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Project Publications: University of California-San Diego: Molecular Mechanisms of Heavy Metal Detoxification and Accumulation in Plants

Superfund Research Program

Molecular Mechanisms of Heavy Metal Detoxification and Accumulation in Plants

Project Leader: Julian I. Schroeder
Grant Number: P42ES010337
Funding Period: 2000-2017
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  • Jalakas P, Takahashi Y, Waadt R, Schroeder JI, Merilo E. 2021. Molecular mechanisms of stomatal closure in response to rising vapour pressure deficit. New Phytol 232(2):doi:10.1111/nph.17592 PMID:34197630 (ahead of print)
  • Jobe TO, Yu Q, Hauser F, Xie Q, Meng Y, Maassen T, Kopriva S, Schroeder JI. 2021. The SLIM1 transcription factor is required for arsenic resistance in Arabidopsis thaliana. FEBS Lett 595(12):1696-1707. doi:10.1002/1873-3468.14096 PMID:33960401 PMCID:PMC8238853
  • Xie Q, Yu Q, Jobe TO, Pham A, Ge C, Guo Q, Liu J, Liu H, Zhang H, Zhao Y, Xue S, Hauser F, Schroeder JI. 2021. An amiRNA screen uncovers redundant CBF and ERF34/35 transcription factors that differentially regulate arsenite and cadmium responses. Plant Cell Environ 44(5):1692-1706. doi:10.1111/pce.14023 PMID:33554343 PMCID:PMC8068611
  • Yu Q, Zhang Z, Wang M, Scavo A, Schroeder JI, Qiu B. 2021. Identification and characterization of SaeIF1 from the eukaryotic translation factor SUI1 family in cadmium hyperaccumulator Sedum alfredii. Planta 253:12. doi:10.1007/s00425-020-03539-3 PMID:33389204 PMCID:PMC7847809


  • Hsu P, Dubeaux G, Takahashi Y, Schroeder JI. 2020. Signaling mechanisms in abscisic acid-mediated stomatal closure. The Plant Journal 15:doi:10.1111/tpj.15067 PMID:33145840


  • Azoulay-Shemer T, Hsu P, Schroeder JI. 2017. Seeing is believing. Nat Plants 3(10):765-766. doi:10.1038/s41477-017-0025-5 PMID:28970562 PMCID:28970562
  • Kobayashi NI, Yamaji N, Yamamoto H, Okubo K, Ueno H, Costa A, Tanoi K, Matsumura H, Fujii-Kashino M, Horiuchi T, Al Nayef M, Shabala S, An G, Ma JF, Horie T. 2017. OsHKT1;5 mediates Na+ exclusion in the vasculature to protect leaf blades and reproductive tissues from salt toxicity in rice. Plant J 91:657-670. doi:10.1111/tpj.13595 PMID:28488420


