Molecular Mechanisms of Heavy Metal Detoxification and Engineering Accumulation in Plants

Research Project 6

Project Narative

Soils and waters with high levels of toxic heavy metal(loid)s such as arsenic, cadmium, lead and mercury are detrimental to human health and have been associated with liver disease. These heavy metal(loid)s are among the top 7 priority hazardous substances at US Superfund sites and uptake of toxic heavy metal(loid)s into plants can provide a cost-effective approach for toxic metal removal and bioremediation of heavy metal-laden soils and waters. Important genes and pathways that function in heavy metal bioremediation and rapid toxic metal(loid)-induced gene expression will be characterized and identified and their bioremediation potential investigated, contributing to cost effective future bioremediation technologies.

Summary of Project

Soils and waters with high levels of toxic metal(loid)s such as cadmium, lead, arsenic and mercury are detrimental to human and environmental health. These 4 heavy metal(loid)s are among the Superfund's top 7 priority hazardous substances. Many human diseases have been attributed to environmental contamination by heavy metals, including cancers and neurological disorders. Research and applications indicate that uptake of heavy metals into plant roots and accumulation of heavy metals could provide a cost effective approach for toxic metal removal and bioremediation of heavy metal-laden soils and waters. In recent research we have made major advances at understanding key mechanisms that function in heavy metal detoxification, transport and accumulation in plants. However important genes and pathways that function in heavy metal over-accumulation in plants remain to be identified. We will combine powerful genomic, genetic, biochemical and engineering approaches to test new central hypotheses by pursuing the following Specific Aims:


Aim I.  The regulatory mechanisms, transcription factors (TFs), and transcriptional network that mediate rapid heavy metal(loid)-induced transcriptional responses in plants remain largely unknown. Using a luciferase-based cadmium- and arsenic-induced reporter mutant screening approach we have isolated mutants in rapid Cd- and As-induced gene expression. New mutants in major Cd-/As-dependent repression and induction loci will be characterized and the underlying genes isolated and their functions determined. Collaborative research with Geoffrey Chang (Project 5) will pursue development of cost-effective innovative heavy metal toxicant nano-reporters in plants.

Aim II.  The many genetic redundancies in plant genomes cause major limitations in heavy metal response gene discovery. To address redundant gene function on a systems biology scale we have designed a genomic scale artificial microRNA (amiRNA) library for genome-wide knockdown of homologous gene family members which is leading to discovery of new genes and will be used to characterize key plant genes and network mechanisms that function in heavy metal accumulation, resistance and remediation.

Aim III: Using genes identified in Specific Aims I and II and previous research, gene-stacking will be used to generate plants and investigate their enhanced heavy metal accumulation and root sequestration (phytostabilization) potential. Furthermore, by genomic investigation of plants that are being used for phytostabilization at semi-arid Superfund sites, the above advances will be used in collaboration with the University of Arizona Superfund Research Center to uncover mechanisms that render plants suitable for phytostabilization of toxic metal(loid)s. The proposed research will be leveraged to develop technologies for avoiding the growing problem of accumulation of heavy metals and arsenic in edible plant tissues.


PubMed Central ID: 

Zhang L, Takahashi Y, Schroeder JI. Protein kinase sensors: an overview of new designs for visualizing kinase dynamics in single plant cells. Plant Physiol. 2021 Oct 5;187(2):527-536. doi: 10.1093/plphys/kiab277.

PubMedID: 35142856
PubMed Central ID: 

Jalakas P, Takahashi Y, Waadt R, Schroeder JI, Merilo E. Molecular mechanisms of stomatal closure in response to rising vapour pressure deficit. New Phytol. 2021 Oct;232(2):468-475. doi: 10.1111/nph.17592. Epub 2021 Jul 29.

