Molecular mechanisms of regulation of sulfate assimilation: First steps on a long road

Frontiers in Plant Science

Volumn 5, Issue October, 2014, Pages

  Koprivova, Anna ^a   Kopriva, Stanislav ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Adenosine 5 phosphosulfate; Glutathione; MicroRNA; Sulfate assimilation; Sulfate uptake; Transcription factors; Transcriptional regulation

Indexed keywords

EID: 84908370402     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00589     Document Type: Review

References (118)

1. Allen, E., Xie, Z., Gustafson, A.M., and Carrington J. C. (2005). MicroRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121, 207-221. doi: 10.1016/j.cell.2005.04.004.
2. Aubry, S., Smith-Unna, R. D., Boursnell, C. M., Kopriva, S., and Hibberd, J. M. (2014). Transcript residency on ribosomes reveals a key role for the Arabidopsis thaliana bundle sheath in sulfur and glucosinolate metabolism. Plant J. 78,659-673. doi: 10.1111/tpj.12502.
3. Awazuhara, M., Kim, H., Goto, D. B., Matsui, A., Hayashi, H., Chino, M., etal. (2002).A235-bp region from a nutritionallyregulated soybean seed-specific gene promoter can confer its sulfur and nitrogen response to a constitutive promoter in aerial tissues of Arabidopsis thaliana. PlantSci. 163, 75-82. doi: 10.1016/S0168-9452(02)00064-X
4. Ball, L., Accotto, G. P., Bechtold, U., Creissen, G., Funck, D., Jimenez, A., et al. (2004). Evidence for a direct link between glutathione biosynthesis and stress defense gene expression in Arabidopsis. Plant Cell 16, 2448-2462. doi: 10.1105/tpc.104.022608.
5. Baxter, I., Brazelton, J. N., Yu, D., Huang, Y. S., Lahner, B., Yakubova, E., etal. (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. doi: 10.1371/journal.pgen.1001193.
6. Berkowitz, O., Wirtz, M., Wolf, A., Kuhlmann, J., and Hell, R. (2002). Use of biomolecular interaction analysis to elucidate the regulatory mechanism of the cysteine synthase complex from Arabidopsis thaliana. J. Biol. Chem. 277, 30629-30634. doi: 10.1074/jbc.M111632200.
7. Bick, J. A., Setterdahl, A. T., Knaff, D. B., Chen, Y., Pitcher, L. H., Zilinskas, B. A., etal. (2001). Regulation of the plant-type 5;-adenylyl sulfate reductase by oxidative stress. Biochemistry 40, 9040-9048. doi: 10.1021/bi010518v
8. Bidart-Bouzat, M. G., and Kliebenstein, D. J. (2008). Differential levels of insect herbivory in the field associated with genotypic variation in glucosinolates in Arabidopsis thaliana. J. Chem. Ecol. 34, 1026-1037. doi: 10.1007/s10886-008-9498-z
9. Brunold, C. (1978). Regulation of sulfate assimilation in plants: 7. Cysteine inactivation of adenosine 5;-phosphosulfate sulfotransferase in Lemna minor L. Plant Physiol. 61,342-347. doi: 10.1104/pp.61.3.342.
10. Buhtz, A., Pieritz, J., Springer, F., and Kehr, J. (2010). Phloem small RNAs, nutrient stress responses,andsystemicmobility. BMCPlantBiol 10:64. doi: 10.1186/1471-2229-10-64.
11. Calderwood, A., and Kopriva, S. (2014). Hydrogen sulfide in plants: from dis¬sipation of excess sulfur to signaling molecule. Nitric Oxide 41C, 72-78. doi: 10.1016/j.niox.2014.02.005.
12. Cao, M. J., Wang, Z., Wirtz, M., Hell, R., Oliver, D. J., and Xiang, C. B. (2013). SULTR3;1 is a chloroplast-localized sulfate transporter in Arabidopsis thaliana. Plant J. 73, 607-616. doi: 10.1111/tpj.12059.
13. Chan, E. K., Rowe, H. C., Corwin, J. A., Joseph, B., and Klieben- stein, D. J. (2011). Combining genome-wide association mapping and transcriptional networks to identify novel genes controlling glucosinolates in Arabidopsis thaliana. PLoS Biol. 9:e1001125. doi: 10.1371/journal.pbio.1001125.
