Plastid-cytosol partitioning and integration of metabolic pathways for APS/PAPS biosynthesis in Arabidopsis thaliana

Frontiers in Plant Science

Volumn 5, Issue JAN, 2015, Pages 1-4

  Bohrer, Anne Sophie ^a   Kopriva, Stanislav ^b   Takahashi, Hideki ^a  

^a Michigan State University   (United States)

^b UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Metabolic flux; Metabolite distribution; Subcellular localization; Sulfate assimilation; Sulfur metabolism

Indexed keywords

ARABIDOPSIS THALIANA;

EID: 84922252544     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00751     Document Type: Article

References (34)

1. Bick, J. A., Setterdahl, A. T., Knaff, D. B., Chen, Y., Pitcher, L. H., Zilinskas, B. A., et al. Regulation of the plant-type 5’-adenylyl sulfate reductase by oxidative stress. Biochemistry 40, 9040-9048. doi: 10.1021/bi010518v
2. Bohrer, A.-S., Yoshimoto, N., Sekiguchi, A., Rykulski, N., Saito, K., and Takahashi, H. (2014). Alternative translational initiation of ATP sulfurylase underlying dual localization of sulfate assimilation pathways in plastids and cytosol in Arabidopsis thaliana. Front. PlantSci. 5:750. doi: 10.3389/fpls.2014.00750
3. Bykowski, T., van der Ploeg, J. R., Iwanicka-Nowicka, R., and Hryniewicz, M. M. .The switch from inorganic to organic sulphur assimilation in Escherichia coli: adenosine 5’-phosphosulphate (APS) as a signalling molecule for sulphate excess. Mol. Microbiol. 43, 1347-1358. doi: 10.1046/j.1365-2958.2002.02846.x
4. Chan, K. X., Wirtz, M., Phua, S. Y., Estavillo, G. M., and Pogson, B. J. (2013). Balancing metabolites in drought: the sulfur assimilation conundrum. Trends PlantSci. 18, 18-29. doi: 10.1016/j.tplants.2012.07.005
5. Chao, D.-Y., Baraniecka, P., Danku, J., Koprivova, A., Lahner, B., Luo, H., et al. . Variation in sulfur and selenium accumulation is controlled by naturally occurring isoforms of the key sulfur assimilation enzyme APR2 across the Arabidopsis thaliana species range. Plant Physiol. 166, 1593-608. doi: 10.1104/pp.114.247825
6. Chen, H., Zhang, B., Hicks, L. M., and Xiong, L. (2011). A nucleotide metabolite controls stress-responsive gene expression and plant development. PLoS ONE 6:e26661. doi: 10.1371/journal.pone.0026661
7. Estavillo, G. M., Crisp, P. A., Pornsiriwong, W., Wirtz, M., Collinge, D., Carrie, etal. (2011). Evidence for a SAL1-PAP chloroplast retrograde pathway that functions in drought and high light signaling in Arabidopsis. PlantCell 23, 39924012. doi: 10.1105/tpc.111.091033
8. Gigolashvili, T., Geier, M., Ashykhmina, N., Frerigmann, H., Wulfert, S., Krueger, S., et al. (2012). The Arabidopsis thylakoid ADP/ATP carrier TAAC has an additional role in supplying plastidic phosphoadenosine 5’-phosphosulfate to the cytosol. PlantCell 24,4187-4204. doi: 10.1105/tpc.112.101964
9. Gigolashvili, T., and Kopriva, S. (2014). Transporters in plant sulfur metabolism. Front. PlantSci. 5:442. doi: 10.3389/fpls.2014.00442
10. Gy, I., Gasciolli, V., Lauressergues, D., Morel, J.-B., Gombert, J., Proux, F., et al. (2007). Arabidopsis FIERY1, XRN2, and XRN3 are endogenous RNA silencing suppressors. Plant Cell 19, 3451-3461. doi: 10.1105/tpc.107.055319
11. Herrmann, J., Ravilious, G. E., McKinney, S. E., Westfall, C. S., Lee, S. G., Baraniecka, P., et al. (2014). Structure and mechanism of soybean ATP sulfurylase and the committed step in plant sulfur assimilation. J. Biol. Chem. 289, 10919-10929. doi: 10.1074/jbc.M113.540401
12. Hirai, M. Y., Klein, M., Fujikawa, Y., Yano, M., Goodenowe, D. B., Yamazaki, Y., etal. (2005). Elucidation of gene-to-gene and metabolite-to-gene networks in Arabidopsis by integration of metabolomics and transcriptomics. J. Biol. Chem. 280, 25590-25595. doi: 10.1074/jbc.M502332200
13. Kawashima, C. G., Matthewman, C. A., Huang, S., Lee, B.-R., Yoshimoto, N., Koprivova, A., etal. (2011). Interplay of SLIM1 and miR395 in the regulation of sulfate assimilation in Arabidopsis. Plant J. 66, 863-876. doi: 10.1111/j.1365-313X.2011.04547.x
14. Klein, M., and Papenbrock, J. (2004). The multi-protein family of Arabidopsis sulphotransferases and their relatives in other plant species. J. Exp. Bot. 55, 1809-1820. doi: 10.1093/jxb/erh183
15. Kopriva, S., Mugford, S. G., Baraniecka, P., Lee, B.-R., Matthewman, C. A., and Koprivova, A. (2012). Control of sulfur partitioning between primary and secondary metabolism in Arabidopsis. Front. Plant Sci. 3:163. doi: 10.3389/fpls.2012.00163
16. Koprivova, A., Giovannetti, M., Baraniecka, P., Lee, B.-R., Grondin, C., Loudet, O., etal. (2013). Natural variation in the ATPS1 isoform of ATP sulfurylase contributes to the control of sulfate levels in Arabidopsis. Plant Physiol. 163, 1133-1141. doi: 10.1104/pp.113.225748
