Professor Andrew Smith

Research interests

Cellular and molecular basis of plant responses to drought, salinity and heavy metals


The distribution and accumulation of solutes in plants depends on the activity of precisely regulated transport processes at the cellular level. These can play an important role in plant responses to environmental stress. We are investigating the molecular basis of plant adaptations to drought, salinity and metals. Much of our work focuses on solute accumulation in the cell vacuole, since this provides the most important storage compartment for osmotically active and potentially cytotoxic ions.

One system studied as a paradigm for regulation of vacuolar solute transport is malic-acid accumulation in plants showing crassulacean acid metabolism (CAM). This process is energized by a vacuolar H+-ATPase (V-ATPase), which drives the influx of malate ions across the tonoplast through a malate-selective ion channel. A combination of approaches has been used to study the mechanism of both malate influx and efflux, as well as the metabolic characteristics of CAM induction during leaf development. In halophytic CAM plants, such as Mesembryanthemum crystallinum, CAM is environmentally regulated, and cell vacuoles can accumulate sodium chloride to concentrations in excess of 1.0 M. We have been studying the transport of both Na+ and Cl- using ion-sensitive fluorescent probes and the patch-clamp technique, as well as the transcriptional regulation of genes encoding the V-ATPase.

Our other major research effort is in the study of "metal-hyperaccumulator plants". These are extremely metal-tolerant plants that accumulate exceptional concentrations of transition metals in their leaves (for example, more than 3 % by dry biomass of nickel or zinc). We are investigating the cellular and molecular basis of this phenomenon to improve our understanding of metal-ion homeostasis in plant cells. Further, it is possible that such plants may aid in the clean-up of contaminated soils through the process of phytoremediation. However, many soils are polluted with mixtures of both organic and inorganic contaminants, and the implications of this for the bioremediation process are being investigated.

Contact details

+44 (0) 1865 275009

Publications (while at this department)

Snowden, C.J, Thomas, B, Baxter, C.J, Smith, J.A.C, Sweetlove, L.J. (2015) A tonoplast Glu/Asp/GABA exchanger that affects tomato fruit amino acid composition Plant Journal. 81 (5): pp 651-660doi:10.1111/tpj.12766.

Givnish, T.J, Barfuss, M.H.J, Ee, B.V, Riina, R, Schulte, K, Horres, R, Gonsiska, P.A, Jabaily, R.S, Crayn, D.M, Smith, J.A.C, Winter, K, Brown, G.K, Evans, T.M, Holst, B.K, Luther, H, Till, W, Zizka, G, Berry, P.E, Sytsma, K.J. (2014) Adaptive radiation, correlated and contingent evolution, and net species diversification in Bromeliaceae Molecular Phylogenetics and Evolution. 71 (1): pp 55-78doi:10.1016/j.ympev.2013.10.010.

Fones, H.N, Eyles, C.J, Bennett, M.H, Smith, J.A.C, Preston, G.M. (2013) Uncoupling of reactive oxygen species accumulation and defence signalling in the metal hyperaccumulator plant Noccaea caerulescens New Phytologist. 199 (4): pp 916-924doi:10.1111/nph.12354.

Jiang, C, Belfield, E.J, Cao, Y, Smith, J.A.C, Harberd, N.P. (2013) An Arabidopsis soil-salinity-tolerance mutation confers ethylene-mediated enhancement of sodium/potassium homeostasis Plant Cell. 25 (9): pp 3535-3552doi:10.1105/tpc.113.115659.

Lee, R.B.Y, Smith, J.A.C, Rickaby, R.E.M. (2013) Cloning, expression and characterization of the δ-carbonic anhydrase of Thalassiosira weissflogii (Bacillariophyceae) Journal of Phycology. 49 (1): pp 170-177doi:10.1111/j.1529-8817.2012.01226.x.

Jiang, C, Belfield, E.J, Mithani, A, Visscher, A, Ragoussis, J, Mott, R, Smith, J.A.C, Harberd, N.P. (2012) ROS-mediated vascular homeostatic control of root-to-shoot soil Na delivery in Arabidopsis EMBO Journal.. doi:10.1038/emboj.2012.273.

