The Arabidopsis thylakoid ADP/ATP Carrier TAAC Has an additional role in supplying plastidic phosphoadenosine 5'-phosphosulfate to the cytosol

Plant Cell

Volumn 24, Issue 10, 2012, Pages 4187-4204

  Gigolashvili, Tamara ^a   Geier, Melanie ^b   Ashykhmina, Natallia ^a   Frerigmann, Henning ^a   Wulfert, Sabine ^a   Krueger, Stephan ^a   Mugfor, Sarah G ^c   Kopriv, Stanislav ^c   Haferkamp, Ilka ^b   Flügge, Ulf Ingo ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b University of Koblenz Landau   (Germany)

^c JOHN INNES CENTRE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84870684024     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.112.101964     Document Type: Article

References (85)

1. Andrès, C., Agne, B., and Kessler, F. (2010). The TOC complex: Preprotein gateway to the chloroplast. Biochim. Biophys. Acta 1803: 715-723.
2. Bak, S., Tax, F.E., Feldmann, K.A., Galbraith, D.W., and Feyereisen, R. (2001). CYP83B1, a cytochrome P450 at the metabolic branch point in auxin and indole glucosinolate biosynthesis in Arabidopsis. Plant Cell 13: 101-111.
3. Benderoth, M., Pfalz, M., and Kroymann, J. (2009). Methylthioalkylmalate synthases: Genetics, ecology and evolution. Phytochem. Rev. 8: 255-268.
4. Bedhomme, M., Hoffmann, M., McCarthy, E.A., Gambonnet, B., Moran, R.G., Rébeillé, F., and Ravanel, S. (2005). Folate metabolism in plants: An Arabidopsis homolog of the mammalian mitochondrial folate transportermediates folate import into chloroplasts. J. Biol. Chem. 280: 34823-34831.
5. Berger, B., Stracke, R., Yatusevich, R., Weisshaar, B., Flügge, U.I., and Gigolashvili, T. (2007). A simplified method for the analysis of transcription factor-promoter interactions that allows highthroughput data generation. Plant J. 50: 911-916.
6. Bernhardt, K., Wilkinson, S., Weber, A.P.M., and Linka, N. (2012). A peroxisomal carrier delivers NAD and contributes to optimal fatty acid degradation during storage oil mobilization. Plant J. 69: 1-13.
7. Bhattacharya, R., Townley, R.A., Berry, K.L., and Bülow, H.E. (2009). The PAPS transporter PST-1 is required for heparan sulfation and is essential for viability and neural development in C. elegans. J. Cell Sci. 122: 4492-4504.
8. Bishop, J.R., Schuksz, M., and Esko, J.D. (2007). Heparan sulphate proteoglycans fine-tune mammalian physiology. Nature 446: 1030-1037.
9. Bouvier, F., Linka, N., Isner, J.-C., Mutterer, J., Weber, A.P.M., and Camara, B. (2006). Arabidopsis SAMT1 defines a plastid transporter regulating plastid biogenesis and plant development. Plant Cell 18: 3088-3105.
10. Brink, S., Bogsch, E.G., Edwards, W.R., Hynds, P.J., and Robinson, C. (1998). Targeting of thylakoid proteins by the delta pH-driven twin-arginine translocation pathway requires a specific signal in the hydrophobic domain in conjunction with the twin-arginine motif. FEBS Lett. 434: 425-430.
11. Clément, A., Wiweger, M., von der Hardt, S., Rusch, M.A., Selleck, S.B., Chien, C.-B., and Roehl, H.H. (2008). Regulation of zebrafish skeletogenesis by ext2/dackel and papst1/pinscher. PLoS Genet. 4: e1000136.
12. Cline, K., and Dabney-Smith, C. (2008). Plastid protein import and sorting: Different paths to the same compartments. Curr. Opin. Plant Biol. 11: 585-592.
13. Davidian, J.-C., and Kopriva, S. (2010). Regulation of sulfate uptake and assimilation-The same or not the same? Mol. Plant 3: 314-325.
14. Estavillo, G.M., et al. (2011). Evidence for a SAL1-PAP chloroplast retrograde pathway that functions in drought and high light signaling in Arabidopsis. Plant Cell 23: 3992-4012.
15. Faiyaz ul Haque, M., King, L.M., Krakow, D., Cantor, R.M., Rusiniak, M.E., Swank, R.T., Superti-Furga, A., Haque, S., Abbas, H., Ahmad, W., Ahmad, M., and Cohn, D.H. (1998). Mutations in orthologous genes in human spondyloepimetaphyseal dysplasia and the brachymorphic mouse. Nat. Genet. 20: 157-162.