14. Chao, D. Y., Baraniecka, P., Danku, J., Koprivova, A., Lahner, B., Luo, H., et al. (2014). Variation in sulfur and selenium accumulation is controlled by naturally occurring isoforms of the key sulfur assimilation enzyme APR2 across the Arabidopsis thaliana speciesrange. PlantPhysiol. doi: 10.1104/pp.114.247825 [Epub ahead of print].
15. Chao, D. Y., Silva, A., Baxter, I., Huang, Y. S., Nordborg, M., Danku, J., etal. (2012). Genome-wide association studies identify heavy metal ATPase3 as the primary determinant of natural variation in leaf cadmium in Arabidopsis thaliana. PLoS Genet. 8:e1002923. doi: 10.1371/journal.pgen.1002923.
16. Chattopadhyay, S., Ang, L. H., Puente, P., Deng, X. W., and Wei, N. (1998). Arabidopsis bZIP protein HY5 directly interacts with light-responsive promoters in mediating light control of gene expression. Plant Cell 10, 673-683. doi: 10.1105/tpc.10.5.673.
17. Conaway, R. C., and Conaway, J.W. (2011). Function andregulation of the mediator complex. Curr. Opin. Genet. Dev. 21, 225-230. doi: 10.1016/j.gde.2011.01.013.
18. Davies, J. P., Yildiz, F. H., and Grossman, A. (1996). Sac1, a putative regulator that is critical for survival of Chlamydomonas reinhardtii during sulfur deprivation. EMBOJ. 15,2150-2159.
19. Dominguez-Solis, J. R., He, Z., Lima, A., Ting, J., Buchanan, B. B., and Luan, S. (2008). A cyclophilin links redox and light signals to cysteine biosynthesis and stress responses in chloroplasts. Proc. Natl. Acad. Sci. U.S.A. 105, 16386-16391. doi: 10.1073/pnas.0808204105.
20. Dooley, F. D., Nair, S. P., andWard, P. D. (2013). Increased growth and germination success in plants following hydrogen sulfide administration. PLoS ONE 8:e62048. doi: 10.1371/journal.pone.0062048.
21. Droux, M., Ruffet, M. L., Douce, R., and Job, D. (1998). Interactions between serine acetyltransferase and O-acetylserine (thiol) lyase in higher plants - structural and kinetic properties of the free and bound enzymes. Eur. J. Biochem. 255, 235-245. doi: 10.1046/j.1432-1327.1998.2550235.x
22. Elfving, N., Davoine, C., Benlloch, R., Blomberg, J., Brannstrom, K., Muller, D., et al. (2011). The Arabidopsis thaliana Med25 mediator subunit integrates environmental cues to control plant development. Proc. Natl. Acad. Sci. U.S.A. 108, 8245-8250. doi: 10.1073/pnas.1002981108.
23. Falkenberg, B., Witt, I., Zanor, M. I., Steinhauser, D., Mueller-Roeber, B., Hesse, H., etal. (2008). Transcription factors relevant to auxin signalling coordinate broad-spectrum metabolic shifts including sulphur metabolism. J. Exp. Bot. 59, 2831-2846. doi: 10.1093/jxb/ern144.
24. Farago, S., and Brunold, C. (1990). Regulation of assimilatory sulfate reduc¬tion by herbicide safeners in Zea mays L. Plant Physiol. 94, 1808-1812. doi: 10.1104/pp.94.4.1808.
25. Francois, J. A., Kumaran, S., and Jez, J. M. (2006). Structural basis for interaction of O-acetylserine sulfhydrylase and serine acetyltransferase in the Arabidopsis cysteinesynthasecomplex. PlantCell 18,3647-3655. doi: 10.1105/tpc.106.047316.
26. Garcia-Mata, C., and Lamattina, L. (2013). Gasotransmitters are emerging as new guard cell signaling molecules and regulators of leaf gas exchange. Plant Sci. 201-202, 66-73. doi: 10.1016/j.plantsci.2012.11.007.