  • Aleman F, Yazaki J, Lee M, Takahashi Y, Kim AY, Li Z, Kinoshita T, Ecker JR, Schroeder JI. 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 PMID:27357749 PMCID:PMC4928087
  • Engineer C, Hashimoto-Sugimoto M, Negi J, Israelsson-Nordstrom M, Azoulay-Shemer T, Rappel WJ, Iba K, Schroeder JI. 2016. 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 PMID:26482956 PMCID:PMC4707055
  • Patterson K, Walters LA, Olvera JG, Rosas MA, Rasmusson AG, Escobar MA. 2016. Nitrate-regulated glutaredoxins control Arabidopsis primary root growth. Plant Physiol 170(2):989-999. doi:10.1104/pp.15.01776 PMID:26662603 PMCID:PMC4734588
  • Stephan AB, Kunz H, Yang E, Schroeder JI. 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-E5249. doi:10.1073/pnas.1519555113 PMID:27528686 PMCID:PMC5024618
  • Suzuki K, Yamaji N, Costa A, Okuma E, Kobayashi NI, Kashiwagi T, Katsuhara M, Wang C, Tanoi K, Murata Y, Schroeder JI, Ma JF, 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 16:22. doi:10.1186/s12870-016-0709-4 PMID:26786707 PMCID:PMC4719677
  • Wang C, Hu H, Qin X, Zeise B, Xu D, Rappel WJ, Boron W, Schroeder JI. 2016. Reconstitution of CO2 regulation of SLAC1 anion channel and function of CO2-permeable PIP2;1 aquaporin as carbonic anhydrase 4 interactor. Plant Cell 28(2):568-582. doi:10.1105/tpc.15.00637 PMID:26764375 PMCID:PMC4790870
  • Yamamoto Y, Negi J, Wang C, Isogai Y, Schroeder JI, Iba K. 2016. The transmembrane region of guard cell SLAC1 channels perceives CO2 signals via an ABA-independent pathway in Arabidopsis. Plant Cell 28(2):557-567. doi:10.1105/tpc.15.00583 PMID:26764376 PMCID:PMC4790869
  • Yazaki J, Galli M, Kim AY, Nito K, Aleman F, Chang KN, Carvunis A, Quan R, Nguyen H, Song L, Alvarez J, Huang SC, Chen H, Ramachandran N, Altmann S, Gutierrez RA, Hill DE, Schroeder JI, Chory J, LaBaer J, Vidal M, Braun P, Ecker JR. 2016. Mapping transcription factor interactome networks using HaloTag protein arrays. Proc Natl Acad Sci U S A 113(29):E4238-E4247. doi:10.1073/pnas.1603229113 PMID:27357687 PMCID:PMC4961138
  • Zhang Z, Xie Q, Jobe TO, Kau AR, Wang C, Li Y, Qiu B, Wang Q, Mendoza-Cozatl DG, Schroeder JI. 2016. Identification of AtOPT4 as a plant glutathione transporter. Mol Plant 9(3):481-484. doi:10.1016/j.molp.2015.07.013 PMID:26283048 PMCID:PMC5139274



  • Deinlein U, Stephan AB, Horie T, Luo W, Xu G, Schroeder JI. 2014. Plant salt-tolerance mechanisms. Trends Plant Sci 19(6):371-379. doi:10.1016/j.tplants.2014.02.001 PMID:24630845 PMCID:PMC4041829
  • Engineer C, Ghassemian M, Anderson JC, Peck SC, Hu H, Schroeder JI. 2014. Carbonic anhydrases, EPF2 and a novel protease mediate CO2 control of stomatal development. Nature 513(7517):246-250. doi:10.1038/nature13452 PMID:25043023 PMCID:PMC4274335
  • Kunz H, Gierth M, Herdean A, Satoh-Cruz M, Kramer DM, Spetea C, Schroeder JI. 2014. Plastidial transporters KEA1, -2, and -3 are essential for chloroplast osmoregulation, integrity, and pH regulation in Arabidopsis. Proc Natl Acad Sci U S A 111(20):7480-7485. doi:10.1073/pnas.1323899111 PMID:24794527 PMCID:PMC4034250
  • Mendoza-Cozatl DG, Xie Q, Akmakjian GZ, Jobe TO, Patel AU, Stacey MG, Song L, Demoin DW, Jurisson SS, Stacey G, Schroeder JI. 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):1455-1469. doi:10.1093/mp/ssu067 PMID:24880337 PMCID:PMC4153440
  • Song W, Mendoza-Cozatl DG, Lee Y, Schroeder JI, Ahn S, Lee H, Wicker T, Martinoia E. 2014. Phytochelatin-metal(loid) transport into vacuoles shows different substrate preferences in barley and Arabidopsis. Plant Cell Environ 37(5):1192-1201. doi:10.1111/pce.12227 PMID:24313707 PMCID:PMC4123957
  • Stephan AB, Schroeder JI. 2014. Plant salt stress status is transmitted systemically via propagating calcium waves. Proc Natl Acad Sci U S A 111(17):6126-6127. doi:10.1073/pnas.1404895111 PMID:24737890 PMCID:PMC4036006
  • Waadt R, Hitomi K, Nishimura N, Hitomi C, Adams SR, Getzoff ED, Schroeder JI. 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 PMID:24737861 PMCID:PMC3985518


