumulation phenotypes, but mechanisms of their regulation are only partially understood. Here, we studied the Cd/Zn transporting ATPases NcHMA3 and NcHMA4 from Noccaea caerulescens as well as AhHMA3 and AhHMA4 from Arabidopsis halleri. Protein biochemistry was analyzed on HMA4 purified from roots of N. caerulescens in active state. Metal titration of NcHMA4 protein with an electrochromic dye as charge indicator suggested that HMA4 reaches maximal ATPase activity when all internal high-affinity Cd2+ binding sites are occupied. Although HMA4 was reported to be mainly responsible for xylem loading of heavy metals for root to shoot transport, the current study revealed high expression of NcHMA4 in shoots as well. Further, there were additional 20 and 40 kD fragments at replete Zn2+ and toxic Cd2+, but not at deficient Zn2+ concentrations. Altogether, the protein level expression analysis suggested a more multifunctional role of NcHMA4 than previously assumed. Organ-level transcription analysis through quantitative PCR of mRNA in N. caerulescens and A. halleri confirmed the strong shoot expression of both NcHMA4 and AhHMA4. Further, in shoots NcHMA4 was more abundant in 10 μM Zn2+ and AhHMA4 in Zn2+ deficiency. In roots, NcHMA4 was up-regulated in response to deficient Zn2+ when compared to replete Zn2+ and toxic Cd2+ treatment. In both species, HMA3 was much more expressed in shoots than in roots, and HMA3 transcript levels remained rather constant regardless of Zn2+ supply, but were up-regulated by 10 μM Cd2+. Analysis of cellular expression by quantitative mRNA in situ hybridisation showed that in A. halleri, both HMA3 and HMA4 mRNA levels were highest in the mesophyll, while in N. caerulescens they were highest in the bundle sheath of the vein. This is likely related to the different final storage sites for hyperaccumulated metals in both species: epidermis in N. caerulescens, mesophyll in A. halleri.
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Apell H. J., Bersch B. (1987). Oxonol VI as an optical indicator for membrane potentials in lipid vesicles. Biochim. Biophys. Acta 903 480–494. 10.1016/0005-2736(87)90055-1 PubMed DOI
Baker A. J. M., Brooks R. R. (1989). Terrestrial higher plants which hyperaccumulate metallic elements - a review of their distribution, ecology and phytochemistry. Biorecovery 1 81–126.
Becher M., Talke I. N., 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. 37 251–268. 10.1046/j.1365-313X.2003.01959.x PubMed DOI
Bühler R., Stürmer W., Apell H. J., Läuger P. (1991). Charge translocation by the Na, K-pump: I. Kinetics of local field changes studied by time-resolved fluorescence measurements. J. Memb. Biol. 121 141–161. 10.1007/BF01870529 PubMed DOI
Bull P. C., Cox D. W. (1994). Wilson disease and Menkes disease: new handles on heavy metal transport. Trends Genet. 10 246–252. 10.1016/0168-9525(94)90172-4 PubMed DOI
Chaney R. L. (1983). “Plant uptake of inorganic waste,” in Land Treatment of Hazardous Wastes eds Parr J. E., Marsh P. B., Kla J. M. (Park Ridge, IL: Noyes Data Corp; ) 50–76.
Chaney R. L., Angle J. S., McIntosh M. S., Reeves R. D., Li Y. M., Brewer E. P., et al. (2005). Using hyperaccumulator plants to phytoextract Soil Ni and Cd. Z. Naturforsch. C 60 190–198. PubMed
Eren E., Argüello J. M. (2004). Arabidopsis HMA2, a divalent heavy metal-transporting P(IB)-type ATPase, is involved in cytoplasmic Zn2+ homeostasis. Plant Physiol. 136 3712–3723. 10.1104/pp.104.046292 PubMed DOI PMC
Gourdon P., Liu X. Y., Skjørringe T., Morth J. P., Møller L. B., Pedersen B. P., et al. (2011). Crystal structure of a copper-transporting PIB-type ATPase. Nature 475 59–64. 10.1038/nature10191 PubMed DOI
Gravot A., Lieutaud A., Verret F., Auroy P., Vavasseur A., Richaud P. (2004). AtHMA3, a plant P1B-ATPase, functions as a Cd/Pb transporter in yeast. FEBS Lett. 561 22–28. 10.1016/S0014-5793(04)00072-9 PubMed DOI