27. Gigolashvili, T., Berger, B., Mock, H. P., Muller, C., Weisshaar, B., and Flugge, U. I. (2007a). The transcription factor HIG1/MYB51 regulates indolic glucosinolate biosynthesis in Arabidopsis thaliana. Plant J. 50, 886-901. doi: 10.1111/j.1365-313X.2007.03099.x
28. Gigolashvili, T., Yatusevich, R., Berger, B., Muller, C., and Flugge, U. I. (2007b). The R2R3-MYB transcription factor HAG1/MYB28 is a regulator of methionine- derived glucosinolate biosynthesis in Arabidopsis thaliana. Plant J. 51, 247-261. doi: 10.1111/j.1365-313X.2007.03133.x
29. Gigolashvili, T., Engqvist, M., Yatusevich, R., Muller, C., and Flugge, U. I. (2008). HAG2/MYB76 and HAG3/MYB29 exert a specific and coordinated control on the regulation of aliphatic glucosinolate biosynthesis in Arabidopsis thaliana. New Phytol. 177, 627-642. doi: 10.1111/j.1469-8137.2007.02295.x
30. Grant, K., Carey, N. M., Mendoza, M., Schulze, J., Pilon, M., Pilon-Smits, E. A., et al. (2011). Adenosine 5;-phosphosulfate reductase (APR2) mutation in Arabidopsis implicates glutathione deficiency in selenate toxicity. Biochem. J. 438, 325-335. doi: 10.1042/BJ20110025.
31. Haas, F. H., Heeg, C., Queiroz, R., Bauer, A., Wirtz, M., and Hell, R. (2008). Mitochondrial serine acetyltransferase functions as a pacemaker of cysteine synthesis in plant cells. PlantPhysiol. 148, 1055-1067. doi: 10.1104/pp.108.125237.
32. Harper, A. L., Trick, M., Higgins, J., Fraser, F., Clissold, L., Wells, R., etal. (2012). Associative transcriptomics of traits in the polyploid crop species Brassica napus. Nat. Biotechnol. 30, 798-802. doi: 10.1038/nbt.2302.
33. Hartmann, T., Honicke, P., Wirtz, M., Hell, R., Rennenberg, H., and Kopriva, S. (2004). Regulation of sulphate assimilation by glutathione in poplars (Popu- lus tremula x P.alba) of wild type and overexpressing gamma-glutamylcysteine synthetase in the cytosol. J. Exp. Bot. 55, 837-845. doi: 10.1093/Jxb/Erh094.
34. Heeg, C., Kruse, C., Jost, R., Gutensohn, M., Ruppert, T., Wirtz, M., etal. (2008). Analysis of the Arabidopsis O-acetylserine(thiol)lyase gene family demonstrates compartment-specific differences in the regulation of cysteine synthesis. Plant Cell 20, 168-185. doi: 10.1105/tpc.107.056747.
35. Hell, R., and Bergmann, L. (1990). Gamma-glutamylcysteine synthetase in higher-plants- catalytic properties and subcellular-localization. Planta 180, 603-612. doi: 10.1007/BF02411460.
36. Hell, R., Jost, R., Berkowitz, O., and Wirtz, M. (2002). Molecular and biochemical analysis of the enzymes of cysteine biosynthesis in the plant Arabidopsis thaliana. Amino Acids 22, 245-257. doi: 10.1007/s007260200012.
37. 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.
38. Hesse, H., Trachsel, N., Suter, M., Kopriva, S., Von Ballmoos, P., Rennenberg, H., etal. (2003). Effect of glucose on assimilatory sulphate reduction in Arabidopsis thaliana roots. J. Exp. Bot. 54, 1701-1709. doi: 10.1093/Jxb/Erg177.
39. Hirai, M. Y., Fujiwara, T., Awazuhara, M., Kimura, T., Noji, M., and Saito, K. (2003). Global expression profiling of sulfur-starved Arabidopsis by DNA macroarray reveals the role of O-acetyl-l-serine as a general regulator of gene expression in response to sulfur nutrition. Plant J. 33, 651-663. doi: 10.1046/j.1365-313X.2003.01658.x
40. Hirai, M. Y., Sugiyama, K., Sawada, Y., Tohge, T., Obayashi, T., Suzuki, A., etal. (2007). Omics-based identification of Arabidopsis Myb transcription factors regulating aliphatic glucosinolate biosynthesis. Proc. Natl. Acad. Sci. U.S.A. 104, 6478-6483. doi: 10.1073/pnas.0611629104.
41. Ho, C. H., Lin, S. H., Hu, H. C., and Tsay, Y. F. (2009). CHL1 functions as a nitrate sensor in plants. Cell 138, 1184-1194. doi: 10.1016/j.cell.2009.07.004.
42. Hopkins, L., Parmar, S., Blaszczyk, A., Hesse, H., Hoefgen, R., and Hawkesford, M. J. (2005). O-acetylserine and the regulation of expression of genes encoding components for sulfate uptake and assimilation in potato. Plant Physiol. 138, 433-440. doi: 10.1104/pp.104.057521.