17. Koprivova, A., and Kopriva, S. (2014). Molecular mechanisms of regulation of sulfate assimilation: first steps on a long road. Front. Plant Sci. 5:589. doi: 10.3389/fpls.2014.00589
18. Lee, B.-R., Huseby, S., Koprivova, A., Chetelat, A., Wirtz, M., Mugford, S. T., etal. (2012). Effects of fou8/fry1 mutation on sulfur metabolism: is decreased internal sulfate the trigger of sulfate starvation response? PLoS ONE 7:e39425. doi: 10.1371/journal.pone.0039425
19. Loudet, O., Saliba-Colombani, V., Camilleri, C., Calenge, F., Gaudon, V., Koprivova, A., etal. (2007). Natural variation for sulfate content in Arabidopsis thaliana is highly controlled byAPR2. Nat. Genet. 39, 896-900. doi: 10.1038/ng2050
20. Maruyama-Nakashita, A., Nakamura, Y., Tohge, T., Saito, K., and Takahashi, H. (2006). Arabidopsis SLIM1 is a central transcriptional regulator of plant sulfur response and metabolism. Plant Cell 18, 3235-3251. doi: 10.1105/tpc.106.046458
21. Mugford, S. G., Lee, B.-R., Koprivova, A., Matthewman, C., and Kopriva, S. (2011). Control of sulfur partitioning between primary and secondary metabolism. Plant J. 65, 96-105. doi: 10.1111/j.1365-313X.2010.04410.x
22. Mugford, S. G., Yoshimoto, N., Reichelt, M., Wirtz, M., Hill, L., Mugford, S. T., et al. (2009). Disruption of adenosine-5’-phosphosulfate kinase in Arabidopsis reduces levels of sulfated secondary metabolites. Plant Cell 21, 910-927. doi: 10.1105/tpc.109.065581
23. Piotrowski, M., Schemenewitz, A., Lopukhina, A., Muller, A., Janowitz, T., Weiler, W., et al. (2004). Desulfoglucosinolate sulfotransferases from Arabidopsis thaliana catalyze the final step in the biosynthesis of the glucosinolate core structure. J. Biol. Chem. 279, 50717-50725. doi: 10.1074/jbc.M407681200
24. Ravilious, G. E., and Jez, J. M. (2012). Nucleotide binding site communication in Arabidopsis thaliana adenosine 5’-phosphosulfate kinase. J. Biol. Chem. 287, 30385-30394. doi: 10.1074/jbc.M112.387001
25. Ravilious, G. E., Nguyen, A., Francois, J. A., and Jez, J. M. (2012). Structural basis and evolution of redox regulation in plant adenosine-5’-phosphosulfate kinase. Proc:. Natl. Acad. Sci. U.S.A 109, 309-314. doi: 10.1073/pnas.1115772108
26. Ravilious, G. E., Westfall, C. S., and Jez, J. M. (2013). Redox-linked gating of nucleotide binding by the N-terminal domain of adenosine 5’-phosphosulfate kinase. J. Biol. Chem. 288,6107-6115. doi: 10.1074/jbc.M112.439414
27. Rodriguez, V. M., Chetelat, A., Majcherczyk, P., and Farmer, E. E. (2010). Chloro- plastic phosphoadenosine phosphosulfate metabolism regulates basal levels of the prohormone jasmonic acid in Arabidopsis leaves. Plant Physiol. 152, 1335-1345. doi: 10.1104/pp.109.150474
28. Rotte, C., and Leustek, T. (2000). Differential subcellular localization and expression of ATP sulfurylase and 5’-adenylylsulfate reductase during ontogenesis of Ara- bidopsis leaves indicates that cytosolic and plastid forms of ATP sulfurylase may havespecializedfunctions. PlantPhysiol. 124, 715-724. doi: 10.1104/pp.124.2.715
29. 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. doi: 10.1146/annurev-arplant-042110-103921
30. Takahashi, H., Yamazaki, M., Sasakura, N., Watanabe, A., Leustek, T., Engler, J. A., et al. (1997). Regulation of sulfur assimilation in higher plants: a sulfate transporter induced in sulfate-starved roots plays a central role in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 94,11102-11107. doi: 10.1073/pnas.94.20.11102
31. Vauclare, P., Kopriva, S., Fell, D., Suter, M., Sticher, L., von Ballmoos, P., et al. . Fluxcontrol of sulphate assimilationin Arabidopsis thaliana: adenosine 5’- phosphosulphate reductase is more susceptible than ATP sulphurylase to negative controlbythiols. PlantJ. 31,729-740. doi: 10.1046/j.1365-313X.2002.01391.x
32. Wilson, P. B., Estavillo, G. M., Field, K. J., Pornsiriwong, W., Carroll, A. J., Howell, K. A., et al. (2009). The nucleotidase/phosphatase SAL1 is a negative regulator of drought tolerance in Arabidopsis. Plant J. 58, 299-317. doi: 10.1111/j.1365-313X.2008.03780.x
33. Xiong, L., Lee, B., Ishitani, M., Lee, H., Zhang, C., and Zhu, J. K. (2001). FIERY1 encoding an inositol polyphosphate 1-phosphatase is a negative regulator of abscisic acid and stress signaling in Arabidopsis. Genes Dev. 15, 1971-1984. doi: 10.1101/gad.891901
34. Xu, J., Yang, J., Wu, Z., Liu, H., Huang, F., Wu, Y., et al. (2013). Identification of a dual-targeted protein belonging to the mitochondrial carrier family that is required for early leaf development in rice. Plant Physiol. 161, 2036-2048. doi: 10.1104/pp.112.210831