Hall J. L., Williams L. E. (2003). Transition metal transporters in plants. J. Exp. Bot. 54 2601–2613. 10.1093/jxb/erg303 PubMed DOI
Hung Y. H., Layton M. J., Voskoboinik I., Mercer J. F. B., Camakaris J. (2007). Purification and membrane reconstitution of catalytically active Menkes copper-transporting P-type ATPase (MNK; ATP7A). Biochem. J. 401 569–579. 10.1042/BJ20060924 PubMed DOI PMC
Krämer U., Pickering I. J., Prince R. C., Raskin I., Salt D. E. (2000). Subcellular localization and speciation of nickel in hyperaccumulator and non-accumulator Thlaspi species. Plant Physiol. 122 1343–1353. 10.1104/pp.122.4.1343 PubMed DOI PMC
Küpper H., Kochian L. V. (2010). Transcriptional regulation of metal transport genes and mineral nutrition during acclimation to cadmium and zinc in the Cd/Zn hyperaccumulator, Thlaspi caerulescens (Ganges population). New Phytol. 185 114–129. 10.1111/j.1469-8137.2009.03051.x PubMed DOI
Küpper H., Kroneck P. M. H. (2005). “Heavy metal uptake by plants and cyanobacteria,” in Metal Ions in Biological Systems Vol. 44 eds Sigel A., Sigel H., Sigel R. K. O. (New York, NY: Marcel Dekker, Inc; ) 97–142. PubMed
Küpper H., Lombi E., Zhao F. J., McGrath S. P. (2000). Cellular compartmentation of cadmium and zinc in relation to other elements in the hyperaccumulator Arabidopsis halleri. Planta 212 75–84. 10.1007/s004250000366 PubMed DOI
Küpper H., Lombi E., Zhao F. J., Wieshammer G., McGrath S. P. (2001). Cellular compartmentation of nickel in the hyperaccumulators Alyssum lesbiacum, Alyssum bertolonii and Thlaspi goesingense. J. Expt. Bot. 52 2291–2300. 10.1093/jexbot/52.365.2291 PubMed DOI
Küpper H., Parameswaran A., Leitenmaier B., Trtßlek M., Šetlßk I. (2007a). Cadmium-induced inhibition of photosynthesis and long-term acclimation to cadmium stress in the hyperaccumulator Thlaspi caerulescens. New Phytol. 175 655–674. 10.1111/j.1469-8137.2007.02139.x PubMed DOI
Küpper H., Seib L. O., Sivaguru M., Hoekenga O. A., Kochian L. V. (2007b). A method for cellular localization of gene expression via quantitative in situ hybridization in plants. Plant J. 50 159–175. 10.1111/j.1365-313X.2007.03031.x PubMed DOI
Küpper H., Zhao F. J., McGrath S. P. (1999). Cellular compartmentation of zinc in leaves of the hyperaccumulator Thlaspi caerulescens. Plant Physiol. 119 305–311. 10.1104/pp.119.1.305 PubMed DOI PMC
Lasat M. M., Baker A., Kochian L. V. (1996). Physiological characterization of root Zn2+ absorption and translocation to shoots in Zn hyperaccumulator and nonaccumulator species of Thlaspi. Plant Physiol. 112 1715–1722. 10.1104/pp.112.4.1715 PubMed DOI PMC
Leitenmaier B., Küpper H. (2011). Cadmium uptake and sequestration kinetics in individual leaf cell protoplasts of the Cd/Zn hyperaccumulator Thlaspi caerulescens. Plant Cell Environ. 34 208–219. 10.1111/j.1365-3040.2010.02236.x PubMed DOI
Leitenmaier B., Küpper H. (2013). Compartmentation and complexation of metals in hyperaccumulator plants. Front. Plant Sci. 4:374 10.3389/fpls.2013.00374 PubMed DOI PMC
Leitenmaier B., Witt A., Witzke A., Stemke A., Meyer-Klaucke W., Kroneck P. M. H., et al. (2011). Biochemical and biophysical characterisation yields insights into the mechanism of TcHMA4, a Cd/Zn transporting ATPase purified from the hyperaccumulator plant Thlaspi caerulescens. Biochim. Biophys. Acta 1808 2591–2599. 10.1016/j.bbamem.2011.05.010 PubMed DOI
Liu Y., Pilankatta R., Hatori Y., Lewis D., Inesi G. (2010). Comparative features of copper ATPases ATP7A and ATP7B heterologously expressed in COS-1 cells. Biochemistry 49 10006–10012. 10.1021/bi101423j PubMed DOI PMC
Lombi E., Zhao F. J., Dunham S. J., McGrath S. P. (2000). Cadmium accumulation in populations of Thlaspi caerulescens and Thlaspi goesingense. New Phytol. 145 11–20. 10.1046/j.1469-8137.2000.00560.x DOI