43. Hothorn, M., Wachter, A., Gromes, R., Stuwe, T., Rausch, T., and Scheffzek, K. (2006). Structural basis for the redox control of plant glutamate cysteine ligase. J. Biol. Chem. 281,27557-27565.doi: 10.1074/jbc.M602770200.
44. Hubberten, H. M., Klie, S., Caldana, C., Degenkolbe, T., Willmitzer, L., and Hoef- gen, R. (2012). Additional role of O-acetylserine as a sulfur status-independent regulator during plant growth. Plant J. 70, 666-677. doi: 10.1111/j.1365-313X.2012.04905.x
45. Inigo, S., Alvarez, M. J., Strasser, B., Califano, A., and Cerdan, P. D. (2012). PFT1, the MED25 subunit of the plant mediator complex, promotes flowering through CONSTANS dependent and independent mechanisms in Arabidopsis. Plant J. 69, 601-612. doi: 10.1111/j.1365-313X.2011.04815.x
46. Jez, J. M., Cahoon, R. E., and Chen, S. (2004). Arabidopsis thaliana glutamate- cysteine ligase: functional properties, kinetic mechanism, and regulation of activity. J. Biol. Chem. 279, 33463-33470. doi: 10.1074/jbc.M405127200.
47. Jones-Rhoades, M. W., and Bartel, D. P. (2004). Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol. Cell. 14, 787-799. doi: 10.1016/j.molcel.2004.05.027.
48. Jost, R., Altschmied, L., Bloem, E., Bogs, J., Gershenzon, J., Hahnel, U., etal. (2005). Expression profiling of metabolic genes in response to methyljasmonate reveals regulation of genes of primary and secondary sulfur-related pathways in Arabidopsis thaliana. Photosyn. Res. 86, 491-508. doi: 10.1007/s11120-005-7386-7388.
49. Kasajima, I., Ohkama-Ohtsu, N., Yoko Ide, Y., Hayashi, H., Yoneyama, T., Suzuki, Y., et al. (2007). The BIG gene is involvedin regulation of sulfur deficiency-responsive genes in Arabidopsis thaliana. Physiol. Plant. 129, 351-363. doi: 10.1111/j.1399-3054.2006.00814.x
50. Kawashima, C. G., Berkowitz, O., Hell, R., Noji, M., and Saito, K. (2005). Characterization and expression analysis of a serine acetyltransferase gene family involved in a key step of the sulfur assimilation pathway in Arabidopsis. Plant Physiol. 137, 220-230. doi: 10.1104/pp.104.045377.
51. Kawashima, C. G., Matthewman, C. A., Huang, S. Q., 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
52. Kawashima, C. G., Yoshimoto, N., Maruyama-Nakashita, A., Tsuchiya, Y. N., Saito, K., Takahashi, H., etal. (2009). Sulphur starvation induces the expression of microRNA-395 and one of its target genes but in different cell types. Plant J. 57, 313-321. doi: 10.1111/j.1365-313X.2008.03690.x
53. Khan, M. S., Haas, F. H., Samami, A. A., Gholami, A. M., Bauer, A., Fellen- berg, K., etal. (2010). Sulfite reductase defines a newly discovered bottleneck for assimilatory sulfate reduction and is essential for growth and development in Arabidopsis thaliana. Plant Cell 22, 1216-1231. doi: 10.1105/tpc.110.074088.
54. Kidd, B. N., Edgar, C. I., Kumar, K. K., Aitken, E. A., Schenk, P. M., Manners, J. M., etal. (2009). The mediator complex subunit PFT1 is a key regulator of jasmonate-dependent defense in Arabidopsis. Plant Cell 21, 2237-2252. doi: 10.1105/tpc.109.066910.
55. Kim, Y. J., Zheng, B., Yu, Y., Won, S. Y., Mo, B., and Chen, X. (2011). The role of mediator in small and long noncoding RNA production in Arabidopsis thaliana. EMBO J. 30, 814-822. doi: 10.1038/emboj.2011.3.
56. Kimura, Y., and Kimura, H. (2004). Hydrogen sulfide protects neurons from oxidative stress. FASEB J. 18, 1165-1167. doi: 10.1096/fj.04-1815fje
57. Kopriva, S., Buchert, T., Fritz, G., Suter, M., Weber, M., Benda, R., etal. (2001). Plant adenosine 5;-phospho sulfate reductase is a novel iron-sulfur protein. J. Biol. Chem. 276, 42881-42886. doi: 10.1074/jbc.M107424200.