16. Ferro, M., Salvi, D., Brugière, S., Miras, S., Kowalski, S., Louwagie, M., Garin, J., Joyard, J., and Rolland, N. (2003). Proteomics of the chloroplast envelope membranes from Arabidopsis thaliana. Mol. Cell. Proteomics 2: 325-345.
17. Fiermonte, G., Paradies, E., Todisco, S., Marobbio, C.M.T., and Palmieri, F. (2009). A novel member of solute carrier family 25 (SLC25A42) is a transporter of coenzyme A and adenosine 39,59-diphosphate in human mitochondria. J. Biol. Chem. 284: 18152-18159.
18. Fischer, K., Arbinger, B., Kammerer, B., Busch, C., Brink, S., Wallmeier, H., Sauer, N., Eckerskorn, C., and Flügge, U.I. (1994). Cloning and in vivo expression of functional triose phosphate/ phosphate translocators from C3-and C4-plants: Evidence for the putative participation of specific amino acid residues in the recognition of phosphoenolpyruvate. Plant J. 5: 215-226.
19. Froehlich, J.E., and Keegstra, K. (2011). The role of the transmembrane domain in determining the targeting of membrane proteins to either the inner envelope or thylakoid membrane. Plant J. 68: 844-856.
20. Gigolashvili, T., Berger, B., and Flügge, U.I. (2009a). Specific and coordinated control of indolic and aliphatic glucosinolate biosynthesis by R2R3-MYB transcription factors in Arabidopsis thaliana. Phytochem. Rev. 8: 3-13.
21. Gigolashvili, T., Berger, B., Mock, H.-P., Müller, C., Weisshaar, B., and Flügge, U.I. (2007b). The transcription factor HIG1/MYB51 regulates indolic glucosinolate biosynthesis in Arabidopsis thaliana. Plant J. 50: 886-901.
22. Gigolashvili, T., Yatusevich, R., Berger, B., Müller, C., and Flügge, U.I. (2007a). The R2R3-MYB transcription factor HAG1/MYB28 is a regulator of methionine-derived glucosinolate biosynthesis in Arabidopsis thaliana. Plant J. 51: 247-261.
23. Gigolashvili, T., Yatusevich, R., Rollwitz, I., Humphry, M., Gershenzon, J., and Flügge, U.I. (2009b). The plastidic bile acid transporter 5 is required for the biosynthesis of methionine-derived glucosinolates in Arabidopsis thaliana. Plant Cell 21: 1813-1829.
24. Haferkamp, I., and Schmitz-Esser, S. (2012). The plant mitochondrial carrier family: Functional and evolutionary aspects. Front Plant Sci. 3: 2.
25. Heazlewood, J.L., and Millar, A.H. (2003). Integrated plant proteomics-Putting the green genomes to work. Funct. Plant Biol. 30: 471-482.
26. Heimpel, S., Basset, G., Odoy, S., and Klingenberg, M. (2001). Expression of the mitochondrial ADP/ATP carrier in Escherichia coli. Renaturation, reconstitution, and the effect of mutations on 10 positive residues. J. Biol. Chem. 276: 11499-11506.
27. Kamiyama, S., Sasaki, N., Goda, E., Ui-Tei, K., Saigo, K., Narimatsu, H., Jigami, Y., Kannagi, R., Irimura, T., and Nishihara, S. (2006). Molecular cloning and characterization of a novel 39-phosphoadenosine 59-phosphosulfate transporter, PAPST2. J. Biol. Chem. 281: 10945-10953.
28. Kamiyama, S., Suda, T., Ueda, R., Yoshida, H., Kikuchi, N., Chiba, Y., Goto, S., Toyoda, H., Narimatsu, H., Jigami, Y., and Nishihara, S. (2003). Molecular cloning and identification of 39-phosphoadenosine 59-phosphosulfate transporter. J. Biol. Chem. 278: 25958-25963.
29. Kirchberger, S., Tjaden, J., and Neuhaus, H.E. (2008). Characterization of the Arabidopsis Brittle1 transport protein and impact of reduced activity on plant metabolism. Plant J. 56: 51-63.
30. Kleffmann, T., Russenberger, D., von Zychlinski, A., Christopher, W., Sjölander, K., Gruissem, W., and Baginsky, S. (2004). The Arabidopsis thaliana chloroplast proteome reveals pathway abundance and novel protein functions. Curr. Biol. 14: 354-362.
