Summary
Soils and waters with high levels of toxic heavy metal(loid)s such as arsenic, cadmium and mercury are detrimental to human and environmental health. These three metal(loid)s are among the Superfund's top 7 priority hazardous substances. Research and applications indicate that uptake of heavy metals into plants via the root system and accumulation of heavy metals in plant shoots could provide a cost effective approach for toxic metal removal and remediation of heavy metal-laden soils and waters. However important genes and pathways that function in heavy metal over-accumulation in plants remain to be identified. In recent research we have made major advances at understanding key mechanisms that function in heavy metal detoxification, transport and accumulation in plants. We will combine powerful genomic, genetic, biochemical and physiological approaches to test new central hypotheses by pursuing the following Specific Aims:
I. Characterize newly identified vacuolar membrane transporters that function in uptake and accumulation of phytochelatin-heavy metal(loid) complexes into plant vacuoles and analyze their bioremediation potential.
II. Understanding the control of heavy metal accumulation and distribution in roots and shoots is critical for engineering of plants for bioremediation. Determine the mechanisms by which a new peptide transporter mutant, opt3, causes hyper-accumulation in roots and under-accumulation of cadmium in plant leaves.
III. Our recent research has shown that heavy metal-chelating and detoxifying thiols undergo long distance transport in plants. However, the plasma membrane transporters for uptake of glutathione (GSH) and phytochelatins (PCs) remain unknown. Using a high-throughput screen we have now identified OPT4 as a putative GSH & PC-Cd transporter. We will characterize OPT4 and additional transporters to determine their underlying GSH/PC-Cd/As transport mechanisms and their functions in heavy metal distribution in plants.
IV. The mechanisms and transcription factors that mediate rapid heavy metal-induced gene expression in plants remain largely unknown, but are important for heavy metal resistance and accumulation. The genes of newly isolated mutants impaired in cadmium-induced gene expression will be identified and their functions characterized. Furthermore, a potent genome-wide approach has been developed and will be pursued to identify and characterize key transcription factors and repressors that control cadmium- and arsenic-induced gene expression. We will work closely with the RTC and CEC in sharing our advances and foremost in translational analyses of our findings for their potential in phytoremediation of contaminated soils and waters.
Roots from Arabidopsis plants that accumulate metals bind to phytochelatins, which are engineered to fluoresce upon association with metals.
Publications
Aleman F., Yazaki J., Lee M., Takahashi Y., Kim A.Y., Li Z., Kinoshita T., Ecker J.R., Schroeder J.I. (2016) An ABA-increased interaction of the PYL6 ABA receptor with MYC2 Transcription Factor: A putative link of ABA and JA signaling. Sci Rep. 6:28941. doi: 10.1038/srep28941.
Yazaki J., Galli M., Kim A.Y., Nito K., Aleman F., Chang K.N., Carvunis A.R., Quan R., Nguyen H., Song L., Alvarez J.M., Huang S.S., Chen H., Ramachandran N., Altmann S., Gutiérrez R.A., Hill D.E., Schroeder J.I., Chory J., LaBaer J., Vidal M., Braun P., Ecker J.R. (2016) Mapping transcription factor interactome networks using HaloTag protein arrays. Proc Natl Acad Sci U S A. 113:E4238-47.
doi: 10.1073/pnas.1603229113.
Suzuki, K., Yamaji, N., Costa, A., Okuma, E., Kobayashi, N. I., Kashiwagi, T., Katsuhara, M., Wang, C., Tanoi, K., Murata, Y., Schroeder, J. I., Ma, J. F., Horie, T. (2016) OsHKT1;4-mediated Na(+) transport in stems contributes to Na(+) exclusion from leaf blades of rice at the reproductive growth stage upon salt stress. BMC Plant Biol. 16(1), 22. doi: 10.1186/s12870-016-0709-4.
Yamamoto Y., Negi J., Wang C., Isogai Y., Schroeder J.I., Iba K. (2016) The Transmembrane Region of Guard Cell SLAC1 Channels Perceives CO2 Signals via an ABA-Independent Pathway in Arabidopsis. Plant Cell. 28:557-67. doi: 10.1105/tpc.15.00583.