58. Kopriva, S., and Koprivova, A. (2004). Plant adenosine 5;-phosphosulphate reductase: the past, the present, and the future. J. Exp. Bot. 55, 1775-1783. doi: 10.1093/Jxb/Erh185.
59. Kopriva, S., Muheim, R., Koprivova, A., Trachsel, N., Catalano, C., Suter, M., et al. (1999). Light regulation of assimilatory sulphate reduction in Arabidopsis thaliana. PlantJ. 20,37-44. doi: 10.1046/j.1365-313X.1999.00573.x
60. Kopriva, S., Suter, M., Von Ballmoos, P., Hesse, H., Krahenbuhl, U., Rennen- berg, H., etal. (2002). Interaction of sulfate assimilation with carbon and nitrogen metabolism in Lemna minor. Plant Physiol. 130, 1406-1413. doi: 10.1104/Pp.007773.
61. Koprivova, A., Calderwood, A., Lee, B. R., and Kopriva, S. (2014a). Do PFT1 and HY5 interact in regulation of sulfate assimilation by light in Arabidopsis? FEBS Lett. 588,1116-1121. doi: 10.1016/j.febslet.2014.02.031.
62. Koprivova, A., Harper, A. L., Trick, M., Bancroft, I., and Kopriva, S. (2014b). Dissection of control of anion homeostasis byassociative transcriptomics in Brassica napus. Plant Physiol. 166,442-450. doi: 10.1104/pp.114.239947.
63. Koprivova, A., Des Francs-Small, C. C., Calder, G., Mugford, S. T., Tanz, S., Lee, B. R., etal. (2010). Identification of a pentatricopeptide repeat protein implicated in splicing of intron 1 of mitochondrial nad7 transcripts. J. Biol. Chem. 285, 32192-32199. doi: 10.1074/jbc.M110.147603.
64. 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.
65. Koprivova, A., and Kopriva, S. (2008). Lessons from investigation of regulation of APS reductase by salt stress. Plant Signal. Behav. 3, 567-569. doi: 10.4161/psb.3.8.5716.
66. Koprivova, A., North, K. A., and Kopriva, S. (2008). Complex signaling network in regulation of adenosine 5’-phosphosulfate reductase by salt stress in Arabidopsis roots. PlantPhysiol. 146,1408-1420. doi: 10.1104/pp.107.113175.
67. Koprivova, A., Suter, M., Op Den Camp, R., Brunold, C., and Kopriva, S. (2000). Regulation of sulfate assimilation by nitrogen in Arabidopsis. Plant Physiol. 122, 737-746. doi: 10.1104/pp.122.3.737.
68. Lappartient, A. G., Vidmar, J. J., Leustek, T., Glass, A. D., and Touraine, B. (1999). Inter-organ signaling in plants: regulation of ATP sulfurylase and sulfate transporter genes expression in roots mediated by phloem-translocated compound. PlantJ. 18,89-95. doi: 10.1046/j.1365-313X.1999.00416.x
69. Lee, B. R., Koprivova, A., and Kopriva, S. (2011). The keyenzyme ofsulfate assimilation, adenosine 5/-phosphosulfate reductase, is regulated by HY5 in Arabidopsis. PlantJ. 67, 1042-1054. doi: 10.1111/j.1365-313X.2011.04656.x
70. Lee, J., He, K., Stolc, V., Lee, H., Figueroa, P., Gao, Y., et al. (2007). Analysis of transcription factor HY5 genomic binding sites revealed its hierarchical role in light regulation of development. Plant Cell 19, 731-749. doi: 10.1105/tpc.106.047688.
71. Lewandowska, M., Wawrzynska, A., Moniuszko, G., Lukomska, J., Zientara, K., Piecho, M., etal. (2010). A contribution to identification of novel regulators of plant response to sulfur deficiency: characteristics of a tobacco gene UP9C, its protein product and the effects of UP9C silencing. Mol. Plant 3, 347-360. doi: 10.1093/mp/ssq007.
72. Liang, G., Yang, F., andYu, D. (2010). MicroRNA395 mediates regulation of sulfate accumulation and allocation in Arabidopsis thaliana. Plant J. 62, 1046-1057. doi: 10.1111/j.1365-313X.2010.04216.x
73. Lisjak, M., Srivastava, N., Teklic, T., Civale, L., Lewandowski, K., Wilson, I., etal. (2010). A novel hydrogen sulfide donor causes stomatal opening and reduces nitric oxide accumulation. Plant Physiol. Biochem. 48, 931-935. doi: 10.1016/j.plaphy.2010.09.016.