31. Kliebenstein, D.J., Kroymann, J., Brown, P., Figuth, A., Pedersen, D., Gershenzon, J., and Mitchell-Olds, T. (2001). Genetic control of natural variation in Arabidopsis glucosinolate accumulation. Plant Physiol. 126: 811-825.
32. Knappe, S., Flügge, U.I., and Fischer, K. (2003). Analysis of the plastidic phosphate translocator gene family in Arabidopsis and identification of new phosphate translocator-homologous transporters, classified by their putative substrate-binding site. Plant Physiol. 131: 1178-1190.
33. Komori, R., Amano, Y., Ogawa-Ohnishi, M., and Matsubayashi, Y. (2009). Identification of tyrosylprotein sulfotransferase in Arabidopsis. Proc. Natl. Acad. Sci. USA 106: 15067-15072.
34. Kopriva, S., Mugford, S.G., Matthewman, C., and Koprivova, A. (2009). Plant sulfate assimilation genes: Redundancy versus specialization. Plant Cell Rep. 28: 1769-1780.
35. Koroleva, O.A., Tomlinson, M.L., Leader, D., Shaw, P., and Doonan, J.H. (2005). High-throughput protein localization in Arabidopsis using Agrobacterium-mediated transient expression of GFP-ORF fusions. Plant J. 41: 162-174.
36. Kroymann, J., Donnerhacke, S., Schnabelrauch, D., and Mitchell-Olds, T. (2003). Evolutionary dynamics of an Arabidopsis insect resistance quantitative trait locus. Proc. Natl. Acad. Sci. USA 100 (suppl. 2): 14587-14592.
37. Kroymann, J., Textor, S., Tokuhisa, J.G., Falk, K.L., Bartram, S., Gershenzon, J., and Mitchell-Olds, T. (2001). A gene controlling variation in Arabidopsis glucosinolate composition is part of the methionine chain elongation pathway. Plant Physiol. 127: 1077-1088.
38. Kurima, K., Warman, M.L., Krishnan, S., Domowicz, M., Krueger, R.C., JrDeyrup, A., and Schwartz, N.B. (1998). A member of a family of sulfate-activating enzymes causes murine brachymorphism. Proc. Natl. Acad. Sci. USA 95: 8681-8685.
39. Kutschmar, A., Rzewuski, G., Stührwohldt, N., Beemster, G.T.S., Inzé, D., and Sauter, M. (2009). PSK-a promotes root growth in Arabidopsis. New Phytol. 181: 820-831.
40. Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
41. Lee, B.-R., et al. (2012). Effects of fou8/fry1 mutation on sulfur metabolism: Is decreased internal sulfate the trigger of sulfate starvation response? PLoS ONE 7: e39425.
42. Leroch, M., Neuhaus, H.E., Kirchberger, S., Zimmermann, S., Melzer, M., Gerhold, J., and Tjaden, J. (2008). Identification of a novel adenine nucleotide transporter in the endoplasmic reticulum of Arabidopsis. Plant Cell 20: 438-451.
43. Li, H.M., and Chiu, C.-C. (2010). Protein transport into chloroplasts. Annu. Rev. Plant Biol. 61: 157-180.
44. Linka, N., Theodoulou, F.L., Haslam, R.P., Linka, M., Napier, J.A., Neuhaus, H.E., and Weber, A.P.M. (2008). Peroxisomal ATP import is essential for seedling development in Arabidopsis thaliana. Plant Cell 20: 3241-3257.
45. Lüders, F., Segawa, H., Stein, D., Selva, E.M., Perrimon, N., Turco, S.J., and Häcker, U. (2003). Slalom encodes an adenosine 39-phosphate 59-phosphosulfate transporter essential for development in Drosophila. EMBO J. 22: 3635-3644.
46. Malitsky, S., Blum, E., Less, H., Venger, I., Elbaz, M., Morin, S., Eshed, Y., and Aharoni, A. (2008). The transcript and metabolite networks affected by the two clades of Arabidopsis glucosinolate biosynthesis regulators. Plant Physiol. 148: 2021-2049.
47. Matsubayashi, Y., Ogawa, M., Kihara, H., Niwa, M., and Sakagami, Y. (2006). Disruption and overexpression of Arabidopsis phytosulfokine receptor gene affects cellular longevity and potential for growth. Plant Physiol. 142: 45-53.
48. Matsuzaki, Y., Ogawa-Ohnishi, M., Mori, A., and Matsubayashi, Y. (2010). Secreted peptide signals required for maintenance of root stem cell niche in Arabidopsis. Science 329: 1065-1067.
