Sultr4;1 mutant seeds of Arabidopsis have an enhanced sulphate content and modified proteome suggesting metabolic adaptations to altered sulphate compartmentalization

BMC Plant Biology

Volumn 10, Issue , 2010, Pages

  Zuber, Hélène ^a   Davidian, Jean Claude ^b   Wirtz, Markus ^c   Hell, Rüdiger ^c   Belghazi, Maya ^d   Thompson, Richard ^a   Gallardo, Karine ^a  

^a CEMAGREF   (France)

^b CNRS   (France)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d IFR Jean Roche   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS;

ANION TRANSPORT PROTEIN; ARABIDOPSIS PROTEIN; BACTERIAL DNA; CARBON; GLUTATHIONE; MESSENGER RNA; NITROGEN; PROTEOME; SULFATE; SULTR4;1 PROTEIN, ARABIDOPSIS; T DNA; T-DNA;

ADAPTATION; ARABIDOPSIS; ARTICLE; CELL COMPARTMENTALIZATION; FLOWER; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; PHYSIOLOGY; PLANT LEAF; PLANT SEED; PRENATAL DEVELOPMENT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ADAPTATION, PHYSIOLOGICAL; ANION TRANSPORT PROTEINS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CARBON; CELL COMPARTMENTATION; DNA, BACTERIAL; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FLOWERS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; GLUTATHIONE; MUTAGENESIS, INSERTIONAL; MUTATION; NITROGEN; PLANT LEAVES; PROTEOME; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEEDS; SULFATES;

EID: 77951589642     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-10-78     Document Type: Article

References (66)