74. Lisjak, M., Teklic, T., Wilson, I. D., Whiteman, M., and Hancock, J. T. (2013). Hydrogen sulfide: environmental factor or signalling molecule? Plant Cell Environ. 36, 1607-1616. doi: 10.1111/pce.12073.
75. Loudet, O., Saliba-Colombani, V., Camilleri, C., Calenge, F., Gaudon, V., Koprivova, A., etal. (2007). Natural variation for sulfate content in Arabidopsis thaliana is highlycontrolled byAPR2. Nat. Genet. 39, 896-900. doi: 10.1038/Ng2050.
76. Malitsky, S., Blum, E., Less, H., Venger, I., Elbaz, M., Morin, S., etal. (2008). The transcript and metabolite networks affected by the two clades of Arabidop- sis glucosinolate biosynthesis regulators. Plant Physiol. 148, 2021-2049. doi: 10.1104/pp.108.124784.
77. Maruyama-Nakashita, A., Inoue, E., Watanabe-Takahashi, A., Yamaya, T., and Takahashi, H. (2003). Transcriptome profiling of sulfur-responsive genes in Ara- bidopsis reveals global effects of sulfur nutrition on multiple metabolic pathways. PlantPhysiol. 132,597-605.doi: 10.1104/pp.102.019802.
78. 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. PlantCell 18, 3235-3251. doi: 10.1105/tpc.106.046458.
79. Maruyama-Nakashita, A., Nakamura, Y., Watanabe-Takahashi, A., Inoue, E., Yamaya, T., and Takahashi, H. (2005). Identification of a novel cis-acting element conferring sulfur deficiency response in Arabidopsis roots. Plant J. 42, 305-314. doi: 10.1111/j.1365-313X.2005.02363.x
80. Maruyama-Nakashita, A., Nakamura, Y., Watanabe-Takahashi, A., Yamaya, T., and Takahashi, H. (2004a). Induction of SULTR1;1 sulfate transporter in Ara- bidopsis roots involves protein phosphorylation/dephosphorylation circuit for transcriptional regulation. Plant Cell Physiol. 45, 340-345. doi: 10.1093/pcp/pch029.
81. Maruyama-Nakashita, A., Nakamura, Y., Yamaya, T., and Takahashi, H. (2004b). A novel regulatory pathway of sulfate uptake in Arabidopsis roots: implication of CRE1/WOL/AHK4-mediated cytokinin-dependent regulation. Plant J. 38, 779-789. doi: 10.1111/j.1365-313X.2004.02079.x
82. Matthewman, C. A., Kawashima, C. G., Huska, D., Csorba, T., Dalmay, T., and Kopriva, S. (2012). miR395 is a general component of the sulfate assim¬ilation regulatory network in Arabidopsis. FEBS Lett. 586, 3242-3248. doi: 10.1016/j.febslet.2012.06.044.
83. Mugford, S. G., Lee, B. R., Koprivova, A., Matthewman, C., and Kopriva, S. (2011). Control ofsulfur partitioningbetween primaryandsecondarymetabolism. Plant J. 65, 96-105. doi: 10.1111/j.1365-313X.2010.04410.x
84. Mugford, S. G., Matthewman, C. A., Hill, L., and Kopriva, S. (2010). Adenosine- 5/-phosphosulfate kinase is essential for Arabidopsis viability. FEBS Lett. 584, 119-123. doi: 10.1016/j.febslet.2009.11.014.
85. 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.
86. Neuenschwander, U., Suter, M., and Brunold, C. (1991). Regulation of sulfate assimilation by light and O-acetyl-l-serine in Lemna minor L. Plant Physiol. 97, 253-258. doi: 10.1104/pp.97.1.253.
87. Nussbaum, S., Schmutz, D., and Brunold, C. (1988). Regulation of assimilatory sulfate reduction by cadmium in Zea mays L. PlantPhysiol. 88, 1407-1410. doi: 10.1104/pp.88.4.1407.
88. Ohkama, N., Takei, K., Sakakibara, H., Hayashi, H., Yoneyama, T., and Fuji- wara, T. (2002). Regulation of sulfur-responsive gene expression by exogenously applied cytokinins in Arabidopsis thaliana. Plant Cell Physiol. 43,1493-1501. doi: 10.1093/pcp/pcf183.
