Elemental Concentrations in the Seed of Mutants and Natural Variants of Arabidopsis thaliana Grown under Varying Soil Conditions

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  McDowell, Stephen C ^a   Akmakjian, Garo ^b   Sladek, Chris ^a   Mendoza Cozatl, David ^b   Morrissey, Joe B ^c   Saini, Nick ^a   Mittler, Ron ^f   Baxter, Ivan ^g   Salt, David E ^d   Ward, John M ^e   Schroeder, Julian I ^b   Guerinot, Mary Lou ^c   Harper, Jeffrey F ^a  

^a UNIVERSITY OF NEVADA   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c Dartmouth College   (United States)

^d UNIVERSITY OF ABERDEEN   (United Kingdom)

^e UNIVERSITY OF MINNESOTA   (United States)

^f UNIVERSITY OF NORTH TEXAS   (United States)

^g DONALD DANFORTH PLANT SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALI; BARIUM; CADMIUM; CALCIUM; COPPER; ELEMENT; HEAVY METAL; IRON; LITHIUM; MAGNESIUM; MANGANESE; MOLYBDENUM; PHOSPHORUS; POTASSIUM; SODIUM; SODIUM CHLORIDE; SULFUR; ZINC;

ABH1 GENE; ARABIDOPSIS THALIANA; ARTICLE; AT3G14280 GENE; CATION CHLORIDE COTRANSPORTER GENE; CONTROLLED STUDY; CYCLIC NUCLEOTIDE GATED CHANNEL 2 GENE; NONHUMAN; NUTRIENT CONTENT; PILOT STUDY; PLANT GENE; PLANT GENOME; PLANT GROWTH; PLANT SEED; SOIL; SOS2 GENE;

ARABIDOPSIS THALIANA;

EID: 84877096991     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0063014     Document Type: Article

References (81)