1. McGrath SP, Zhao F, Crosland AR, Salmon SE. Sulphur status in British wheat grain and its relationship with quality parameters. Asp Appl Biol 1993, 36:317-326.
2. Schnug E. Sulphur nutritional status of European crops and consequences for agriculture. Sulphur Agric 1991, 15:7-12.
3. Zhao F, McGrath SP. Assessing the risk of sulphur deficiency in cereals. J Sci Food Agric 1993, 63:119.
4. Buchner P, Takahashi H, Hawkesford MJ. Plant sulphate transporters: co-ordination of uptake, intracellular and long-distance transport. J Exp Bot 2004, 55:1765-73. 10.1093/jxb/erh206, 15258169.
5. Kaiser G, Martinoia E, Schroppelmeier G, Heber U. Active-transport of sulfate into the vacuole of plant cells provides halotolerance and can detoxify SO2. J Plant Physiol 1989, 133:756-763.
6. Martinoia E, Massonneau A, Frangne N. Transport processes of solutes across the vacuolar membrane of higher plants. Plant Cell Physiol 2000, 41:1175-1186. 10.1093/pcp/pcd059, 11092901.
7. Martinoia E, Maeshima M, Neuhaus HE. Vacuolar transporters and their essential role in plant metabolism. J Exp Bot 2007, 58:83-102. 10.1093/jxb/erl183, 17110589.
8. Tabe L, Droux M. Sulfur assimilation in developing lupin cotyledons could contribute significantly to the accumulation of organic sulfur reserves in the seed. Plant Physiol 2001, 126:176-187. 10.1104/pp.126.1.176, 102292, 11351081.
9. Rouached H, Berthomieu P, El Kassis E, Cathala N, Catherinot V, Labesse G, Davidian JC, Fourcroy P. Structural and Functional Analysis of the C-terminal STAS (Sulfate Transporter and Anti-sigma Antagonist) Domain of the Arabidopsis thaliana Sulfate Transporter SULTR1.2. J Biol Chem 2005, 280:15976-15983. 10.1074/jbc.M501635200, 15718229.
10. Tomatsu H, Takano J, Takahashi H, Watanabe-Takahashi A, Shibagaki N, Fujiwara T. An Arabidopsis thaliana high-affinity molybdate transporter required for efficient uptake of molybdate from soil. Proc Natl Acad Sci USA 2007, 104:18807-12. 10.1073/pnas.0706373104, 2141858, 18003916.
11. Hawkesford MJ. Transporter gene families in plants: the sulphate transporter gene family: redundancy or specialization?. Physiol Plant 2003, 117:115-163.
12. Smith FW, Ealing PM, Hawkesford MJ, Clarkson T. Plant members of a family of sulfate transporters reveal functional subtypes. Proc Natl Acad Sci USA 1995, 92:9373-9377. 10.1073/pnas.92.20.9373, 40987, 7568135.
13. Smith FW, Hawkesford MJ, Ealing PM, Clarkson DT, Vanden Berg PJ, Belcher AR, Warrilow AG. Regulation of expression of a cDNA from barley roots encoding a high affinity sulphate transporter. Plant J 1997, 12:875-84. 10.1046/j.1365-313X.1997.12040875.x, 9375399.
14. Takahashi H, Watanabe-Takahashi A, Smith FW, Blake-Kalff M, Hawkesford MJ, Saito K. The roles of three functional sulphate transporters involved in uptake and translocation of sulphate in Arabidopsis thaliana. The Plant J 2000, 23:171-182.
15. Shibagaki N, Rose A, McDermott JP, Fujiwara T, Hayashi H, Yoneyama T, Davies JP. Selenate-resistant mutants of Arabidopsis thaliana identify Sultr1;2, a sulfate transporter required for efficient transport of sulfate into roots. Plant J 2002, 29:475-486. 10.1046/j.0960-7412.2001.01232.x, 11846880.
16. Yoshimoto N, Takahashi H, Smith FW, Yamaya T, Saito K. Two distinct high-affinity sulfate transporters with different inducibilities mediate uptake of sulfate in Arabidopsis roots. Plant J 2002, 29:465-473. 10.1046/j.0960-7412.2001.01231.x, 11846879.
17. El Kassis E, Cathala N, Rouached H, Fourcroy P, Berthomieu P, Terry N, Davidian JC. Characterization of a selenate-resistant Arabidopsis mutant. Root growth as a potential target for selenate toxicity. Plant Physiol 2007, 143:1231-1241. 10.1104/pp.106.091462, 1820920, 17208959.
18. Awazuhara M, Fujiwara T, Hayashi H, Watanabe-Takahashi A, Takahashi H, Saito K. The function of SULTR2;1 sulfate transporter during seed development in Arabidopsis thaliana. Plant Physiol 2005, 125:95-105.