  • Hauser F, Chen W, Deinlein U, Chang K, Ossowski S, Fitz J, Hannon GJ, Schroeder JI. 2013. A genomic-scale artificial microRNA library as a tool to investigate the functionally redundant gene space in Arabidopsis. Plant Cell 25(8):2848-2863. doi:10.1105/tpc.113.112805 PMID:23956262 PMCID:PMC3784584
  • McDowell SC, Akmakjian GZ, Sladek C, Mendoza-Cozatl DG, Morrissey JB, Saini N, Mittler R, Baxter I, Salt DE, Ward JM, Schroeder JI, Guerinot ML, Harper JF. 2013. Elemental concentrations in the seed of mutants and natural variants of Arabidopsis thaliana grown under varying soil conditions. PLoS One 8(5):e63014. doi:10.1371/journal.pone.0063014 PMID:23671651 PMCID:PMC3646034
  • Schroeder JI, Delhaize E, Frommer WB, Guerinot ML, Harrison MJ, Herrera-Estrella L, Horie T, Kochian LV, Munns R, Nishizawa NK, Tsay Y, Sanders D. 2013. Using membrane transporters to improve crops for sustainable food production. Nature 497:60-66. doi:10.1038/nature11909 PMID:23636397 PMCID:PMC3954111


  • Jobe TO, Sung D, Akmakjian GZ, Pham AL, Komives EA, Mendoza-Cozatl DG, Schroeder JI. 2012. Feedback inhibition by thiols outranks glutathione depletion: a luciferase-based screen reveals glutathione-deficient y-ECS and glutathione synthetase mutants impaired in cadmium-induced sulfate assimilation. Plant J 70:783-795. doi:10.1111/j.1365-313X.2012.04924.x PMID:22283708 PMCID:PMC4688143



  • Costa A, Drago I, Behera S, Zottini M, Pizzo P, Schroeder JI, Pozzan T, Schiavo F. 2010. H2O2 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 PMID:20230493 PMCID:PMC2884081
  • Mendoza-Cozatl DG, Zhai Z, Jobe TO, Akmakjian GZ, Song W, Limbo O, Russell MR, Kozlovskyy VI, Martinoia E, Vatamaniuk OK, Russell P, Schroeder JI. 2010. Tonoplast-localized Abc2 transporter mediates phytochelatin accumulation in vacuoles and confers cadmium tolerance. J Biol Chem 285(52):40416-40426. doi:10.1074/jbc.M110.155408 PMID:20937798 PMCID:PMC3003340
  • Nishimura N, Sarkeshik A, Park S, Wang A, Carvalho PC, Lee S, Caddell DF, Cutler SR, Chory J, Yates JR, Schroeder JI, Nito K. 2010. PYR/PYL/RCAR family members are major in-vivo ABI1 protein phosphatase 2C-interacting proteins in Arabidopsis. Plant J 61(2):290-299. doi:10.1111/j.1365-313X.2009.04054.x PMID:19874541 PMCID:PMC2807913
  • Pyo Y, Gierth M, Schroeder JI, Cho M. 2010. High-affinity K(+) transport in Arabidopsis: AtHAK5 and AKT1 are vital for seedling establishment and postgermination growth under low-potassium conditions. Plant Physiol 153(2):863-875. doi:10.1104/pp.110.154369 PMID:20413648 PMCID:PMC2879780
  • Song W, Park J, Mendoza-Cózatl D, Suter-Grotemeyer M, Shim D, Hortensteiner S, Geisler M, Weder B, Rea PA, Rentsch D, Schroeder JI. 2010. Arsenic tolerance in Arabidopsis is mediated by two ABCC-type phytochelatin transporters. Proc Natl Acad Sci U S A 107(49):21187-21192. doi:10.1073/pnas.1013964107 PMID:21078981 PMCID:PMC3000282
  • Yao X, Horie T, Xue S, Leung H, Katsuhara M, Brodsky DE, Wu Y, Schroeder JI. 2010. Differential sodium and potassium transport selectivities of the rice OsHKT2;1 and OsHKT2;2 transporters in plant cells. Plant Physiol 152(1):341-355. doi:10.1104/pp.109.145722 PMID:19889878 PMCID:PMC2799368