1. Marschner H (1995) Mineral Nutrition of Higher Plants. Ed 2. San Diego: Academic Press.
2. Baxter I, (2009) Ionomics: studying the social network of mineral nutrients. Curr Opin Plant Biol 12: 381-386.
3. Baxter I, (2010) Ionomics: The functional genomics of elements. Briefings Funct Genomics 9: 149-156.
4. Salt DE, Baxter I, Lahner B, (2008) Ionomics and the study of the plant ionome. Annu Rev Plant Biol 59: 709-733.
5. Chen Z, Watanabe T, Shinano T, Okazaki K, Osaki M, et al. (2008) Rapid characterization of plant mutants with an altered ion-profile: a case study using Lotus japonicus. New Phytol 181: 795-801.
6. Eide DJ, Clark S, Nair TM, Gehl M, Gribskov M, et al. (2005) Characterization of the yeast ionome: a genome-wide analysis of nutrient mineral and trace element homeostasis in Saccharomyces cerevisiae. Genome Biol 6: R77.
7. 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.
8. Danku JMC, Gumaelius L, Baxter I, Salt DE, (2009) A high-throughput method for Saccharomyces cerevisiae (yeast) ionomics. J Anal At Spectrom 24: 103.
9. Kobayashi Y, Koyama H, (2002) QTL analysis of Al tolerance in recombinant inbred lines of Arabidopsis thaliana. Plant Cell Physiol 43: 1526-1533.
10. Bentsink L, Yuan K, Koornneef M, Vreugdenhil D, (2003) The genetics of phytate and phosphate accumulation in seeds and leaves of Arabidopsis thaliana, using natural variation. Theor Appl Genet 106: 1234-1243.
11. Hoekenga OA, Vision TJ, Shaff JE, Monforte AJ, Lee GP, et al. (2003) Identification and characterization of aluminum tolerance loci in Arabidopsis (Landsberg erecta x Columbia) by quantitative trait locus mapping. A physiologically simple but genetically complex trait. Plant Physiol 132: 936-948.
12. Payne KA, Bowen HC, Hammond JP, Hampton CR, Lynn JR, et al. (2004) Natural genetic variation in caesium (Cs) accumulation by Arabidopsis thaliana. New Phytol 162: 535-548.
13. 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.
14. 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.
15. Conn SJ, Berninger P, Broadley MR, Gilliham M, (2012) Exploiting natural variation to uncover candidate genes that control element accumulation in Arabidopsis thaliana. New Phytol 193: 859-866.
16. Baxter I, Hermans C, Lahner B, Yakubova E, Tikhonova M, et al. (2012) Biodiversity of mineral nutrient and trace element accumulation in Arabidopsis thaliana. PloS One 7: e35121.
17. 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.
18. 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.
19. 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.
20. 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.
21. 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.
22. Morrissey J, Baxter IR, Lee J, Li L, Lahner B, et al. (2009) The ferroportin metal efflux proteins function in iron and cobalt homeostasis in Arabidopsis. Plant Cell 21: 3326-3338.
23. Tian H, Baxter IR, Lahner B, Reinders A, Salt DE, et al. (2010) Arabidopsis NPCC6/NaKR1 is a phloem mobile metal binding protein necessary for phloem function and root meristem maintenance. Plant Cell 22: 3963-3979.
24. Garcia-Oliveira AL, Tan L, Fu Y, Sun C, (2009) Genetic identification of quantitative trait loci for contents of mineral nutrients in rice grain. J Integr Plant Biol 51: 84-92.
25. Munns R, James RA, Xu B, Athman A, Conn SJ, et al. (2012) Wheat grain yield on saline soils is improved by an ancestral Na(+) transporter gene. Nat Biotechnol 30: 360-364.
26. Sánchez-Rodríguez E, Rubio-Wilhelmi M, Cervilla LM, Blasco B, Rios JJ, et al. (2010) Study of the ionome and uptake fluxes in cherry tomato plants under moderate water stress conditions. Plant Soil 335: 339-347.
27. Sorić R, Ledenčan T, Zdunić Z, Jambrović A, Brkić I, et al. (2011) Quantitative trait loci for metal accumulation in maize leaf. Maydica 56: 323-329.
28. Ernst WH, Nelissen HJ, Ten Bookum WM, (2000) Combination toxicology of metal-enriched soils: physiological responses of a Zn- and Cd-resistant ecotype of Silene vulgaris on polymetallic soils. Environ Exp Bot 43: 55-71.
29. Ghandilyan A, Barboza L, Tisné 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.
30. 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.
31. 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.