19. Buchner P, Stuiver E, Westerman S, Wirtz M, Hell R, Hawkesford M, De Kok L. Regulation of Sulfate Uptake and Expression of Sulfate Transporter Genes in Brassica oleracea as Affected by Atmospheric H2S and Pedospheric Sulfate Nutrition. Plant Physiol 2004, 136:3396-3408. 10.1104/pp.104.046441, 523398, 15377780.
20. Kataoka T, Hayashi N, Yamaya T, Takahashi H. Root-to-shoot transport of sulfate in Arabidopsis: Evidence for the role of SULTR3;5 as a component of low-affinity sulfate transport system in the root vasculature. Plant Physiol 2004, 136:4198-4204. 10.1104/pp.104.045625, 535849, 15531709.
21. Kataoka T, Watanabe-Takahashi A, Hayashi N, Ohnishi M, Mimura T, Buchner P, Hawkesford MJ, Yamaya T, Takahashi H. Vacuolar sulfate transporters are essential determinants controlling internal distribution of sulfate in Arabidopsis. Plant Cell 2004, 16:2693-2704. 10.1105/tpc.104.023960, 520965, 15367713.
22. Toufighi K, Brady SM, Austin R, Ly E, Provart NJ. The Botany Array Resource: e-Northerns, Expression Angling, and promoter analyses. Plant J 2005, 43:153-163. 10.1111/j.1365-313X.2005.02437.x, 15960624.
23. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Huaming C, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, Gadrinab C, Heller C, Jeske A, Koesema E, Meyers CC, Parker H, Prednis L, Ansari Y, Choy N, Deen H, Geralt M, Hazari N, Hom E, Karnes M, Mulholland C, Ndubaku R, Schmidt I, Guzman P, Aguilar-Henonin L, Schmid M, Weigel D, Carter D, Marchand T, Risseeuw E, Brogden D, Zeko A, Crosby WL, Berry CC, Ecker JR. Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 2003, 301:653-657. 10.1126/science.1086391, 12893945.
24. Shibagaki N, Grossman AR. The role of the STAS domain in the function and biogenesis of a sulfate transporter as probed by random mutagenesis. J Biol Chem 2006, 281:22964-22973. 10.1074/jbc.M603462200, 16754669.
25. Gallardo K, Job C, Groot SP, Puype M, Demol H, Vandekerckhove J, Job D. Proteomic analysis of Arabidopsis seed germination and priming. Plant Physiol 2001, 126:835-848. 10.1104/pp.126.2.835, 111173, 11402211.
26. Gallardo K, Job C, Groot SP, Puype M, Demol H, Vandekerckhove J, Job D. Proteomics of Arabidopsis seed germination. A comparative study of wild-type and gibberellin-deficient seeds. Plant Physiol 2002, 129:823-837. 10.1104/pp.002816, 161704, 12068122.
27. Rajjou L, Gallardo K, Debeaujon I, Vandekerckhove J, Job C, Job D. The effect of α-amanitin on the Arabidopsis seed proteome highlights the distinct roles of stored and neosynthesized mRNAs during germination. Plant Physiol 2004, 134:1598-1613. 10.1104/pp.103.036293, 419834, 15047896.
28. Bevan M, Bancroft I, Bent E, Love K, Goodman H, Dean C, Bergkamp R, Dirkse W, Van Staveren M, Stiekema W, Drost L, Ridley P, Hudson SA, Patel K, Murphy G, Piffanelli P, Wedler H, Wedler E, Wambutt R, Weitzenegger T, Pohl TM, Terryn N, Gielen J, Villarroel R, De Clerck R, Van Montagu M, Lecharny A, Auborg S, Gy I, Kreis M, Lao N, Kavanagh T, Hempel S, Kotter P, Entian KD, Rieger M, Schaeffer M, Funk B, Mueller-Auer S, Silvey M, James R, Montfort A, Pons A, Puigdomenech P, Douka A, Voukelatou E, Milioni D, Hatzopoulos P, Piravandi E, Obermaier B, Hilbert H, Düsterhöft A, Moores T, Jones JD, Eneva T, Palme K, Benes V, Rechman S, Ansorge W, Cooke R, Berger C, Delseny M, Voet M, Volckaert G, Mewes HW, Klosterman S, Schueller C, Chalwatzis N. Analysis of 1.9 Mb of contiguous sequence from chromosome 4 of Arabidopsis thaliana. Nature 1998, 391:485-488. 10.1038/35140, 9461215.
29. Sweetlove LJ, Heazlewood JL, Herald V, Holtzapffel R, Day DA, Leaver CJ, Millar AH. The impact of oxidative stress on Arabidopsis mitochondria. Plant J 2002, 32:891-904. 10.1046/j.1365-313X.2002.01474.x, 12492832.
30. Bindschedler LV, Palmblad M, Cramer R. Hydroponic isotope labelling of entire plants (HILEP) for quantitative plant proteomics; an oxidative stress case study. Phytochem 2008, 69:1962-1972.
31. Desikan R, Mackerness SA-H, Hancock JT, Neill SJ. Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol 2001, 127:159-172. 10.1104/pp.127.1.159, 117972, 11553744.