PubMedID: 34197630
PubMed Central ID: 
Jobe, T. O., Yu, Q., Hauser, F., Xie, Q., Meng, Y., Maassen, T., Kopriva, S., & Schroeder, J. I. (2021). The SLIM1 transcription factor is required for arsenic resistance in Arabidopsis thaliana. FEBS letters, 595(12), 1696–1707.
PubMedID: 33960401
PubMed Central ID: 
Xie, Q., Yu, Q., Jobe, T. O., Pham, A., Ge, C., Guo, Q., Liu, J., Liu, H., Zhang, H., Zhao, Y., Xue, S., Hauser, F., & Schroeder, J. I. (2021). An amiRNA screen uncovers redundant CBF and ERF34/35 transcription factors that differentially regulate arsenite and cadmium responses. Plant, cell & environment, 44(5), 1692–1706.
PubMedID: 33554343
PubMed Central ID: 
Yu, Q., Zhang, Z. C., Wang, M. Y., Scavo, A., Schroeder, J. I., & Qiu, B. S. (2021). Identification and characterization of SaeIF1 from the eukaryotic translation factor SUI1 family in cadmium hyperaccumulator Sedum alfredii. Planta, 253(1), 12.
PubMedID: 33389204
PubMed Central ID: 
Schulze, S., Dubeaux, G., Ceciliato, P., Munemasa, S., Nuhkat, M., Yarmolinsky, D., Aguilar, J., Diaz, R., Azoulay-Shemer, T., Steinhorst, L., Offenborn, J. N., Kudla, J., Kollist, H., & Schroeder, J. I. (2021). A role for calcium-dependent protein kinases in differential CO2 - and ABA-controlled stomatal closing and low CO2 -induced stomatal opening in Arabidopsis. The New phytologist, 229(5), 2765–2779.
PubMedID: 33187027
PubMed Central ID: 
Hsu, P. K., Dubeaux, G., Takahashi, Y., & Schroeder, J. I. (2021). Signaling mechanisms in abscisic acid-mediated stomatal closure. The Plant journal : for cell and molecular biology, 105(2), 307–321.
PubMedID: 33145840
PubMed Central ID: 
Cooper, A. M., Felix, D., Alcantara, F., Zaslavsky, I., Work, A., Watson, P. L., Pezzoli, K., Yu, Q., Zhu, D., Scavo, A. J., Zarabi, Y., & Schroeder, J. I. (2020). Monitoring and mitigation of toxic heavy metals and arsenic accumulation in food crops: A case study of an urban community garden. Plant direct, 4(1), e00198.
PubMedID: 31956855
PubMed Central ID: 

Takahashi, Y., Zhang, J., Hsu, P.K., Ceciliato, P.H.O., Zhang, L., Dubeaux, G., Munemasa, S., Ge, C., Zhao, Y., Hauser, F., Schroeder, J.I. (2020) MAP3Kinase-Dependent SnRK2-kinase activation is required for abscisic acid signal transduction and rapid osmotic stress response. Nat Commun. 2020 Jan 2;11(1):12. doi: 10.1038/s41467-019-13875-y

PubMedID: 31896774
PubMed Central ID: 

Bailey-Serres J, Parker JE, Ainsworth EA, Oldroyd GED, Schroeder JI. (2019) Genetic strategies for improving crop yields. Nature. Nov;575(7781):109-118. doi: 10.1038/s41586-019-1679-0

PubMedID: 31695205
PubMed Central ID: 

Ceciliato, P. H. O., Zhang, J., Liu, Q., Shen, X., Hu, H., Liu, C., Schaffner, A. R., Schroeder, J. I. (2019) Intact leaf gas exchange provides a robust method for measuring the kinetics of stomatal conductance responses to abscisic acid and other small molecules in Arabidopsis and grasses. Plant Methods. Apr 17;15:38. doi: 10.1186/s13007-019-0423-y

PubMedID: 31019545
PubMed Central ID: 

Park, J., Kim, T.H., Takahashi, Y., Schwab, R., Dressano, K., Stephan, A.B., Ceciliato, P.H.O., Ramirez, E., Garin, V., Huffaker, A., Schroeder, J.I. (2019) Chemical genetic identification of a lectin receptor kinase that transduces immune responses and interferes with abscisic acid signaling. Plant J. 98(3):492-510. Epub 2019 Mar 7. doi:10.1111/tpj.14232

PubMedID: 30659683
PubMed Central ID: 

Hauser, F., Ceciliato, P.H.O., Lin, Y.C., Guo, D., Gregerson, J.D., Abbasi, N., Youhanna, D., Park, J., Dubeaux, G., Shani, E., Poomchongkho, N., Schroeder, J.I. (2019) A seed resource for screening functionally redundant genes and isolation of new mutants impaired in CO2 and ABA responses. J Exp Bot. 70(2):641-651. doi: 10.1093/jxb/ery363

PubMedID: 30346611
PubMed Central ID: 