Kapralov, M.V, Smith, J.A.C, Filatov, D.A. (2012) Rubisco Evolution in C4 Eudicots: An Analysis of Amaranthaceae Sensu Lato PLoS ONE. 7 (12):. doi:10.1371/journal.pone.0052974.

Lee, R.B.Y, Smith, J.A.C, Rickaby, R.E.M. (2012) Cloning, expression and characterization of the δ-carbonic anhydrase of Thalassiosira Weissflogii (Bacillariophyceae) Journal of Phycology.. doi:10.1111/j.1529-8817.2012.01226.x.

Wu, L.H, Liu, Y.J, Zhou, S.B, Guo, F.G, Bi, D, Guo, X.H, Baker, A.J.M, Smith, J.A.C, Luo, Y.M. (2012) Sedum plumbizincicola X.H. Guo et S.B. Zhou ex L.H. Wu (Crassulaceae): a new species from Zhejiang Province, China Plant Systematics and Evolution. pp 1-12doi:10.1007/s00606-012-0738-x.

Baresch, A, Smith, J.A.C, Winter, K, Valerio, A.L, Jaramillo, C. (2011) Karatophyllum bromelioides L.D. Gómez revisited: A probable fossil CAM bromeliad American Journal of Botany. 98 (11): pp 1905-1908.

Givnish, T.J, Barfuss, M.H.J, van, Ee B, Riina, R, Schulte, K, Horres, R, Gonsiska, P.A, Jabaily, R.S, Crayn, D.M, Smith, J.A.C, Winter, K, Brown, G.K, Evans, T.M, Holst, B.K, Luther, H, Till, W, Zizka, G, Berry, P.E, Sytsma, K.J. (2011) Phylogeny, adaptive radiation, and historical biogeography in Bromeliaceae: Insights from an eight-locus plastid phylogeny American Journal of Botany. 98 (5): pp 872-895doi:10.3732/ajb.1000059.

West-Eberhard, M.J, Smith, J.A.C, Winter, K. (2011) Photosynthesis, reorganized Science. 332 (6027): pp 311-312doi:10.1126/science.1205336.

Yan, X, Tan, D.K.Y, Inderwildi, O.R, Smith, J.A.C, King, D.A. (2011) Life cycle energy and greenhouse gas analysis for agave-derived bioethanol Energy and Environmental Science. 4 (9): pp 3110-3121doi:10.1039/c1ee01107c.

Fones, H, Davis, C.A.R, Rico, A, Fang, F, Smith, J.A.C, Preston, G.M. (2010) Metal hyperaccumulation armors plants against disease PLoS Pathogens. 6 (9):. doi:10.1371/journal.ppat.1001093.

Smart, K.E, Smith, J.A.C, Kilburn, M.R, Martin, B.G.H, Hawes, C, Grovenor, C.R.M. (2010) High-resolution elemental localization in vacuolate plant cells by nanoscale secondary ion mass spectrometry Plant Journal. 63 (5): pp 870-879doi:10.1111/j.1365-313X.2010.04279.x.

Borland, A.M, Griffiths, H, Hartwell, J, Smith, J.A.C. (2009) Exploiting the potential of plants with crassulacean acid metabolism for bioenergy production on marginal lands Journal of Experimental Botany. 60 (10): pp 2879-2896doi:10.1093/jxb/erp118.

Rees, J.D, Ingle, R.A, Smith, J.A.C. (2009) Relative contributions of nine genes in the pathway of histidine biosynthesis to the control of free histidine concentrations in Arabidopsis thaliana Plant Biotechnology Journal. 7 (6): pp 499-511doi:10.1111/j.1467-7652.2009.00419.x.

Richau, K.H, Kozhevnikova, A.D, Seregin, I.V, Vooijs, R, Koevoets, P.L.M, Smith, J.A.C, Ivanov, V.B, Schat, H. (2009) Chelation by histidine inhibits the vacuolar sequestration of nickel in roots of the hyperaccumulator Thlaspi caerulescens New Phytologist. 183 (1): pp 106-116doi:10.1111/j.1469-8137.2009.02826.x.

