In order to grow on soils that vary widely in chemical composition, plants have evolved mechanisms for regulating the elemental composition of their tissues to balance the mineral nutrient and trace element bioavailability in the soil with the requirements of the plant for growth and development. The biodiversity that exists within a species can be utilized to investigate how regulatory mechanisms of individual elements interact and to identify genes important for these processes. We analyzed the elemental composition (ionome) of a set of 96 wild accessions of the genetic model plant Arabidopsis thaliana grown in hydroponic culture and soil using inductively coupled plasma mass spectrometry (ICP-MS). The concentrations of 17–19 elements were analyzed in roots and leaves from plants grown hydroponically, and leaves and seeds from plants grown in artificial soil. Significant genetic effects were detected for almost every element analyzed. We observed very few correlations between the elemental composition of the leaves and either the roots or seeds. There were many pairs of elements that were significantly correlated with each other within a tissue, but almost none of these pairs were consistently correlated across tissues and growth conditions, a phenomenon observed in several previous studies. These results suggest that the ionome of a plant tissue is variable, yet tightly controlled by genes and gene×environment interactions. The dataset provides a valuable resource for mapping studies to identify genes regulating elemental accumulation. All of the ionomic data is available at www.ionomicshub.org.
References
[1]
White PJ, Broadley MR (2009) Biofortification of crops with seven mineral elements often lacking in human diets–iron, zinc, copper, calcium, magnesium, selenium and iodine. New Phytol 182: 49–84.
[2]
Baker AJ (1987) Metal Tolerance. New Phytol 106: 93–111.
[3]
Brady KU, Kruckeberg AR, Bradshaw HD Jr (2005) EVOLUTIONARY ECOLOGY OF PLANT ADAPTATION TO SERPENTINE SOILS. Annual Review of Ecology, Evolution, and Systematics 36: 243.
[4]
Verbruggen N, Hermans C, Schat H (2009) Molecular mechanisms of metal hyperaccumulation in plants. New Phytol 181: 759–776.
[5]
Courbot M, Willems G, Motte P, Arvidsson S, Roosens N, et al. (2007) A major quantitative trait locus for cadmium tolerance in Arabidopsis halleri colocalizes with HMA4, a gene encoding a heavy metal ATPase. Plant Physiol 144: 1052–1065.
[6]
Hanikenne M, Talke IN, Haydon MJ, Lanz C, Nolte A, et al. (2008) Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 453: 391–395.
[7]
Lexer C, Welch ME, Durphy JL, Rieseberg LH (2003) Natural selection for salt tolerance quantitative trait loci (QTLs) in wild sunflower hybrids: implications for the origin of Helianthus paradoxus, a diploid hybrid species. Mol Ecol 12: 1225–1235.
[8]
Lowry DB, Hall MC, Salt DE, Willis JH (2009) Genetic and physiological basis of adaptive salt tolerance divergence between coastal and inland Mimulus guttatus. New Phytol 183: 776–788.
[9]
Turner TL, Bourne EC, Von Wettberg EJ, Hu TT, Nuzhdin SV (2010) Population resequencing reveals local adaptation of Arabidopsis lyrata to serpentine soils. Nat Genet 42: 260–263.
[10]
Hoffmann MH (2002) Biogeography of Arabidopsis thaliana (L.) Heynh. (Brassicaceae). Journal of Biogeography 29: 125–134.
[11]
Bradshaw HD Jr (2005) Mutations in CAX1 produce phenotypes characteristic of plants tolerant to serpentine soils. New Phytol 167: 81–88.
[12]
DeRose-Wilson L, Gaut BS (2011) Mapping salinity tolerance during Arabidopsis thaliana germination and seedling growth. PLoS One 6: e22832.
[13]
Galpaz N, Reymond M (2010) Natural variation in Arabidopsis thaliana revealed a genetic network controlling germination under salt stress. PLoS One 5: e15198.