Zhang, Y., Nasser, V., Pisanty, O., Omary, M., Wulff, N., Di, Donato, M., Tal, I., Hauser, F., Hao, P., Roth, O., Fromm, H., Schroeder, J.I., Geisler, M., Nour-Eldin, H.H., Shani, E. (2018) A transportome-scale amiRNA-based screen identifies redundant roles of Arabidopsis ABCB6 and ABCB20 in auxin transport. Nat Commun. 9(1):4204.
doi: 10.1038/s41467-018-06410-y

PubMedID: 30310073
PubMed Central ID: 

Hsu, P.K., Takahashi, Y., Munemasa, S., Merilo, E., Laanemets, K., Waadt, R., Pater, D., Kollist, H., Schroeder, J.I. (2018) Abscisic acid-independent stomatal CO2 signal transduction pathway and convergence of CO2 and ABA signaling downstream of OST1 kinase. Proc Natl Acad Sci U S A. 115(42):E9971-E9980. Epub 2018 Oct 3.
doi: 10.1073/pnas.1809204115

PubMedID: 30282744
PubMed Central ID: 

Tõldsepp, K., Zhang, J., Takahashi, Y., Sindarovska, Y., Hõrak, H., Ceciliato, P.H.O., Koolmeister, K., Wang, Y.S., Vaahtera, L., Jakobson, L., Yeh, C.Y., Park, J., Brosche, M., Kollist, H., Schroeder, J.I. (2018) Mitogen-activated protein kinases MPK4 and MPK12 are key components mediating CO2 -induced stomatal movements. Plant J. 96(5):1018-1035. Epub 2018 Oct 23. doi: 10.1111/tpj.14087

PubMedID: 30203878
PubMed Central ID: 

Li, Z., Takahashi, Y., Scavo, A., Brandt, B., Nguyen, D., Rieu, P., Schroeder, J.I. (2018) Abscisic acid-induced degradation of Arabidopsis guanine nucleotide exchange factor requires calcium-dependent protein kinases. Proc Natl Acad Sci U S A. 115(19):E4522-E4531. Epub 2018 Apr 23. doi: 10.1073/pnas.1719659115

PubMedID: 29686103
PubMed Central ID: 

Azoulay-Shemer T, Hsu PK, Schroeder JI. (2017) Seeing is believing. Nat Plants. 3(10):765-766. doi: 10.1038/s41477-017-0025-5.

PubMedID: 28970562
PubMed Central ID: 

Stephan A.B., Kunz H.H., Yang E., Schroeder J.I. (2016) Rapid hyperosmotic-induced Ca2+ responses in Arabidopsis thaliana exhibit sensory potentiation and involvement of plastidial KEA transporters. Proc Natl Acad Sci U S A. 113(35):E5242-9. doi: 10.1073/pnas.1519555113. Epub 2016 Aug 15.

PubMedID: 27528686
PubMed Central ID: 

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.

PubMedID: 27357749
PubMed Central ID: 

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.

PubMedID: 27357687
PubMed Central ID: 

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.

PubMedID: 26786707
PubMed Central ID: 

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.

PubMedID: 26764376
PubMed Central ID: 

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.

PubMedID: 26764375
PubMed Central ID: 

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. 154-162. doi: 10.1016/j.pbi.2015.10.010.

PubMedID: 26599955
PubMed Central ID: 
Waadt, R., Hsu, P. K., Schroeder, J. I. (2015) Abscisic acid and other plant hormones: Methods to visualize distribution and signaling. Bioessays. 37(12),1338-49. doi: 10.1002/bies.201500115.
PubMedID: 26577078
PubMed Central ID: 

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.

PubMedID: 26482956
PubMed Central ID: 

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. (2015) Identification of AtOPT4 as a Plant Glutathione Transporter. Mol Plant. 9(3):481-484. doi: 10.1016/j.molp.2015.07.013.

PubMedID: 26283048
PubMed Central ID: 

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.

PubMedID: 26192964
PubMed Central ID: 

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.

PubMedID: 26096271
PubMed Central ID: 

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.

PubMedID: 26002145
PubMed Central ID: 

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.

PubMedID: 25043023
PubMed Central ID: 

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

PubMedID: 24880337
PubMed Central ID: 

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.