Mills R., Krijger G., Baccarini P., Hall J. L., Williams L. (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 PubMed DOI
Mills R. F., Francini A., Ferreira da Rocha P. S. C., Baccarini P. J., Aylett M., Krijger G. C., et al. (2005). The plant P1B-type ATPase AtHMA4 transports Zn and Cd and plays a role in detoxification of transition metals supplied at elevated levels. FEBS Lett. 579 783–791. 10.1016/j.febslet.2004.12.040 PubMed DOI
Miyadate H., Adachi S., Hiraizumi A., Tezuka K., Nakazawa N., Kawamoto T., et al. (2011). OsHMA3, a P1B-type of ATPase affects root-to-shoot cadmium translocation in rice by mediating efflux into vacuoles. New Phytol. 189 190–199. 10.1111/j.1469-8137.2010.03459.x PubMed DOI
Morel M., Crouzet J., Gravot A., Auroy P., Leonhardt N., Vavasseur A., et al. (2009). AtHMA3, a P1B-ATPase allowing Cd/Zn/Co/Pb vacuolar storage in Arabidopsis. Plant Physiol. 149 894–904. 10.1104/pp.108.130294 PubMed DOI PMC
Papoyan A., Kochian L. V. (2004). Identification of Thlaspi caerulescens genes that may be involved in heavy metal hyperaccumulation and tolerance. Characterization of a novel heavy metal transporting ATPase. Plant Physiol. 136 3814–3823. 10.1104/pp.104.044503 PubMed DOI PMC
Parameswaran A., Leitenmaier B., Yang M., Welte W., Kroneck P. M. H., Lutz G., et al. (2007). A native Zn/Cd transporting P1B type ATPase protein from natural overexpression in a Zn/Cd hyperaccumulator plant. Biochem. Biophys. Res. Comm. 364 51–56. 10.1016/j.bbrc.2007.08.105 PubMed DOI
Pfaffl M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45 10.1093/nar/29.9.e45 PubMed DOI PMC
Sinclair S. A., Sherson S. M., Jarvis R., Camakaris J., Cobbett C. S. (2007). The use of the zinc-fluorophore, Zinpyr-1, in the study of zinc homeostasis in Arabidopsis roots. New Phytol. 174 39–45. 10.1111/j.1469-8137.2007.02030.x PubMed DOI
Solioz M., Vulpe C. D. (1996). CPx type ATPases: a class of P-type ATPases that pump heavy metals. Trends Biochem. Sci. 21 237–241. 10.1016/S0968-0004(96)20016-7 PubMed DOI
Tezuka K., Miyadate H., Kato K., Kodama I., Matsumoto S., Kawamoto T., et al. (2010). A single recessive gene controls cadmium translocation in the cadmium hyperaccumulating rice cultivar Cho-Ko-Koku. Theor. Appl. Genet. 120 1175–1182. 10.1007/s00122-009-1244-6 PubMed DOI
Ueno D., Koyama E., Yamaji N., Ma J. F. (2011). Physiological, genetic, and molecular characterization of a high-Cd-accumulating rice cultivar, Jarjan. J. Exp. Bot. 62 2265–2272. 10.1093/jxb/erq383 PubMed DOI
Ueno D., Yamaji N., Kono I., Huang C. F., Ando T., Yano M., et al. (2010). Gene limiting cadmium accumulation in rice. Proc. Natl. Acad. Sci. U.S.A. 107 16500–16505. 10.1073/pnas.1005396107 PubMed DOI PMC
Van de Mortel J. E., Villanueva L. A., 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 PubMed DOI PMC
Verret F., Gravot A., Auroy P., Leonhardt N., David P., Nussaume L., et al. (2004). Over-expression 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 PubMed DOI
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 PubMed DOI PMC
Weber M., Harada E., Vess C., Von Roepenack-Lahaye E., Clemens S. (2004). Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotianamine synthase, a ZIP transporter and other genes as potential metal hyperaccumulation factors. Plant J. 37 269–281. 10.1046/j.1365-313X.2003.01960.x PubMed DOI
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 PubMed DOI
Wong C. K., Cobbett C. S. (2009). HMA P-type ATPases are the major mechanism for root-to-shoot translocation in Arabidopsis thaliana. New Phytol. 181 71–78. 10.1111/j.1469-8137.2008.02638.x PubMed DOI
Zhang Z., Yu Q., Du H., Ai W., Yao X., Mendoza-Cózatl D. G., et al. (2016). Enhanced cadmium efflux and root-to-shoot translocation are conserved in the hyperaccumulator Sedum alfredii (Crassulaceae family). FEBS Lett. 590 1757–1764. 10.1002/1873-3468 PubMed DOI