32. Nikiforova V, Freitag J, Kempa S, Adamikn M, Hesse H, Hoefgen R. Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: interlacing of biosynthetic pathways provides response specificity. Plant J 2003, 33:633-650. 10.1046/j.1365-313X.2003.01657.x, 12609038.
33. Maruyama-Nakashita A, Inoue E, Watanabe-Takahashi A, Yamaya T, Takahashi H. Transcriptome profiling of sulfur-responsive genes in Arabidopsis reveals global effects of sulfur nutrition on multiple metabolic pathways. Plant Physiol 2003, 132:597-605. 10.1104/pp.102.019802, 167000, 12805590.
34. Higashi Y, Hirai MY, Fujiwara T, Naito S, Noji M, Saito K. Proteomic and transcriptomic analysis of Arabidopsis seeds: molecular evidence for successive processing of seed proteins and its implication in the stress response to sulfur nutrition. Plant J 2006, 48:557-571. 10.1111/j.1365-313X.2006.02900.x, 17059406.
35. Chen W, Singh K. The auxin, hydrogen peroxide and salicylic acid induced expression of the Arabidopsis GST6 promoter is mediated in part by an ocs element. Plant J 1999, 19:667-677. 10.1046/j.1365-313x.1999.00560.x, 10571852.
36. Job C, Rajjou L, Lovigny Y, Belghazi M, Job D. Patterns of protein oxidation in Arabidopsis seeds and during germination. Plant Physiol 2005, 138:790-802. 10.1104/pp.105.062778, 1150397, 15908592.
37. Rajjou L, Debeaujon I. Seed longevity: Survival and maintenance of high germination ability of dry seeds. C R Biol 2008, 331:796-805. 10.1016/j.crvi.2008.07.021, 18926494.
38. Bailly C, El-Maarouf-Bouteau H, Corbineau F. From intracellular signaling networks to cell death: the dual role of reactive oxygen species in seed physiology. C R Biol 2008, 331:806-814. 10.1016/j.crvi.2008.07.022, 18926495.
39. Herbette S, Taconnat L, Hugouvieux V, Piette L, Magniette MLM, Cuine S, Auroy P, Richaud P, Forestier C, Bourguignon J, Renou JP, Vavasseur A, Leonhardt N. Genome-wide transcriptome profiling of the early cadmium response of Arabidopsis roots and shoots. Biochimie 2006, 88:1751-1765. 10.1016/j.biochi.2006.04.018, 16797112.
40. Cho UH, Seo NH. Oxidative stress in Arabidopsis thaliana exposed to cadmium is due to hydrogen peroxide accumulation. Plant Sci 2005, 168:113-120.
41. Srivastava S, Srivastava AK, Suprasanna P, D'Souza SF. Comparative biochemical and transcriptional profiling of two contrasting varieties of Brassica juncea L. in response to arsenic exposure reveals mechanisms of stress perception and tolerance. J Exp Bot 2009, 60:3419-3431. 10.1093/jxb/erp181, 19528528.
42. Mascher R, Lippmann B, Holzinger S, Bergmann H. Arsenate toxicity: effects on oxidative stress response molecules and enzymes in red clover plants. Plant Sci 2002, 163:961-969.
43. Li F, Asami T, Wu X, Tsang EWT, Cutler A. A Putative Hydroxysteroid Dehydrogenase Involved in Regulating Plant Growth and Development. Plant Physiol 2007, 145:87-97. 10.1104/pp.107.100560, 1976581, 17616511.
44. Baud S, Lepiniec L. Regulation of de novo fatty acid synthesis in maturing oilseeds of Arabidopsis. Plant Physiology and Biochemistry 2009, 47:448-455. 10.1016/j.plaphy.2008.12.006, 19136270.
45. Higgins TJ, Chandler PM, Randall PJ, Spencer D, Beach LR, Blagrove RJ, Kortt AA, Inglis AS. Gene structure, protein structure, and regulation of the synthesis of a sulfur-rich protein in pea seeds. J Biol Chem 1986, 261:11124-11130.
46. Hirai MY, Fujiwara T, Chino M, Naito S. Effects of sulfate concentrations on the expression of a soybean seed storage protein gene and its reversibility in transgenic Arabidopsis thaliana. Plant Cell Physiol 1995, 36:1331-1339.
47. Tabe L, Droux M. Limits to sulfur accumulation in transgenic lupin seeds expressing a foreign sulfur-rich protein. Plant Physiol 2002, 128:1137-1148. 10.1104/pp.010935, 152225, 11891268.
48. Nikiforova VJ, Kopka J, Tolstikov V, Fiehn O, Hopkins L, Hawkesford MJ, Hesse H, Hoefgen R. Systems Rebalancing of Metabolism in Response to Sulfur Deprivation, as Revealed by Metabolome Analysis of Arabidopsis Plants. Plant Physiol 2005, 138:304-318. 10.1104/pp.104.053793, 1104185, 15834012.