Wang, C., Hu, H., Qin, X., Zeise, B., Xu, D., Rappel, W.-J., Boron, W.F., Schroeder, J.I. (2016) Reconstitution of CO2 regulation of SLAC1 anion channel and function of CO2-permeable PIP2;1 aquaporin as CARBONIC ANHYDRASE 4 interactor. Plant Cell. 282: 568-82. doi: 10.1105/tpc.15.00637.
Munemasa, S., Hauser, F., Park, J., Waadt, R., Brandt, B., Schroeder, J. I. (2015) Mechanisms of abscisic acid-mediated control of stomatal aperture. Curr Opin Plant Biol. 28, 154-162.
Engineer, C. B., Hashimoto-Sugimoto, M., Negi, J., Israelsson-Nordström, M., Azoulay-Shemer, T., Rappel, W. J., Iba, K., Schroeder, J. I. (2015) CO2 Sensing and CO2 Regulation of Stomatal Conductance: Advances and Open Questions. Trends Plant Sci. 21(1):16-30. doi: 10.1016/j.tplants.2015.08.014.
Zhang Z., Xie Q., Jobe T.O., Kau A.R., Wang C., Li Y., Qiu B., Wang Q., Mendoza-Cózatl D.G., Schroeder J.I. (2016) Identification of AtOPT4 as a plant glutathione transporter. Mol Plant. 9: 481-4. doi: 10.1016/j.molp.2015.07.013.
Brandt, B., Munemasa, S., Wang, C., Nguyen, D., Yong, T., Yang, P. G., Poretsky, E., Belknap, T. F., Waadt, R., Alemán, F., Schroeder, J. I. (2015) Calcium specificity signaling mechanisms in abscisic acid signal transduction in Arabidopsis guard cells. Elife. 4. doi: 10.7554/eLife.03599.
Azoulay-Shemer, T., Palomares, A., Bagheri, A., Israelsson-Nordstrom, M., Engineer, C. B., Bargmann, B. O., Stephan, A. B., Schroeder, J. I. (2015) Guard cell photosynthesis is critical for stomatal turgor production, yet does not directly mediate CO2 - and ABA-induced stomatal closing. Plant J. 83(4), 567-81. doi: 10.1111/tpj.12916.
Keinath, N. F., Waadt, R., Brugman, R., Schroeder, J. I., Grossmann, G., Schumacher, K., Krebs, M. (2015) Live Cell Imaging with R-GECO1 Sheds Light on flg22- and Chitin-Induced Transient [Ca(2+)]cyt Patterns in Arabidopsis. Mol Plant. 8(8),1188-200. doi: 10.1016/j.molp.2015.05.006.
Engineer, C. B., Ghassemian, M., Anderson, J. C., Peck, S. C., Hu, H., Schroeder, J. I. (2014) Carbonic anhydrases, EPF2 and a novel protease mediate CO2 control of stomatal development. Nature. 513(7517), 246-50. doi: 10.1038/nature13452.
Mendoza-Cózatl, D.G., Xie, Q., Akmakjian, G. Z., Jobe, T. O., Patel, A., Stacey, M. G., Song, L., Demoin, D. W., Jurisson, S. S., Stacey, G., Schroeder, J. I. (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(9), 1455-69.
doi: 10.1093/mp/ssu067
Kunz, H. H., Gierth, M., Herdean, A., Satoh-Cruz, M., Kramer, D. M., Spetea, C., Schroeder, J. I. (2014) Plastidial transporters KEA1, -2, and -3 are essential for chloroplast osmoregulation, integrity, and pH regulation in Arabidopsis. Proc Natl Acad Sci USA. 111(20), 7480-5. doi: 10.1073/pnas.1323899111.
Deinlein, U., Stephan, A. B., Horie, T., Luo, W., Xu, G., Schroeder, J. I. (2014) Plant salt-tolerance mechanisms. Trends Plant Sci. 19(6), 371-379. doi: 10.1016/j.tplants.2014.02.001.
Song, W. Y., Mendoza-Cózatl, D. G., Lee, Y., Schroeder, J. I., Ahn, S. N., Lee, H. S., Wicker, T., Martinoia, E. (2014) Phytochelatin-metal(loid) transport into vacuoles shows different substrate preferences in barley and Arabidopsis. Plant Cell Environ. 37(5), 1192-201. doi: 10.1111/pce.12227.