32. 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.
33. Zhu JK, Liu J, Xiong L, (1998) Genetic analysis of salt tolerance in Arabidopsis. Evidence for a critical role of potassium nutrition. Plant Cell 10: 1181-1191.
34. Huang G-T, Ma S-L, Bai L-P, Zhang L, Ma H, et al. (2012) Signal transduction during cold, salt, and drought stresses in plants. Mol Biol Rep 39: 969-987.
35. Zhu JK, (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6: 441-445.
36. Mahajan S, Pandey GK, Tuteja N, (2008) Calcium- and salt-stress signaling in plants: shedding light on SOS pathway. Arch Biochem Biophys 471: 146-158.
37. Liu J, Ishitani M, Halfter U, Kim CS, Zhu JK, (2000) The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. Proc Natl Acad Sci U S A 97: 3730-3734.
38. Quintero FJ, Ohta M, Shi H, Zhu J-K, Pardo JM, (2002) Reconstitution in yeast of the Arabidopsis SOS signaling pathway for Na+ homeostasis. Proc Natl Acad Sci U S A 99: 9061-9066.
39. Qiu Q-S, Guo Y, Dietrich MA, Schumaker KS, Zhu J-K, (2002) Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc Natl Acad Sci U S A 99: 8436-8441.
40. Shi H, Ishitani M, Kim C, Zhu JK, (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proc Natl Acad Sci U S A 97: 6896-6901.
41. Qiu Q-S, Guo Y, Quintero FJ, Pardo JM, Schumaker KS, et al. (2004) Regulation of vacuolar Na+/H+ exchange in Arabidopsis thaliana by the salt-overly-sensitive (SOS) pathway. J Biol Chem 279: 207-215.
42. Shi H, Quintero FJ, Pardo JM, Zhu J-K, (2002) The putative plasma membrane Na(+)/H(+) antiporter SOS1 controls long-distance Na(+) transport in plants. Plant Cell 14: 465-477.
43. Hugouvieux V, Kwak JM, Schroeder JI, (2001) An mRNA cap binding protein, ABH1, modulates early abscisic acid signal transduction in Arabidopsis. Cell 106: 477-487.
44. Hugouvieux V, Murata Y, Young JJ, Kwak JM, Mackesy DZ, et al. (2002) Localization, ion channel regulation, and genetic interactions during abscisic acid signaling of the nuclear mRNA cap-binding protein, ABH1. Plant Physiol 130: 1276-1287.
45. Izaurralde E, Stepinski J, Darzynkiewicz E, Mattaj IW, (1992) A cap binding protein that may mediate nuclear export of RNA polymerase II-transcribed RNAs. J Cell Biol 118: 1287-1295.
46. Hamm J, Mattaj IW, (1990) Monomethylated cap structures facilitate RNA export from the nucleus. Cell 63: 109-118.
47. Balatsos NAA, Nilsson P, Mazza C, Cusack S, Virtanen A, (2006) Inhibition of mRNA deadenylation by the nuclear cap binding complex (CBC). J Biol Chem 281: 4517-4522.
48. Kuhn JM, Hugouvieux V, Schroeder JI, (2007) mRNA cap binding proteins: effects on abscisic acid signal transduction, mRNA processing, and microarray analyses. Curr Top Microbiol Immunol 326: 139-150.
49. Raczynska KD, Simpson CG, Ciesiolka A, Szewc L, Lewandowska D, et al. (2010) Involvement of the nuclear cap-binding protein complex in alternative splicing in Arabidopsis thaliana. Nucleic Acids Res 38: 265-278.
50. Chen X, (2008) A silencing safeguard: links between RNA silencing and mRNA processing in Arabidopsis. Dev Cell 14: 811-812.
51. Gregory BD, O'Malley RC, Lister R, Urich MA, Tonti-Filippini J, et al. (2008) A link between RNA metabolism and silencing affecting Arabidopsis development. Dev Cell 14: 854-866.
52. Laubinger S, Sachsenberg T, Zeller G, Busch W, Lohmann JU, et al. (2008) Dual roles of the nuclear cap-binding complex and SERRATE in pre-mRNA splicing and microRNA processing in Arabidopsis thaliana. Proc Natl Acad Sci U S A 105: 8795-8800.
53. Kim S, Yang J-Y, Xu J, Jang I-C, Prigge MJ, et al. (2008) Two cap-binding proteins CBP20 and CBP80 are involved in processing primary MicroRNAs. Plant Cell Physiol 49: 1634-1644.
54. Bush MS, Hutchins AP, Jones AME, Naldrett MJ, Jarmolowski A, et al. (2009) Selective recruitment of proteins to 5′ cap complexes during the growth cycle in Arabidopsis. Plant J 59: 400-412.
55. Colmenero-Flores JM, Martínez G, Gamba G, Vázquez N, Iglesias DJ, et al. (2007) Identification and functional characterization of cation-chloride cotransporters in plants. Plant J 50: 278-292.
56. Grennan AK, (2006) Genevestigator. Facilitating web-based gene-expression analysis. Plant Physiol 141: 1164-1166.