49. Mikkelsen, M.D., Hansen, C.H., Wittstock, U., and Halkier, B.A. (2000). Cytochrome P450 CYP79B2 from Arabidopsis catalyzes the conversion of tryptophan to indole-3-acetaldoxime, a precursor of indole glucosinolates and indole-3-acetic acid. J. Biol. Chem. 275: 33712-33717.
50. Mikkelsen, M.D., Naur, P., and Halkier, B.A. (2004). Arabidopsis mutants in the C-S lyase of glucosinolate biosynthesis establish a critical role for indole-3-acetaldoxime in auxin homeostasis. Plant J. 37: 770-777.
51. Millar, A.H., and Heazlewood, J.L. (2003). Genomic and proteomic analysis of mitochondrial carrier proteins in Arabidopsis. Plant Physiol. 131: 443-453.
52. Moore, K.L. (2003). The biology and enzymology of protein tyrosine O-sulfation. J. Biol. Chem. 278: 24243-24246.
53. Mugford, S.G., Matthewman, C.A., Hill, L., and Kopriva, S. (2010). Adenosine-59-phosphosulfate kinase is essential for Arabidopsis viability. FEBS Lett. 584: 119-123.
54. Mugford, S.G., et al. (2009). Disruption of adenosine-59-phosphosulfate kinase in Arabidopsis reduces levels of sulfated secondary metabolites. Plant Cell 21: 910-927.
55. Naur, P., Petersen, B.L., Mikkelsen, M.D., Bak, S., Rasmussen, H., Olsen, C.E., and Halkier, B.A. (2003). CYP83A1 and CYP83B1, two nonredundant cytochrome P450 enzymes metabolizing oximes in the biosynthesis of glucosinolates in Arabidopsis. Plant Physiol 133: 63-72.
56. Neuhaus, H.E., Thom, E., Möhlmann, T., Steup, M., and Kampfenkel, K. (1997). Characterization of a novel eukaryotic ATP/ ADP translocator located in the plastid envelope of Arabidopsis thaliana L. Plant J. 11: 73-82.
57. Palmieri, F., Pierri, C.L., De Grassi, A., Nunes-Nesi, A., and Fernie, A.R. (2011). Evolution, structure and function of mitochondrial carriers: A review with new insights. Plant J. 66: 161-181.
58. Palmieri, F., et al. (2009). Molecular identification and functional characterization of Arabidopsis thaliana mitochondrial and chloroplastic NAD+ carrier proteins. J. Biol. Chem. 284: 31249-31259.
59. Palmieri, L., Santoro, A., Carrari, F., Blanco, E., Nunes-Nesi, A., Arrigoni, R., Genchi, F., Fernie, A.R., and Palmieri, F. (2008). Identification and characterization of ADNT1, a novel mitochondrial adenine nucleotide transporter from Arabidopsis. Plant Physiol. 148: 1797-1808.
60. Patron, N.J., Durnford, D.G., and Kopriva, S. (2008). Sulfate assimilation in eukaryotes: Fusions, relocations and lateral transfers. BMC Evol. Biol. 8: 39.
61. Reinhold, T., Alawady, A., Grimm, B., Beran, K.C., Jahns, P., Conrath, U., Bauer, J., Reiser, J., Melzer, M., Jeblick, W., and Neuhaus, H.E. (2007). Limitation of nocturnal import of ATP into Arabidopsis chloroplasts leads to photooxidative damage. Plant J. 50: 293-304.
62. Reiser, J., Linka, N., Lemke, L., Jeblick, W., and Neuhaus, H.E. (2004). Molecular physiological analysis of the two plastidic ATP/ ADP transporters from Arabidopsis. Plant Physiol. 136: 3524-3536.
63. Rieder, B., and Neuhaus, H.E. (2011). Identification of an Arabidopsis plasma membrane-located ATP transporter important for anther development. Plant Cell 23: 1932-1944.
64. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
65. Schünemann, D. (2007). Mechanisms of protein import into thylakoids of chloroplasts. Biol. Chem. 388: 907-915.
66. Schuster, J., Knill, T., Reichelt, M., Gershenzon, J., and Binder, S. (2006). Branched-chain aminotransferase4 is part of the chain elongation pathway in the biosynthesis of methionine-derived glucosinolates in Arabidopsis. Plant Cell 18: 2664-2679.
67. Schwacke, R., Schneider, A., van der Graaff, E., Fischer, K., Catoni, E., Desimone, M., Frommer, W.B., Flügge, U.I., and Kunze, R. (2003). ARAMEMNON, a novel database for Arabidopsis integral membrane proteins. Plant Physiol. 131: 16-26.