  • Horie T, Sugawara M, OKUNOU K, NAKAYAMA H, Schroeder JI, Shinmyo A, Yoshida K. 2008. Functions of HKT transporters in sodium transport in roots and in protecting leaves from salinity stress. Plant Biotechnology 25:233-239.
  • Kim Y, Kim D, Shim D, Song W, Lee J, Schroeder JI, Kim S, Moran| N, Lee Y. 2008. Expression of the novel wheat gene TM20 confers enhanced cadmium tolerance to bakers' yeast. J Biol Chem 283:15893-15902. doi:10.1074/jbc.M708947200 PMID:18411273 PMCID:PMC2414300
  • Mendoza-Cózatl D, Butko E, Springer F, Torpey JW, Komives EA, Kehr J, Schroeder JI. 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 J 54(2):249-259. doi:10.1111/j.1365-313X.2008.03410.x PMID:18208526 PMCID:PMC2839885
  • VAHISALU T, KOLLIST H, Wang Y, Nishimura N, Chan W, Valerio G, LAMMINMÄKI A, BROSCHE M, DESIKAN R, Schroeder JI, KANGASJÄRVI J, MOLDAU H. 2008. SLAC1 is required for plant guard cell S-type anion channel function in stomatal signalling. Nature 452:487-491. PMID:18305484


  • Horie T, Costa A, Kim T, Han M, Horie R, Leung H, Miyao A, Hirochika H, An G, Schroeder JI. 2007. Rice OsHKT2;1 transporter mediates large Na+ influx component into K+-starved roots for growth. EMBO J 26(12):3003-14. PMID:17541409


  • Chen A, Komives EA, Schroeder JI. 2006. An improved grafting technique for mature Arabidopsis plants demonstrates long-distance shoot-to-root transport of phytochelatins in Arabidopsis. Plant Physiol 141(1):108-120. doi:10.1104/pp.105.072637 PMID:16531489 PMCID:PMC1459314
  • Platten JD, Cotsaftis O, Berthomieu P, Bohnert H, Davenport RJ, Fairbairn DJ, Horie T, Leigh RA, Lin H, Luan S, Maser P, Pantoja O, Rodriguez-Navarro A, Schachtman DP, Schroeder JI, Sentenac H, Uozumi N, Very A, Zhu J, Dennis ES, Tester M. 2006. Nomenclature for HKT transporters, key determinants of plant salinity tolerance. Trends Plant Sci 11(8):372-374. PMID:16809061


  • Sunarpi, Horie T, Motoda J, Kubo M, Yang H, Yoda K, Horie R, Chan W, Leung H, Hattori K, Konomi M, Osumi M, Yamagami M, Schroeder JI, Uozumi N. 2005. Enhanced salt tolerance mediated by AtHKT1 transporter-induced Na+ unloading from xylem vessels to xylem parenchyma cells. Plant J 44(6):928-938. PMID:16359386


  • Gong J, Waner DA, Horie T, Li S, Horie R, Abid KB, Schroeder JI. 2004. Microarray-based rapid cloning of an ion accumulation deletion mutant in Arabidopsis thaliana. Proc Natl Acad Sci U S A 101(43):15404-15409. PMID:15486089
  • Li Y, Dhankher OP, Carreira L, Lee DA, Chen A, Schroeder JI, Balish RS, Meagher RB. 2004. Overexpression of phytochelatin synthase in Arabidopsis leads to enhanced arsenic tolerance and cadmium hypersensitivity. Plant and Cell Physiology 45(12):1787-1797. PMID:15653797
  • Schroeder JI, Mori IC. 2004. Reactive oxygen species activation of plant Ca2+ channels. A signaling mechanism in polar growth, hormone transduction, stress signaling, and hypothetically mechanotransduction. Plant Physiol 135(2):702-708. PMID:15208417
  • Wycisk K, Kim EJ, Schroeder JI, Kramer U. 2004. Enhancing the first enzymatic step in the histidine biosynthesis pathway increases the free histidine pool and nickel tolerance in Arabidopsis thaliana. FEBS Lett 578(1-2):128-134. PMID:15581629


  • Lee DA, Chen A, Schroeder JI. 2003. Ars1, an Arabidopsis mutant exhibiting increased tolerance to arsenate and increased phosphate uptake. Plant J 35(5):637-646. PMID:12940956
  • Maier T, Yu C, Kullertz G, Clemens S. 2003. Localization and functional characterization of metal-binding sites in phytochelatin synthases. Planta 218(2):300-308. PMID:12905027
  • Schroeder JI. 2003. Knockout of the guard cell K+ out channel and stomatal movements. Proc Natl Acad Sci U S A 100(9):4976-4977. PMID:12704226
  • Thomine S, Lelievre F, Debarbieux E, Schroeder JI, Barbier-Brygoo H. 2003. AtNRAMP3, a multispecific vacuolar metal transporter involved in plant responses to iron deficiency. Plant J 34(5):685-695. PMID:12787249