Hauser, F., Chen, W., Deinlein, U., Chang, K., Ossowski, S., Fitz, J., Hannon, G. J., Schroeder, J. I. (2013) A genomic-scale artificial microRNA library as a tool to investigate the functionally redundant gene space in Arabidopsis. Plant Cell. 25(8), 2848-63. doi: 10.1105/tpc.113.112805.
McDowell, S. C., Akmakjian, G., Sladek, C., Mendoza-Cozatl, D., Morrissey, J. B., Saini, N., Mittler, R., Baxter, I., Salt, D. E., Ward, J. M., Schroeder, J. I., Guerinot, M. L., Harper, J. F. (2013) Elemental concentrations in the seed of mutants and natural variants of Arabidopsis thaliana grown under varying soil conditions. PLoS One. doi: 10.1371/journal.pone.0063014.
Schroeder, J. I., Delhaize, E., Frommer, W. B., Guerinot, M. L., Harrison, M. J., Herrera-Estrella, L., Horie, T., Kochian, L. V., Munns, R., Nishizawa, N. K., Tsay, Y. F., Sanders, D. (2013) Using membrane transporters to improve crops for sustainable food production. Nature. 497(7447), 60-6. doi: 10.1038/nature11909.
Jobe, T. O., Sung, D. Y., Akmakjian, G., Pham, A., Komives, E. A., Mendoza-Cózatl, D. G., Schroeder, J. I. (2012) Feedback inhibition by thiols outranks glutathione depletion: a luciferase-based screen reveals glutathione-deficient γ-ECS and glutathione synthetase mutants impaired in cadmium-induced sulfate assimilation. Plant J. 70(5), 783-95.
Xue, S., Yao, X., Luo, W., Jha, D., Tester, M., Horie, T., Schroeder, J. I. (2011) AtHKT1;1 mediates nernstian sodium channel transport properties in Arabidopsis root stelar cells. PLoS One. 6(9):e24725. doi: 10.1371/journal.pone.0024725.
Mendoza-Cózatl, D.G., Jobe, T. O., Hauser, F., Schroeder, J. I. (2011) Long-distance transport, vacuolar sequestration, tolerance, and transcriptional responses induced by cadmium and arsenic. Curr Opin Plant Biol. 14(5), 554-62. doi: 10.1016/j.pbi.2011.07.004.
Jannat, R., Uraji, M., Morofuji, M., Islam, M. M., Bloom, R. E., Nakamura, Y., McClung, C. R., Schroeder, J. I., Mori, I. C., Murata, Y. (2011) Roles of intracellular hydrogen peroxide accumulation in abscisic acid signaling in Arabidopsis guard cells. J Plant Physiol. 168(16),1919-26. doi: 10.1016/j.jplph.2011.05.006.
Horie, T., Brodsky, D. E., Costa, A., Kaneko, T., Lo Schiavo, F., Katsuhara, M., Schroeder, J. I. (2011) K+ transport by the OsHKT2;4 transporter from rice with atypical Na+ transport properties and competition in permeation of K+ over Mg2+ and Ca2+ ions. Plant Physiol. 156(3), 1493-507. doi: 10.1104/pp.110.168047.
Hauser, F. Waadt, R. & Schroeder, J. I. (2011) Evolution of abscisic acid synthesis and signaling mechanisms. Curr Biol. doi: 10.1016/j.cub.2011.03.015.
Böhmer, M. & Schroeder, J. I. (2011) Quantitative transcriptomic analysis of ABA-induced and ROSdependent expression changes and proteomic profiling in Arabidopsis suspension cells. Plant Journal. 67(1):105-18. doi: 10.1111/j.1365-313X.2011.04579.x.
Song, W. Y., Park, J., Mendoza-Cózatl, D.G., Suter-Grotemeyer, M., Shim, D., Hörtensteiner, S., Geisler, M., Weder, B., Rea, P. A., Rentsch, D., Schroeder, J. I., Lee, Y., Martinoia, E. (2010) Arsenic tolerance in Arabidopsis is mediated by two ABCC-type phytochelatin transporters. Proc Natl Acad Sci USA. 107, 21187-92. doi: 10.1073/pnas.1013964107.