57. Russell JM, (2000) Sodium-potassium-chloride cotransport. Physiol Rev 80: 211-276.
58. Kong X-Q, Gao X-H, Sun W, An J, Zhao Y-X, et al. (2011) Cloning and functional characterization of a cation-chloride cotransporter gene OsCCC1. Plant Mol Biol 75: 567-578.
59. Gollery M, Harper J, Cushman J, Mittler T, Girke T, et al. (2006) What makes species unique? The contribution of proteins with obscure features. Genome Biol 7: R57.
60. Gollery M, Harper J, Cushman J, Mittler T, Mittler R, (2007) POFs: what we don't know can hurt us. Trends Plant Sci 12: 492-496.
61. Krogh A, Larsson B, Von Heijne G, Sonnhammer EL, (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305: 567-580.
62. Mäser P, Thomine S, Schroeder JI, Ward JM, Hirschi K, et al. (2001) Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol 126: 1646-1667.
63. Leng Q, Mercier RW, Yao W, Berkowitz GA, (1999) Cloning and first functional characterization of a plant cyclic nucleotide-gated cation channel. Plant Physiol 121: 753-761.
64. Leng Q, Mercier RW, Hua B-G, Fromm H, Berkowitz GA, (2002) Electrophysiological analysis of cloned cyclic nucleotide-gated ion channels. Plant Physiol 128: 400-410.
65. Ali R, Ma W, Lemtiri-Chlieh F, Tsaltas D, Leng Q, et al. (2007) Death don't have no mercy and neither does calcium: Arabidopsis CYCLIC NUCLEOTIDE GATED CHANNEL2 and innate immunity. Plant Cell 19: 1081-1095.
66. Chan CWM, Schorrak LM, Smith RK, Bent AF, Sussman MR, (2003) A cyclic nucleotide-gated ion channel, CNGC2, is crucial for plant development and adaptation to calcium stress. Plant Physiol 132: 728-731.
67. Clough SJ, Fengler KA, Yu IC, Lippok B, Smith RK, et al. (2000) The Arabidopsis dnd1 "defense, no death" gene encodes a mutated cyclic nucleotide-gated ion channel. Proc Natl Acad Sci U S A 97: 9323-9328.
68. Gobert A, Park G, Amtmann A, Sanders D, Maathuis FJM, (2006) Arabidopsis thaliana cyclic nucleotide gated channel 3 forms a non-selective ion transporter involved in germination and cation transport. J Exp Bot 57: 791-800.
69. Ma W, Ali R, Berkowitz GA, (2006) Characterization of plant phenotypes associated with loss-of-function of AtCNGC1, a plant cyclic nucleotide gated cation channel. Plant Physiol Biochem 44: 494-505.
70. Guo KM, Babourina O, Christopher DA, Borsic T, Rengel Z, (2010) The cyclic nucleotide-gated channel AtCNGC10 transports Ca2+ and Mg2+ in Arabidopsis. Physiol Plant 139: 303-312.
71. Frietsch S, Wang Y-F, Sladek C, Poulsen LR, Romanowsky SM, et al. (2007) A cyclic nucleotide-gated channel is essential for polarized tip growth of pollen. Proc Natl Acad Sci U S A 104: 14531-14536.
72. Baxter I, Dilkes BP, (2012) Elemental profiles reflect plant adaptations to the environment. Science 336: 1661-1663.
73. Mäser P, Eckelman B, Vaidyanathan R, Horie T, Fairbairn DJ, et al. (2002) Altered shoot/root Na+ distribution and bifurcating salt sensitivity in Arabidopsis by genetic disruption of the Na+ transporter AtHKT1. FEBS Lett 531: 157-161.
74. Salt DE, (2004) Update on plant ionomics. Plant Physiol 136: 2451-2456.
75. Nordborg M, Hu TT, Ishino Y, Jhaveri J, Toomajian C, et al. (2005) The pattern of polymorphism in Arabidopsis thaliana. PLoS Biol 3: e196.
76. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657.
77. Sessions A, Burke E, Presting G, Aux G, Mcelver J, et al. (2002) A high-throughput Arabidopsis reverse genetics system. Plant Cell 14: 2985-2994.
78. Woody ST, Austin-Phillips S, Amasino RM, Krysan PJ, (2007) The WiscDsLox T-DNA collection: an Arabidopsis community resource generated by using an improved high-throughput T-DNA sequencing pipeline. J Plant Res 120: 157-165.
79. Sundaresan V, Springer P, Volpe T, Haward S, Jones JD, et al. (1995) Patterns of gene action in plant development revealed by enhancer trap and gene trap transposable elements. Genes Dev 9: 1797-1810.
80. Tissier AF, Marillonnet S, Klimyuk V, Patel K, Torres MA, et al. (1999) Multiple independent defective suppressor-mutator transposon insertions in Arabidopsis: a tool for functional genomics. Plant Cell 11: 1841-1852.
81. Krysan PJ, Young JC, Tax F, Sussman MR, (1996) Identification of transferred DNA insertions within Arabidopsis genes involved in signal transduction and ion transport. Proc Natl Acad Sci U S A 93: 8145-8150.