  • Allen GJ, Murata Y, Chu SP, Nafisi M, Schroeder JI. 2002. Hypersensitivity of abscisic acid-induced cytosolic calcium increases in the Arabidopsis farnesyltransferase mutant era1-2. Plant Cell 14(7):1649-1662. PMID:12119381 PMCID:PMC150713
  • Beachy R, Bennetzen JL, Chassy BM, Chrispeels M, Chory J, Ecker JR, Noel JP, Kay SA, Dean C, Lamb C, Jones J, Santerre CR, Schroeder JI, Umen J, Yanofsky M, Wessler S, Zhao Y, Parrott W. 2002. Divergent perspectives on GM food. Nat Biotechnol 20(12):1195-1196. PMID:12454665
  • Kuchitsu K, Ward JM, Allen GJ, Schelle I, Schroeder JI. 2002. Loading acetoxymethyl ester fluorescent dyes into the cytoplasam of Arabidopsis and Commelina guard cells. New Phytologist 153:527-533.
  • Lee DA, Schroeder JI. 2002. Heavy metal stress. In: Arabidopsis - A Laboratory Manual. Cold Spring Harbor Laboratory Press, pp.75-77.
  • Maser P, Eckelman B, Vaidyanathan R, Horie T, Fairbairn DJ, Kubo M, Yamagami M, Yamaguchi K, Nishimura M, Uozumi N, Robertson W, Sussman MR, Schroeder JI. 2002. Altered shoot/root Na+ distribution and bifurcating salt sensitivity in Arabidopsis by genetic disruption of the Na+ transporter AtHKT1. FEBS Lett 531(2):157-161. PMID:12417304
  • Maser P, Hosoo Y, Goshima S, Horie T, Eckelman B, Yamada K, Yoshida K, Bakker EP, Shinmyo A, Oiki S, Schroeder JI, 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 U S A 99(9):6428-6433. PMID:11959905
  • Oksman-Caldentey KM, Bartz MH, eds. 2002. Molecular mechanisms that control plant tolerances to heavy metals and possible roles in manipulating metal accumulation. In: Plant Biotechnology and Transgenic Plants, New York. Marcel Kekker, Inc., New York, NY. pp.665-691.


  • Clemens S, Schroeder JI, Degenkolb T. 2001. Caenorhabditis elegans express a functional phytochelatin synthase. FEBS J 268(13):3640-3643.
  • Ghassemian M, Waner DA, Tchieu J, Gribskov M, Schroeder JI. 2001. An integrated Arabidopsis annotation database for Affymetrix Genechip data analysis, and tools for regulatory motif searches. Trends Plant Sci 6(10):448-449. PMID:11590042
  • LaCombe B, Becker D, Hedrich R, DeSalle R, Hollman M, Kwak JM, Schroeder JI, Le Novere N, Nam HG, Spalding EP, Tester M, Turano FJ, Chiu J, Coruzzi G. 2001. The identity of plant glutamate receptors. Science 292:1486-1487. PMID:11379626
  • Murata Y, Pei Z, Mori IC, Schroeder JI. 2001. ABA activation of plasma membrane Ca2+ channels in guard cells requires cytosolic NAD(P)H and is differentially disrupted upstream and downstream of reactive oxygen species production in the abi1-1 and abi2-1 PP2C mutants. Plant Cell 13:2513-2523.
  • Schroeder JI, Kwak JM, Allen GJ. 2001. Guard cell abscisic acid signalling and engineering drought hardiness in plants. Nature 410:327-330. PMID:11268200


  • Pei Z, Murata Y, Benning G, Thomine S, Klusener B, Allen GJ, Grill E, Schroeder JI. 2000. Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406:731-734. PMID:10963598
  • Thomine S, Wang R, Ward JM, Crawford NM, Schroeder JI. 2000. Cadmium and iron transport by members of a plant metal transporter family in Arabidopsis with homology to Nramp genes. Proc Natl Acad Sci U S A 97(9):4991-4996. PMID:10781110


  • Clemens S, Kim EJ, Neumann D, Schroeder JI. 1999. Tolerance to toxic metals by a gene family of phytochelatin synthases from plants and yeast. EMBO J 18(12):3325-3333. PMID:10369673
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