PubMedID: 24794527
PubMed Central ID: 
Stephan, A. B., Schroeder, J. I. (2014) Plant salt stress status is transmitted systemically via propagating calcium waves.
Proc Natl Acad Sci U S A. 111(17), 6126-7. doi: 10.1073/pnas.1404895111.
PubMedID: 24737890
PubMed Central ID: 
Waadt, R., Hitomi, K., Nishimura, N., Hitomi, C., Adams, S. R., Getzoff, E. D., Schroeder, J. I. (2014) FRET-based reporters for the direct visualization of abscisic acid concentration changes and distribution in Arabidopsis.
Elife. 3, e01739. doi: 10.7554/eLife.01739.
PubMedID: 24737861
PubMed Central ID: 

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.

PubMedID: 24630845
PubMed Central ID: 

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.

PubMedID: 24313707
PubMed Central ID: 

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.

PubMedID: 23956262
PubMed Central ID: 

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.

PubMedID: 23671651
PubMed Central ID: 

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.

PubMedID: 23636397
PubMed Central ID: 

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. doi: 10.1111/j.1365-313X.2012.04924.x.

PubMedID: 22283708
PubMed Central ID: 

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.

PubMedID: 21931830
PubMed Central ID: 

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.

PubMedID: 21820943
PubMed Central ID: 

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.

PubMedID: 21665322
PubMed Central ID: 

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.

PubMedID: 21610181
PubMed Central ID: 

​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.

PubMedID: 21549957
PubMed Central ID: 

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. 

PubMedID: 21426425
PubMed Central ID: 

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.

PubMedID: 21078981
PubMed Central ID: 

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.

PubMedID: 20937798
PubMed Central ID: 

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.

PubMedID: 20230493
PubMed Central ID: 

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.

PubMedID: 20192751
PubMed Central ID: 

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.

PubMedID: 19889878
PubMed Central ID: 

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.

PubMedID: 19874541
PubMed Central ID: 

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.

PubMedID: 19783197
PubMed Central ID: 

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.

PubMedID: 19453443
PubMed Central ID: 

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.

PubMedID: 19933100
PubMed Central ID: 

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.

PubMedID: 18842100
PubMed Central ID: 

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.

PubMedID: 18411273
PubMed Central ID: 

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.

PubMedID: 18305484
PubMed Central ID: 

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.

PubMedID: 18208526
PubMed Central ID: 

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

PubMedID: 18065298
PubMed Central ID: 

Imaizumi, T., Kay, S. A., Schroeder, J. I. (2007) Circadian rhythms. Daily watch on metabolism. Science. 318, 730-1731. doi: 10.1126/science.1151360

PubMedID: 18006706
PubMed Central ID: 

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.

PubMedID: 17565121
PubMed Central ID: 

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.

PubMedID: 17541409

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 J49, 1064-107. doi: 10.1111/j.1365-313X.2006.03018.x.

PubMedID: 17335514

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.

PubMedID: 16990126

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.

PubMedID: 16809061
PubMed Central ID: 

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

PubMedID: 16760482
PubMed Central ID: 

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.

PubMedID: 16531489

Schroeder, J. I., Kuhn, J. M. (2006) Plant biology abscisic acid in bloom. Nature. 439, 277-278. doi: 10.1038/439277a

PubMedID: 16421556

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

PubMedID: 16359386

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.

PubMedID: 15653797

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

PubMedID: 15581629
PubMed Central ID: 

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

PubMedID: 15486089
PubMed Central ID: 

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.

PubMedID: 15208417

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.

PubMedID: 12940956
PubMed Central ID: 

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.

PubMedID: 12909714

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.

PubMedID: 12417304
PubMed Central ID: 

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.

PubMedID: 12119381
PubMed Central ID: 

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.

PubMedID: 11959905

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.

PubMedID: 11590042

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.

PubMedID: 11432729

Main Contact Information

Project Leader
  • Dr. Julian I. Schroeder
    Professor, Torrey Mesa Research Institute Chair in Plant Science, Department of Biology and Bioengineering, UCSD

Superfund Project Members

  • Felix Hauser, Assistant Project Scientist
  • Po-Kai Hsu, Post-Doctoral Scholar
  • Guillaume Dubeaux, Post-Doctoral Scholar
  • Andrew Cooper, Graduate Student


UCSD Superfund Research Center
University of California, San Diego
Pharmacology Department
9500 Gilman Drive, Mail Code 0722
La Jolla, CA 92093-0722