89. Ou, B., Yin, K. Q., Liu, S. N., Yang, Y., Gu, T., Wing Hui, J. M., et al. (2011). A high-throughput screening system for Arabidopsis transcription factors and its application to Med25-dependent transcriptional regulation. Mol. Plant 4, 546-555. doi: 10.1093/mp/ssr002.
90. Pant, B. D., Musialak-Lange, M., Nuc, P., May, P., Buhtz, A., Kehr, J., et al. (2009). Identification of nutrient-responsive Arabidopsis and rapeseed microR- NAs by comprehensive real-time polymerase chain reaction profiling and small RNA sequencing. Plant Physiol. 150, 1541-1555. doi: 10.1104/pp.109.139139.
91. Park, S.-W., Li, W., Viehhausrer, A., He, B., Kim, S., Nilsson, A. K., et al. (2013). Cyclophilin 20-3 relays a 12-oxo-phytodienoic acid signal during stress responsive regulation of cellular redox homeostasis. Proc. Natl. Acad. Sci. U.S.A. 110, 9559-9564. doi: 10.1073/pnas.1218872110.
92. Pilon-Smits, E. A., Hwang, S., Mel Lytle, C., Zhu, Y., Tai, J. C., Bravo, R. C., et al. (1999). Overexpression of ATP sulfurylase in indian mustard leads to increased selenate uptake, reduction, and tolerance. Plant Physiol. 119, 123-132. doi: 10.1104/pp.119.1.123.
93. 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.
94. Rouached, H., Wirtz, M., Alary, R., Hell, R., Arpat, A. B., Davidian, J. C., et al. (2008). Differential regulation of the expression of two high-affinitysulfate trans-porters,SULTR1.1 andSULTR1.2,inArabidopsis. PlantPhysiol. 147,897-911.doi: 10.1104/pp.108.118612.
95. Sakakibara, H., Takei, K., and Hirose, N. (2006). Interactions between nitrogen and cytokinin in the regulation of metabolism and development. Trends PlantSci. 11, 440-448. doi: 10.1016/j.tplants.2006.07.004.
96. Scheerer, U., Haensch, R., Mendel, R. R., Kopriva, S., Rennenberg, H., and Her- schbach, C. (2010). Sulphur flux through the sulphate assimilation pathway is differently controlled by adenosine 5/-phosphosulphate reductase under stress and in transgenic poplar plants overexpressing gamma-ECS, SO, or APR. J. Exp. Bot. 61, 609-622. doi: 10.1093/Jxb/Erp327.
97. Shibagaki, N., and Grossman, A. R. (2010). Binding of cysteine synthase to the STAS domain of sulfate transporter and its regulatory consequences. J. Biol. Chem. 285, 25094-25102. doi: 10.1074/jbc.M110.126888.
98. Smith, F. W., Hawkesford, M. J., Ealing, P. M., Clarkson, D. T., Vanden Berg, P. J., Belcher, A. R., et al. (1997). Regulation of expression of a cDNA from barley roots encoding a high affinity sulphate transporter. Plant J. 12, 875-884. doi: 10.1046/j.1365-313X.1997.12040875.x
99. Sonderby, I. E., Hansen, B. G., Bjarnholt, N., Ticconi, C., Halkier, B. A., and 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. doi: 10.1371/journal.pone.0001322.
100. Sun, J., Wang, R., Zhang, X., Yu, Y., Zhao, R., Li, Z., etal. (2013). Hydrogen sulfide alleviates cadmium toxicity through regulations of cadmium transport across the plasma and vacuolar membranes in Populus euphratica cells. Plant Physiol. Biochem. 65, 67-74. doi: 10.1016/j.plaphy.2013.01.003.
101. 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.
102. Takahashi, H., Watanabe-Takahashi, A., Smith, F. W., Blake-Kalff, M., Hawkesford, M. J., and Saito, K. (2000). The roles of three functional sulphate transporters involved in uptake and translocation of sulphate in Arabidopsis thaliana. Plant J. 23, 171-182. doi: 10.1046/j.1365-313x.2000.00768.x
103. 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 inducedin sulfate-starvedroots playsacentral rolein Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A 94,11102-11107. doi: 10.1073/pnas.94.20.11102.