Mendoza-Cózatl, D. G., Zhai, Z, Jobe, T. O., Akmakjian, G. Z., Song, W. Y., Limbo, O., Russell, M. R., Kozlovskyy, V. I., Martinoia, E., Vatamaniuk, O. K., Russell, P., Schroeder, J. I. (2010) Tonoplast-localized Abc2 transporter mediates phytochelatin accumulation in vacuoles and confers cadmium tolerance. J Biol Chem. 285(52), 40416-26. doi: 10.1074/jbc.M110.155408.
Costa, A., Drago, I., Behera, S., Zottini, M., Pizzo, P., Schroeder, J. I., Pozzan, T., Schiavao, F. L. (2010) H(2)O(2) in plant peroxisomes: an in vivo analysis uncovers a Ca(2+)-dependent scavenging system. Plant J. 62(5), 760-772. doi: 10.1111/j.1365-313X.2010.04190.x.
Kim, T. H., Bohmer, M., Hu, H., Nishimura, N., Schroeder, J. I. (2010) Guard cell signal transduction network: advances in understanding Abscisic acid, CO2, and Ca2+ signaling. Annual Review of Plant Biology. 61, 561-91. doi: 10.1146/annurev-arplant-042809-112226.
Yao, X., Horie, T., Xue, S., Leung, H. Y., Katsuhara, M., Brodsky, D. E., Wu, Y. & Schroeder, J. I. (2010) Differential sodium and potassium transport selectivities of the rice OsHKT2;1 and OsHKT2;2 transporters in plant cells. Plant Physiol. 152, 341-55. doi: 10.1104/pp.109.145722.
Nishimura, N., Sarkeshik, A., Nito, K., Park, S. Y., Wang, A., Carvalho, P. C., Lee, S., Caddell, D. F., Cutler, S. R., Chory, J., Yates, J. R., Schroeder, J. I. (2010) PYR/PYL/RCAR family members are major in-vivo ABI1 protein phosphatase 2C-interacting proteins in Arabidopsis. Plant J. 61, 290-299. doi: 10.1111/j.1365-313X.2009.04054.x.
Horie, T., Hauser, F., Schroeder, J. I. (2009) HKT transporter-mediated salinity resistance mechanisms in Arabidopsis and monocot crop plants. Trends Plant Sci. 14(12):660-8. doi: 10.1016/j.tplants.2009.08.009.
Sung, D. Y., Kim, T. H., Komives, E. A., Mendoza-Cózatl, D. G., Schroeder, J. I. (2009) ARS5 is a component of the 26S proteasome complex, and negatively regulates thiol biosynthesis and arsenic tolerance in Arabidopsis. Plant J. 59(5):802-13. doi: 10.1111/j.1365-313X.2009.03914.x.
Nishimura, N., Hitomi, K., Arvai, A. S., Rambo, R. P., Hitomi, C., Cutler, S. R., Schroeder, J. I., Getzoff, E. D. (2009) Structural mechanism of abscisic acid binding and signaling by dimeric PYR1. Science. 326(5958), 1373-9. doi: 10.1126/science.1181829.
Ward, J. M., Mäser, P., Schroeder, J. I. (2009) Plant ion channels: gene families, physiology, and functional genomics analyses. Annu Rev Physio. 71, 59-82. doi: 10.1146/annurev.physiol.010908.163204.
Kim, Y. Y., Kim, D. Y., Shim, D., Song, W. Y., Lee, J., Schroeder, J. I., Kim, S., Moran, N., Lee Y. (2008) Expression of the Novel Wheat Gene TM20 Confers Enhanced Cadmium Tolerance to Bakers Yeast. J Biol Chem. 283, 15893-15892. doi: 10.1074/jbc.M708947200.
Vahisalu, T., Kollist, H., Wang, Y. F., Nishimura, N., Chan, W. Y., Valerio, G., Lamminmaki, A., Brosche, M., Moldau, H., Desikan, R., Schroeder, J. I., Kangasjarvi, J. (2008) SLAC1 is required for plant guard cell S‐type anion channel function in stomatal signalling. Nature. 452, 487‐91. doi: 10.1038/nature06608.