49. Nikiforova VJ, Bielecka M, Gakière B, Krueger S, Rinder J, Kempa S, Morcuende R, Scheible WR, Hesse H, Hoefgen R. Effect of sulfur availability on the integrity of amino acid biosynthesis in plants. Amino acids 2006, 30:173-183. 10.1007/s00726-005-0251-4, 16552493.
50. Ravanel S, Gakière B, Job D, Douce R. The specific features of methionine biosynthesis and metabolism in plants. Proc Nat Acad Sci USA 1998, 95:7805-7812. 10.1073/pnas.95.13.7805, 22764, 9636232.
51. Ravanel S, Block MA, Rippert P, Jabrin S, Curien G, Rébeillé F, Douce R. Methionine metabolism in plants: chloroplasts are autonomous for de novo methionine synthesis and can import S-adenosylmethionine from the cytosol. J Biol Chem 2004, 279:22548-22557. 10.1074/jbc.M313250200, 15024005.
52. Levine RL, Mosoni L, Berlett BS, Stadtman ER. Methionine residues as endogenous antioxidants in proteins. Proc Natl Acad Sci USA 1996, 93:15036-15040. 10.1073/pnas.93.26.15036, 26351, 8986759.
53. Levine R, Berlett B, Moskovitz J, Mosoni L, Stadtman ER. Methionine residues may protect proteins from critical oxidative damage. Mechanisms of Ageing and Development 1999, 107:323-332. 10.1016/S0047-6374(98)00152-3, 10360685.
54. Bewley JD, Black M. Seeds: Physiology of development and germination 1994, New York Plenum Press.
55. Kranner I, Birtic S. Modulating Role for Antioxidants in Desiccation Tolerance. Integrative and Comparative Biology 2005, 45:734-740.
56. Bräutigam K, Dietzel L, Kleine T, Ströher E, Wormuth D, Dietz KJ, Radke D, Wirtz M, Hell R, Dörmann P, Nunes-Nesi A, Schauer N, Fernie AR, Oliver SN, Geigenberger P, Leister D, Pfannschmidt T. Dynamic Plastid Redox Signals Integrate Gene Expression and Metabolism to Induce Distinct Metabolic States in Photosynthetic Acclimation in Arabidopsis. Plant Cell 2009, 21:2715-32. 10.1105/tpc.108.062018, 2768923, 19737978.
57. Fey V, Wagner R, Bräutigam K, Wirtz M, Hell R, Dietzmann A, Leister D, Oelmüller R, Pfannschmidt T. Retrograde plastid redox signals in the expression of nuclear genes for chloroplast proteins of Arabidopsis thaliana. J Biol Chem 2005, 280:5318-5328. 10.1074/jbc.M406358200, 15561727.
58. Meyer AJ. The integration of glutathione homeostasis and redox signaling. J Plant Physiol 2008, 165:1390-1403. 10.1016/j.jplph.2007.10.015, 18171593.
59. Schwarzländer M, Fricker MD, Müller C, Marty L, Brach T, Novak J, Sweetlove LJ, Hell R, Meyer AJ. Confocal imaging of glutathione redox potential in living plant cells. J Microsc 2008, 231:299-316. 10.1111/j.1365-2818.2008.02030.x, 18778428.
60. Doyle JL, Doyle JJ. Isolation of plant DNA from fresh tissue. Focus 1990, 12:13-15.
61. Chang S, Puryear J, Cairney J. A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 1993, 11:113-116.
62. Wirtz M, Droux M, Hell R. O-Acetylserine (thiol) lyase: An enigmatic enzyme of plant cysteine biosynthesis revisited in Arabidopsis thaliana. J Exp Bot 2004, 55:1785-1798. 10.1093/jxb/erh201, 15258168.
63. Gallardo K, Le Signor C, Vandekerckhove J, Thompson RD, Burstin J. Proteomics of Medicago truncatula seed development establishes the time frame of diverse metabolic processes related to reserve accumulation. Plant Physiol 2003, 133:664-82. 10.1104/pp.103.025254, 219042, 12972662.
64. Bradford M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254. 10.1016/0003-2697(76)90527-3, 942051.
65. Mathesius U, Keijzers G, Natera SH, Weinman JJ, Djordjevic MA, Rolfe BG. Establishment of a root proteome reference map for the model legume Medicago truncatula using the expressed sequence tag database for peptide mass fingerprinting. Proteomics 2001, 1:1424-1240. 10.1002/1615-9861(200111)1:11<1424::AID-PROT1424>3.0.CO;2-J, 11922602.
66. Gallardo K, Firnhaber C, Zuber H, Héricher D, Belghazi M, Henry C, Küster H, Thompson R. A Combined Proteome and Transcriptome Analysis of Developing Medicago truncatula Seeds: Evidence for Metabolic Specialization of Maternal and Filial Tissues. MCP 2007, 6:2165-2179.