68. Shroff, R., Vergara, F., Muck, A., Svatos, A., and Gershenzon, J. (2008). Nonuniform distribution of glucosinolates in Arabidopsis thaliana leaves has important consequences for plant defense. Proc. Natl. Acad. Sci. USA 105: 6196-6201.
69. Sønderby, I.E., Burow, M., Rowe, H.C., Kliebenstein, D.J., and Halkier, B.A. (2010a). A complex interplay of three R2R3 MYB transcription factors determines the profile of aliphatic glucosinolates in Arabidopsis. Plant Physiol. 153: 348-363.
70. Sønderby, I.E., Geu-Flores, F., and Halkier, B.A. (2010b). Biosynthesis of glucosinolates-Gene discovery and beyond. Trends Plant Sci. 15: 283-290.
71. Sønderby, I.E., Hansen, B.G., Bjarnholt, N., Ticconi, C., Halkier, B.A., Kliebenstein, D.J. (2007). A systems biology approach identifies a R2R3 MYB gene subfamily with distinct and overlapping functions in regulation of aliphatic glucosinolates. PLoS One 2: e1322.
72. Strittmatter, P., Soll, J., and Bölter, B. (2010). The chloroplast protein import machinery: A review. Methods Mol. Biol. 619: 307-321.
73. Strott, C.A. (2002). Sulfonation and molecular action. Endocr. Rev. 23: 703-732.
74. Stührwohldt, N., Dahlke, R.I., Steffens, B., Johnson, A., and Sauter, M. (2011). Phytosulfokine-a controls hypocotyl length and cell expansion in Arabidopsis thaliana through phytosulfokine receptor 1. PLoS ONE 6: e21054.
75. Takahashi, H., Kopriva, S., Giordano, M., Saito, K., and Hell, R. (2011). Sulfur assimilation in photosynthetic organisms: Molecular functions and regulations of transporters and assimilatory enzymes. Annu. Rev. Plant Biol. 62: 157-184.
76. Thomas, D., and Surdin-Kerjan, Y. (1997). Metabolism of sulfur amino acids in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 61: 503-532.
77. Thuswaldner, S., Lagerstedt, J.O., Rojas-Stütz, M., Bouhidel, K., Der, C., Leborgne-Castel, N., Mishra, A., Marty, F., Schoefs, B., Adamska, I., Persson, B.L., and Spetea, C. (2007). Identification, expression, and functional analyses of a thylakoid ATP/ADP carrier from Arabidopsis. J. Biol. Chem. 282: 8848-8859.
78. van der Fits, L., Deakin, E.A., Hoge, J.H.C., and Memelink, J. (2000). The ternary transformation system: constitutive virG on a compatible plasmid dramatically increases Agrobacterium-mediated plant transformation. Plant Mol. Biol. 43: 495-502.
79. Voinnet, O., Rivas, S., Mestre, P., and Baulcombe, D. (2003). An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J. 33: 949-956.
80. Wirtz, M., and Hell, R. (2003). Production of cysteine for bacterial and plant biotechnology: Application of cysteine feedback-insensitive isoforms of serine acetyltransferase. Amino Acids 24: 195-203.
81. Yang, H.P., Matsubayashi, Y., Nakamura, K., and Sakagami, Y. (1999). Oryza sativa PSK gene encodes a precursor of phytosulfokine-alpha, a sulfated peptide growth factor found in plants. Proc. Natl. Acad. Sci. USA 96: 13560-13565.
82. Yang, H.P., Matsubayashi, Y., Nakamura, K., and Sakagami, Y. (2001). Diversity of Arabidopsis genes encoding precursors for phytosulfokine, a peptide growth factor. Plant Physiol. 127: 842-851.
83. Yin, L., Lundin, B., Bertrand, M., Nurmi, M., Solymosi, K., Kangasjärvi, S., Aro, E.-M., Schoefs, B., and Spetea, C. (2010). Role of thylakoid ATP/ADP carrier in photoinhibition and photoprotection of photosystem II in Arabidopsis. Plant Physiol. 153: 666-677.
84. Yoo, S.D., Cho, Y.H., and Sheen, J. (2007). Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat. Protoc. 2: 1565-1572.
85. Zhou, W., Wei, L., Xu, J., Zhai, Q., Jiang, H., Chen, R., Chen, Q., Sun, J., Chu, J., Zhu, L., Liu, C.-M., and Li, C. (2010). Arabidopsis tyrosylprotein sulfotransferase acts in the auxin/PLETHORA pathway in regulating postembryonic maintenance of the root stem cell niche. Plant Cell 22: 3692-3709.