Mendoza-Cozatl, D. G., Butko, E., Springer, F., Torpey, J. W., Komives, E. A., Kehr, J., Schroeder, J. I. (2008) Identification of high levels of phytochelatins, glutathione and cadmium in the phloem sap of Brassica napus. A role for thiol-peptides in the long-distance transport of cadmium and the effect of cadmium on iron translocation. Plant Journal. 54, 249-59. 54(2):249-59. doi: 10.1111/j.1365-313X.2008.03410.x.
Sadi, B. B., Vonderheide, A. P., Gong, J. M., Schroeder, J. I., Shann, J. R. & Caruso, J. A. (2008) An HPLC-ICP-MS technique for determination of cadmium-phytochelatins in genetically modified Arabidopsis thaliana. J Chromatogr B Analyt Technol Biomed Life Sci. 861,123-9. doi: 10.1016/j.jchromb.2007.11.004
Imaizumi, T., Kay, S. A., Schroeder, J. I. (2007) Circadian rhythms. Daily watch on metabolism. Science. 318, 730-1731. doi: 10.1126/science.1151360
Imaizumi, T., Schroeder, J. I., Kay, S. A. (2007) In SYNC: the ins and outs of circadian oscillations in calcium. Sci STKE. 390, pe32. doi: 10.1126/stke.3902007pe32.
Horie, T., Costa, A., Kim, T. H., Han, M. H., Horie, R., Leung, H. Y., Miyao, A., Hirochika, H., An, G. and Schroeder, J.I. (2007) Rice OsHKT2;1 transporter mediates large Na+ influx component into K+-starved roots for growth. EMBO J. 26, 3003-3014. doi: 10.1038/sj.emboj.7601732.
Sung, D. Y., Lee, D., Harris, H., Raab, A., Feldmann, J., Meharg, A., Kumabe, B., Komives, E. A., Schroeder, J. I. (2007) Identification of an arsenic tolerant double mutant with a thiol-mediated component and increased arsenic tolerance in phyA mutants. Plant J. 49, 1064-107. doi: 10.1111/j.1365-313X.2006.03018.x.
Schroeder, J. I., Nambara, E. (2006) A quick release mechanism for abscisic acid. Cell. 126, 1023-1025. doi: 10.1016/j.cell.2006.09.001.
Platten, J. D., Cotsaftis, O., Berthomieu, P., Bohnert, H., Davenport, R. J., Fairbairn, D. J., Horie, T., Leigh, R.A., Lin, H. X., Luan, S., Maser, P., Pantoja, O., Rodriguez-Navarro, A., Schachtman, D. P., Schroeder, J. I., Sentenac, H., Uozumi, N., Very AA, Zhu JK, Dennis ES, Tester M. (2006) Nomenclature for HKT transporters, key determinants of plant salinity tolerance. Trends Plant Sci. 11, 372-374. doi: 10.1016/j.tplants.2006.06.001.
Kwak, J. M., Nguyen, V., Schroeder, J. I. (2006) The role of reactive oxygen species in hormonal responses. Plant Physiology. 141, 323-329. doi: 10.1104/pp.106.079004
Chen, A., Komives, E. A., Schroeder, J. I. (2006) An improved grafting technique for mature Arabidopsis plants demonstrates long-distance shoot-to-root transport of phytochelatins in Arabidopsis. Plant Physiology. 141, 108-120. doi: 10.1104/pp.105.072637.
Schroeder, J. I., Kuhn, J. M. (2006) Plant biology abscisic acid in bloom. Nature. 439, 277-278. doi: 10.1038/439277a
Sunarpi, Horie, T., Motoda, J., Kubo, M., Yang, H., Yoda, K., Horie, R., Chan, W., Leung, H. Y., Hattori, K., Konomi, M., Osumi, M., Yamagami, M., *Schroeder, J. I., *Uozumi, N. (* corresponding authors) (2005) Enhanced salt tolerance mediated by AtHKT1 transporter-induced Na+ unloading from xylem parenchyma cells. Pl Journal. 44, 928-938. doi: 10.1111/j.1365-313X.2005.02595.x
Li, Y., Dhankher, O. P., Carreira, L., Lee, D., Chen, A., Schroeder, J. I., Balish, R. S., Meagher, R. B. (2004) Overexpression of phytochelatin synthase in Arabidopsis leads to enhanced arsenic tolerance and cadmium hypersensitivity. Plant Cell Physiol. 45, 1787-1797. doi: 10.1093/pcp/pch202.