Antony, E, Taybi, T, Courbot, M, Mugford, S.T, Smith, J.A.C, Borland, A.M. (2008) Cloning, localization and expression analysis of vacuolar sugar transporters in the CAM plant Ananas comosus (pineapple) Journal of Experimental Botany. 59 (7): pp 1895-1908doi:10.1093/jxb/ern077.

Ingle, R.A, Fricker, M.D, Smith, J.A.C. (2008) Evidence for nickel/proton antiport activity at the tonoplast of the hyperaccumulator plant Alyssum lesbiacum Plant Biology. 10 (6): pp 746-753doi:10.1111/j.1438-8677.2008.00080.x.

Singer, A.C, Bell, T, Heywood, C.A, Smith, J.A.C, Thompson, I.P. (2007) Phytoremediation of mixed-contaminated soil using the hyperaccumulator plant Alyssum lesbiacum: Evidence of histidine as a measure of phytoextractable nickel Environmental Pollution. 147 (1): pp 74-82.doi:10.1016/j.envpol.2006.08.029.

Smart, K.E, Kilburn, M.R, Salter, C.J, Smith, J.A.C, Grovenor, C.R.M. (2007) NanoSIMS and EPMA analysis of nickel localisation in leaves of the hyperaccumulator plant Alyssum lesbiacum International Journal of Mass Spectrometry. 260: pp 107-114doi:10.1016/j.ijms.2006.08.011.

Behmer, S.T, Lloyd, C.M, Raubenheimer, D, Stewart-Clark, J, Knight, J, Leighton, R.S, Harper, F.A, Smith, J.A.C. (2005) Metal hyperaccumulation in plants: Mechanisms of defence against insect herbivores Functional Ecology. 19 (1): pp 55-66doi:10.1111/j.0269-8463.2005.00943.x.

Eitinger, T, Suhr, J, Moore, L, Smith, J.A.C. (2005) Secondary transporters for nickel and cobalt ions: Theme and variations BioMetals. 18 (4): pp 399-405.

Holtum, J.A.M, Smith, J.A.C, Neuhaus, H.E. (2005) Intracellular transport and pathways of carbon flow in plants with crassulacean acid metabolism Functional Plant Biology. 32 (5): pp 429-449doi:10.1071/FP04189.

Ingle, R.A, Mugford, S.T, Rees, J.D, Campbell, M.M, Smith, J.A.C. (2005) Constitutively high expression of the histidine biosynthetic pathway contributes to nickel tolerance in hyperaccumulator plants Plant Cell. 17 (7): pp 2089-2106doi:10.1105/tpc.105.030577.

Ingle, R.A, Smith, J.A.C, Sweetlove, L.J. (2005) Responses to nickel in the proteome of the hyperaccumulator plant Alyssum lesbiacum BioMetals. 18 (6): pp 627-641doi:10.1007/s10534-005-2999-0.

Crayn, D.M, Winter, K, Smith, J.A.C. (2004) Multiple origins of crassulacean acid metabolism and the epiphytic habit in the Neotropical family Bromeliaceae Proceedings of the National Academy of Sciences of the United States of America. 101 (10): pp 3703-3708

Whiting, S.N, Reeves, R.D, Richards, D, Johnson, M.S, Cooke, J.A, Malaisse, F, Paton, A, Smith, J.A.C, Angle, J.S, Chaney, R.L, Ginocchio, R, Jaffre, T, Johns, R, McIntyre, T, Purvis, O.W, Salt, D.E, Schat, H, Zhao, F.J, Baker, A.J.M. (2004) Research priorities for conservation of metallophyte biodiversity and their potential for restoration and site remediation Restoration Ecology. 12 (1): pp 106-116

Hafke, J.B, Hafke, Y, Smith, J.A.C, Luttge, U, Thiel, G. (2003) Vacuolar malate uptake is mediated by an anion-selective inward rectifier Plant Journal. 35 (1): pp 116-128

Roosens, N, Verbruggen, N, Meerts, P, Ximenez-Embun, P, Smith, J.A.C. (2003) Natural variation in cadmium tolerance and its relationship to metal hyperaccumulation for seven populations of Thlaspi caerulescens from western Europe Plant, Cell and Environment. 26 (10): pp 1657-1672

Pantoja, O, Smith, J.A.C. (2002) Sensitivity of the plant vacuolar malate channel to pH, Ca2+ and anion-channel blockers Journal of Membrane Biology. 186 (1): pp 31-42. doi:10.1007/s00232-001-0132-z.