104. Tsakraklides, G., Martin, M., Chalam, R., Tarczynski, M. C., Schmidt, A., and Leustek, T. (2002). Sulfate reduction is increased in transgenic Arabidopsis thaliana expressing 5/adenylylsulfate reductase from Pseudomonas aeruginosa. PlantJ. 32,879-889. doi: 10.1046/j.1365-313X.2002.01477.x
105. Vauclare, P., Kopriva, S., Fell, D., Suter, M., Sticher, L., Von Ballmoos, P., et al. (2002). Flux control of sulphate assimilation in 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
106. Wangeline, A. L., Burkhead, J. L., Hale, K. L., Lindblom, S. D., Terry, N., Pilon, M., et al. (2004). Overexpression ofATP sulfurylase in Indian mustard: effects on tolerance and accumulation of twelve metals. J. Environ. Qual. 33, 54-60. doi: 10.2134/jeq2004.5400.
107. Wawrzynska, A., Lewandowska, M., and Sirko, A. (2010). Nicotiana tabacum EIL2 directly regulates expression of at least one tobacco gene induced by sulphur starvation. J. Exp. Bot. 61, 889-900. doi: 10.1093/jxb/erp356.
108. Wawrzynska, A., and Sirko, A. (2014). To control and to be controlled - understanding the Arabidopsis SLIM1 function in sulfur deficiencythrough comprehensive investigation of the EIL protein family. Front. Plant Sci. 5:575. doi: 10.3389/fpls.2014.00575.
109. Wirtz, M., Beard, K. F. M., Lee, C. P., Boltz, A., Schwarzlander, M., Fuchs, C., etal. (2012). Mitochondrial cysteine synthase complex regulates O- acetylserine biosynthesis in plants. J. Biol. Chem. 287, 27941-27947. doi: 10.1074/jbc.M112.372656.
110. Wirtz, M., Birke, H., Heeg, C., Muller, C., Hosp, F., Throm, C., et al. (2010). Structure and function of the hetero-oligomeric cysteine synthase complex in plants. J. Biol. Chem. 285,32810-32817. doi: 10.1074/jbc.M110.157446.
111. Wirtz, M., Droux, M., and Hell, R. (2004). O-acetylserine (thiol) lyase: an enigmatic enzyme of plant cysteine biosynthesis revisited in Arabidopsis thaliana. J. Exp. Bot. 55, 1785-1798. doi: 10.1093/Jxb/Erh201.
112. Wirtz, M., and Hell, R. (2006). Functional analysis of the cysteine synthase protein complex from plants: structural, biochemical and regulatory properties. J. Plant Physiol. 163,273-286. doi: 10.1016/j.jplph.2005.11.013.
113. Yarmolinsky, D., Brychkova, G., Fluhr, R., and Sagi, M. (2013). Sulfite reduc¬tase protects plants against sulfite toxicity. Plant Physiol. 161, 725-743. doi: 10.1104/pp.112.207712.
114. Yatusevich, R., Mugford, S. G., Matthewman, C., Gigolashvili, T., Frerigmann, H., Delaney, S., etal. (2010). Genes of primary sulfate assimilation are part of the glucosinolate biosynthetic network in Arabidopsis thaliana. Plant J. 62,1-11. doi: 10.1111/j.1365-313X.2009.04118.x
115. Yoshimoto, N., Inoue, E., Watanabe-Takahashi, A., Saito, K., and Taka- hashi, H. (2007). Posttranscriptional regulation of high-affinity sulfate trans¬porters in Arabidopsis by sulfur nutrition. Plant Physiol. 145, 378-388. doi: 10.1104/pp.107.105742.
116. Yoshimoto, N., Takahashi, H., Smith, F. W., Yamaya, T., and Saito, K. (2002). Two distinct high-affinity sulfate transporters with different inducibilities mediate uptake of sulfate in Arabidopsis roots. Plant J. 29, 465-473. doi: 10.1046/j.0960-7412.2001.01231.x
117. Zhang, B., Pasini, R., Dan, H., Joshi, N., Zhao, Y., Leustek, T., et al. (2014). Aberrant gene expression in the Arabidopsis SULTR1;2 mutants suggests a possible regula¬tory role for this sulfate transporter in response to sulfur nutrient status. Plant J. 77, 185-197. doi: 10.1111/tpj.12376.
118. Zhang, L. W., Song, J. B., Shu, X. X., Zhang, Y., and Yang, Z. M. (2013). miR395 is involved in detoxification of cadmium in Brassica napus. J. Hazard. Mater. 250-251,204-211. doi: 10.1016/j.jhazmat.2013.01.053