Wycisk, K., Kim, E. J., Schroeder, J. I., Kramer, U. (2004) Enhancing the First Enzymatic Step in Histidine Biosynthesis Pathway Increases the Free Histidine Pool and Nickel Tolerance in Arabidosis Thaliana. FEBS Letters. 578, 128-134. doi: 10.1016/j.febslet.2004.10.086
Gong, J. M., Waner, D. A., Horie, T., Li, S. L., Horie, R., Abid, K. B., Schroeder, J. I. (2004) Microarray-based rapid cloning of an ion accumulation deletion mutant in Arabidopsis thaliana. Proc Natl Acad Sci USA. 101, 15404-15409. doi:10.1073/pnas.0404780101
Mori, I. and Schroeder, J. I. (2004) Reactive Oxygen Species Activation of Plant Ca2+ Channels: A Signaling Mechanism in Polar Growth, Hormone Transduction, Stress Signaling, and Hypothetically Mechano-transduction. Plant Physiology 135(2), 702-708. doi: 10.1104/pp.104.042069.
Lee, D. A., Chen, A., Schroeder, J. I. (2003) ars1, an Arabidopsis mutant exhibiting increased tolerance to arsenate and increased phosphate uptake. Plant J. 35(5), 637-46.
Gong, J. M., Lee, D. A., Schroeder, J. I. (2003) Long-distance root-to-shoot transport of phytochelatins and cadmium in Arabidopsis. Proc Natl Acad Sci USA. 100(17), 10118-23. doi: 10.1073/pnas.1734072100.
Mäser, P., Eckelman, B., Vaidyanathan, R., Horie, T., Fairbairn, D. J., Kubo, M., Yamagami, M., Yamaguchi, K., Nishimura, M., Uozumi, N., Robertson, W., Sussman, M. R., Schroeder, J. I. (2002) Altered shoot/root Na+ distribution and bifurcating salt sensitivity in Arabidopsis by genetic disruption of the Na+ transporter AtHKT1. FEBS Lett. 531(2), 157-61.
Allen, G. J., Murata, Y., Chu, S. P., Nafisi, M., Schroeder, J. I. (2002) Hypersensitivity of abscisic acid-induced cytosolic calcium increases in the Arabidopsis farnesyltransferase mutant era1-2. Plant Cell. 14(7), 1649-62. doi: 10.1105/tpc.010448.
Mäser, P., Hosoo, Y., Goshima, S., Horie, T., Eckelman, B., Yamada, K., Yoshida, K., Bakker, E. P., Shinmyo, A., Oiki, S., Schroeder, J. I., Uozumi, N. (2002) Glycine residues in potassium channel-like selectivity filters determine potassium selectivity in four-loop-per-subunit HKT transporters from plants. Proc Natl Acad Sci USA. 99(9), 6428-33. doi: 10.1073/pnas.082123799.
Ghassemian, M., Waner, D., Tchieu, J., Gribskov, M., Schroeder, J. I. (2001) An integrated Arabidopsis annotation database for Affymetrix Genechip data analysis, and tools for regulatory motif searches. Trends Plant Sci. 6(10), 448-9. doi: 10.1016/S1360-1385(01)02092-1.
Clemens, S., Schroeder, J. I., Degenkolb, T. (2001) Caenorhabditis elegans expresses a functional phytochelatin synthase. Eur J Biochem. 268(13), 3640-3. doi: 10.1046/j.1432-1327.2001.02293.x.
Main Contact Information
Project Leader
- Dr. Julian I. Schroeder
Superfund Related Project Members
- Aaron Stephan, Post-Doctoral Scholar
- Andrew Cooper, Graduate Student
- Andrew Kai, Masters Student
- Cawas Engineer, Project Scientist
Resources
UCSD Division of Biological Sciences
Contact
UCSD Superfund Research Center
University of California, San Diego
Pharmacology Department
9500 Gilman Drive, Mail Code 0722
La Jolla, CA 92093-0722
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