Pollard, A.J, Powell, K.D, Harper, F.A, Smith, J.A.C. (2002) The genetic basis of metal hyperaccumulation in plants Critical Reviews in Plant Sciences. 21 (6): pp 539-566

Wissing, F, Smith, J.A.C. (2000) Vacuolar chloride transport in Mesembryanthemum crystallinum L. measured using the fluorescent dye lucigenin Journal of Membrane Biology. 177 (3): pp 199-208doi:10.1007/s002320010003.

Tyerman, S.D, Bohnert, H.J, Maurel, C, Steudle, E, Smith, J.A.C. (1999) Plant aquaporins: Their molecular biology, biophysics and significance for plant water relations Journal of Experimental Botany. 50: pp 1055-1071

Murphy, R, Smith, J.A.C. (1998) Determination of cell water-relation parameters using the pressure probe: Extended theory and practice of the pressure-clamp technique Plant, Cell and Environment. 21 (7): pp 637-657.

Cheffings, C.M, Pantoja, O, Ashcroft, F.M, Smith, J.A.C. (1997) Malate transport and vacuolar ion channels in CAM plants Journal of Experimental Botany. 48: pp 623-631

Kramer, U, Grime, G.W, Smith, J.A.C, Hawes, C.R, Baker, A.J.M. (1997) Micro-PIXE as a technique for studying nickel localization in leaves of the hyperaccumulator plant Alyssum lesbiacum Nuclear Instruments and Methods in Physics Research, Section B: Beam Interactions with Materials and Atoms. 130: pp 346-350

Bartholomew, D.M, Rees, D.J.G, Rambaut, A, Smith, J.A.C. (1996) Isolation and sequence analysis of a cDNA encoding the c subunit of a vacuolar-type H+-ATPase from the CAM plant Kalanchoë daigremontiana Plant Molecular Biology. 31 (2): pp 435-442

Kramer, U, Cotter-Howells, J.D, Charnock, J.M, Baker, A.J.M, Smith, J.A.C. (1996) Free histidine as a metal chelator in plants that accumulate nickel Nature. 379 (6566): pp 635-638doi:10.1038/379635a0.

Tsiantis, M.S, Bartholomew, D.M, Smith, J.A.C. (1996) Salt regulation of transcript levels for the c subunit of a leaf vacuolar H+-ATPase in the halophyte Mesembryanthemum crystallinum Plant Journal. 9 (5): pp 729-736

Murphy, R, Smith, J.A.C. (1994) Derivation of a weighted-average reflection coefficient for mesophyll cell membranes of Kalanchoe daigremontiana Planta. 193 (1): pp 145-147

Murphy, R, Smith, J.A.C. (1994) A critical comparison of the pressure-probe and pressure-chamber techniques for estimating leaf-cell turgor pressure in Kalanchoe daigremontiana Plant, Cell and Environment. 17 (1): pp 15-29

Bettey, M, Smith, J.A.C. (1993) Dicarboxylate transport at the vacuolar membrane of the CAM plant Kalanchoe daigremontiana: Sensitivity to protein-modifying and sulphydryl reagents Biochimica et Biophysica Acta - Biomembranes. 1152 (2): pp 270-279doi:10.1016/0005-2736(93)90258-2.

White, P.J, Marshall, J, Smith, J.A.C. (1990) Substrate kinetics of the tonoplast H+-translocating inorganic pyrophosphatase and its activation by Free Mg2+ Plant Physiology. 93 (3): pp 1063-1070

List of site pages