[14]
Baxter I (2009) Ionomics: studying the social network of mineral nutrients. Curr Opin Plant Biol 12: 381–386.
[15]
Baxter I (2010) Ionomics: The functional genomics of elements. Briefings in Functional Genomics 9: 149–156.
[16]
Salt DE, Baxter I, Lahner B (2008) Ionomics and the study of the plant ionome. Annu Rev Plant Biol 59: 709–733.
[17]
Prinzenberg AE, Barbier H, Salt DE, Stich B, Reymond M (2010) Relationships between growth, growth response to nutrient supply, and ion content using a recombinant inbred line population in Arabidopsis. Plant Physiol 154: 1361–1371.
[18]
Baxter I, Hosmani PS, Rus A, Lahner B, Borevitz JO, et al. (2009) Root suberin forms an extracellular barrier that affects water relations and mineral nutrition in Arabidopsis. PLoS Genet 5: e1000492.
[19]
Baxter IR, Vitek O, Lahner B, Muthukumar B, Borghi M, et al. (2008) The leaf ionome as a multivariable system to detect a plant’s physiological status. Proc Natl Acad Sci U S A 105: 12081–12086.
[20]
Chao DY, Gable K, Chen M, Baxter I, Dietrich CR, et al. (2011) Sphingolipids in the Root Play an Important Role in Regulating the Leaf Ionome in Arabidopsis thaliana. Plant Cell 23: 1061–1081.
[21]
Atwell S, Huang Y, Vilhjálmsson B, Willems G, Horton M, et al. (2010) Genome-wide association study of 107 phenotypes in a common set of Arabidopsis thaliana inbred lines. Nature 465: 627–631.
[22]
Nordborg M, Hu TT, Ishimo Y, Toomajian C, Zheng HG, et al. (2005) The pattern of polymorphism in Arabidopsis thaliana. PLOS Biol 3: e196.
[23]
Baxter I, Brazelton JN, Yu D, Huang YS, Lahner B, et al. (2010) A Coastal Cline in Sodium Accumulation in Arabidopsis thaliana Is Driven by Natural Variation of the Sodium Transporter AtHKT1;1. PLoS Genet 6: e1001193.
[24]
Buescher E, Achberger T, Amusan I, Giannini A, Ochsenfeld C, et al. (2010) Natural genetic variation in selected populations of Arabidopsis thaliana is associated with ionomic differences. PLoS One 5: e11081.
[25]
Ding G, Yang M, Hu Y, Liao Y, Shi L, et al. (2010) Quantitative trait loci affecting seed mineral concentrations in Brassica napus grown with contrasting phosphorus supplies. Ann Bot 105: 1221–1234.
[26]
Ghandilyan A, Barboza L, Tisne S, Granier C, Reymond M, et al. (2009) Genetic analysis identifies quantitative trait loci controlling rosette mineral concentrations in Arabidopsis thaliana under drought. New Phytol 184: 180–192.
[27]
Ghandilyan A, Ilk N, Hanhart C, Mbengue M, Barboza L, et al. (2009) A strong effect of growth medium and organ type on the identification of QTLs for phytate and mineral concentrations in three Arabidopsis thaliana RIL populations. J Exp Bot 60: 1409–1425.
[28]
Klein MA, Grusak MA (2009) Identification of nutrient and physical seed trait QTL in the model legume Lotus japonicus. Genome 52: 677–691.
[29]
Liu J, Yang J, Li R, Shi L, Zhang C, et al. (2009) Analysis of genetic factors that control shoot mineral concentrations in rapeseed (Brassica napus) in different boron environments. Plant Soil 320: 255–266.
[30]
Sankaran RP, Huguet T, Grusak MA (2009) Identification of QTL affecting seed mineral concentrations and content in the model legume Medicago truncatula. Theor Appl Genet 119: 241–253.
[31]
Vreugdenhil D, Aarts MGM, Koornneef M, Nelissen H, Ernst WHO (2004) Natural variation and QTL analysis for cationic mineral content in seeds of Arabidopsis thaliana. Plant Cell Environ 27: 828–839.
[32]
Waters BM, Grusak MA (2008) Quantitative trait locus mapping for seed mineral concentrations in two Arabidopsis thaliana recombinant inbred populations. New Phytol 179: 1033–1047.
[33]
Lahner B, Gong J, Mahmoudian M, Smith EL, Abid KB, et al. (2003) Genomic scale profiling of nutrient and trace elements in Arabidopsis thaliana. Nat Biotechnol 21: 1215–1221.
[34]
Baxter I, Muthukumar B, Park HC, Buchner P, Lahner B, et al. (2008) Variation in molybdenum content across broadly distributed populations of Arabidopsis thaliana is controlled by a mitochondrial molybdenum transporter (MOT1). PLoS Genet 4: e1000004.
[35]
Kobayashi Y, Kuroda K, Kimura K, Southron-Francis JL, Furuzawa A, et al. (2008) Amino acid polymorphisms in strictly conserved domains of a P-type ATPase HMA5 are involved in the mechanism of copper tolerance variation in Arabidopsis. Plant Physiol 148: 969–980.
[36]
Loudet O, Saliba-Colombani V, Camilleri C, Calenge F, Gaudon V, et al. (2007) Natural variation for sulfate content in Arabidopsis thaliana is highly controlled by APR2. Nat Genet 39: 896–900.
[37]
Morrissey J, Baxter I, Lee J, Li L, Lahner B, et al. (2009) The ferroportin metal efflux proteins function in iron and cobalt homeostasis in Arabidopsis. Plant Cell.
[38]
Rus A, Baxter I, Muthukumar B, Gustin J, Lahner B, et al. (2006) Natural variants of AtHKT1 enhance Na+ accumulation in two wild populations of Arabidopsis. PLoS Genet 2: e210.
[39]
Broadley MR, Hammond JP, King GJ, Astley D, Bowen HC, et al. (2008) Shoot calcium and magnesium concentrations differ between subtaxa, are highly heritable, and associate with potentially pleiotropic loci in Brassica oleracea. Plant Physiol 146: 1707–1720.
[40]
Broadley MR, Hammond JP, White PJ, Salt DE (2010) An efficient procedure for normalizing ionomics data for Arabidopsis thaliana. New Phytol 186: 270–274.
[41]
Karley AJ, White PJ (2009) Moving cationic minerals to edible tissues: potassium, magnesium, calcium. Curr Opin Plant Biol 12: 291–298.
[42]
Watanabe T, Broadley MR, Jansen S, White PJ, Takada J, et al. (2007) Evolutionary control of leaf element composition in plants. New Phytol 174: 516–523.
[43]
Hermans C, Chen J, Coppens F, Inze D, Verbruggen N (2011) Low magnesium status in plants enhances tolerance to cadmium exposure. New Phytol 192: 428–436.
[44]
Waters BM, Grusak MA (2008) Whole-plant mineral partitioning throughout the life cycle in Arabidopsis thaliana ecotypes Columbia, Landsberg erecta, Cape Verde Islands, and the mutant line ysl1ysl3. New Phytol 177: 389–405.
[45]
Durrett TP, Gassmann W, Rogers EE (2007) The FRD3-mediated efflux of citrate into the root vasculature is necessary for efficient iron translocation. Plant Physiol 144: 197–205.
[46]
Michelmore RW, Paran I, Kesseli RV (1991) Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc Natl Acad Sci U S A 88: 9828–9832.
[47]
Becker A, Chao DY, Zhang X, Salt DE, Baxter I (2011) Bulk segregant analysis using single nucleotide polymorphism microarrays. PLoS One 6: e15993.
[48]
Baxter I, Ouzzani M, Orcun S, Kennedy B, Jandhyala SS, et al. (2007) Purdue Ionomics Information Management System. An integrated functional genomics platform. Plant Physiol 143: 600–611.
