Exploring the importance of sulfate transporters and ATP sulphurylases for selenium hyperaccumulation — a comparison of Stanleys pinnata and Brassica juncea (Brassicaceae)

Frontiers in Plant Science

Volumn 6, Issue JAN, 2015, Pages 1-13

  Schiavon, Michela ^a   Pilon, Marinus ^b   Malagoli, Mario ^a   Pilon Smits, Elizabeth A H ^b  

^a UNIVERSITY OF PADOVA   (Italy)

^b Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

ATP sulphurylase; Brassica juncea; Gene expression; Selenium; Stanleya pinnata; Sulfur; Uptake

Indexed keywords

BRASSICA JUNCEA; BRASSICACEAE; STANLEYA PINNATA;

EID: 84922260950     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2015.00002     Document Type: Article

References (48)

1. Barberon, M., Berthomieu, P., Clairotte, M., Shibagaki, N., Davidian, J. C., and Gosti, F. (2008). Unequal functional redundancy between the two Arabidopsis thaliana high-affinity sulphate transporters SULTR1;1 and SULTR1;2. New Phytol. 180, 608-619. doi: 10.1111/j.1469-8137.2008.02604.x
2. Broadley, M. R., White, P. J., Bryson, R. J., Meacham, M. C., Bowen, H. C., Johnson, S. E., et al. (2006). Biofortification ofU.K. food crops with selenium (Se). Proc. Nutr. Soc. 65, 169-181. doi: 10.1079/PNS2006490
3. Buchner, P., Stuiver, C. E., Westerman, S., Wirtz, M., Hell, R., Hawkesford, M. J., et al. (2004). Regulation of sulfate uptake and expression of sulfate transporter genes in Brassica oleracea as affected by atmospheric H2S and pedospheric sulfate nutrition. Plant Physiol. 136, 3396-3408. doi: 10.1104/pp.104.046441
4. Cabannes, E., Buchner, P., Broadley, M. R., and Hawkesford, M. J. (2011). A comparison of sulfate and selenium accumulation in relation to the expression of sulfate transporter genes in astragalus species. Plant Physiol. 157, 2227-2239. doi: 10.1104/pp.111.183897
5. de Souza, M. P., Pilon-Smits, E. A., Lytle, C. M., Hwang, S., Tai, J., Honma, T. S., et al. (1998). Rate-limiting steps in selenium assimilation and volatilization by indian mustard. PlantPhysiol. 117, 1487-1494. doi: 10.1104/pp.117.4.1487
6. Ellis, D. R., and Salt, D. E. (2003). Plant, selenium and human health. Curr. Opin. Plant. Biol. 6, 273-279. doi: 10.1016/S1369-5266(03)00030-X
7. El Mehdawi, A. F., Cappa, J. J., Fakra, S. C., Self, J., and Pilon-Smits, E. A. H. (2012). Interactions of selenium and non-accumulators during co-cultivation on seleniferous or non-seleniferous soil - The importance of having good neighbors. NewPhytol. 194, 264-277. doi: 10.1111/j.1469-8137.2011.04043.x
8. Fassel, V. A. (1978). Quantitative elemental analyses by plasma emission spectroscopy. Science 202, 183-191. doi: 10.1126/science.202.4364.183
9. Freeman, J. L., Marcus, M. A., Fakra, S. C., Devonshire, J., McGrath, S. P., and Pilon- Smits, E. A. H. (2012). Seeds of selenium hyperaccumulators Stanleya pinnata and Astragalus bisulcatus are colonized by Se-resistant, Se-excluding wasp and beetle herbivores. PLoS ONE 7:e50516. doi: 10.1371/journal.pone.0050516
10. Freeman, J. L., Tamaoki, M., Stushnoff, C., Quinn, C. F., Cappa, J. J., Devonshire, J., et al. (2010). Molecular mechanisms of selenium tolerance and hyperaccumulation in Stanleya pinnata. Plant Physiol. 153, 1630-1652. doi: 10.1104/pp.110.156570
11. Freeman, J. L., Zhang, L. H., Marcus, M. A., Fakra, S., McGrath, S. P., and Pilon-Smits, E. A. H. (2006). Spatial imaging, speciation and quantification of selenium in the hyperaccumulator plants Astragalus bisulcatus and Stanleya pinnata. Plant Physiol. 142, 124-134. doi: 10.1104/pp.106.081158
12. Galeas, M. L., Zhang, L. H., Freeman, J. L., Wegner, M., and Pilon-Smits, E. A. H. (2007). Seasonal fluctuations of selenium and sulphur accumulation in selenium hyperaccumulators and related nonaccumulators. New Phytol. 173, 517-525. doi: 10.1111/j.1469-8137.2006.01943.x
13. Harris, J., Schneberg, K. A., and Pilon-Smits, E. A. H. (2014). Sulphur—selenium— molybdenum interactions distinguish selenium hyperaccumulator Stanleyapin- nata from non-hyperaccumulator Brassica juncea (Brassicaceae). Planta 239, 479-491. doi: 10.1007/s00425-013-1996-8
14. Hatfield, D. L., Tsuji, P. A., Carlson, B. A., and Gladyshev, V. N. (2014). Selenium and selenocysteine: roles in cancer, health, and development. Trends Biochem. Sci. 39, 112-120. doi: 10.1016/j.tibs.2013.12.007
15. Hatzfeld, Y., Lee, S., Lee, M., Leustek, T., and Saito, K. (2000). Functional characterization of a gene encoding a fourth ATP sulfurylase isoform from Arabidopsis thaliana. Gene 248, 51-58. doi: 10.1016/S0378-1119(00)00132-3
16. Hawkesford, M. J. (2003) Transporter gene families in plants: the sulphate transporter gene family—redundancy or specialization? Physiol. Plantarum 117, 155-163. doi: 10.1034/j.1399-3054.2003.00034.x
17. Hoagland, D., and Arnon, D. I. (1938). The water culture method for growing plants without soil. Calif. Agric. Exp. Stat. Circ. 347, 1-39.
18. Kawashima, C. G., Yoshimoto, N., Maruyama-Nakashita, A., Tsuchiya, Y. N., Saito, K., Takahashi, H., et al. (2009). Sulphur starvation induces the expression of microRNA-395 and one of its target genes but in different cell types. PlantJ. 57, 313-321. doi: 10.1111/j.1365-313X.2008.03690.x
19. Lee, K. H., and Jeong, D. (2012). Bimodal actions of selenium essential for antioxidant and toxic pro-oxidant activities: the selenium paradox. Mol. Med. Rep. 5, 299-304. doi: 10.3892/mmr.2011.651
20. Leustek, T., Murillo, M., and Cervantes, M. (1994). Cloning of a cDNA encoding ATP sulfurylase from Arabidopsis thaliana by functional expression in Saccharomyces cerevisiae. Plant Physiol. 105, 897-902. doi: 10.1104/pp.105.3.897
21. Liang, G., and Yu, D. (2010). Reciprocal regulation among miR395, APS and SULTR2;1 in Arabidopsis thaliana. Plant Signal. Behav. 5, 1257-1259. doi: 10.4161/psb.5.10.12608
22. Muller, P. Y., Janovjak, H., Miserez, A. R., and Dobbie, Z. (2002). Processing of gene expression data generated by quantitative real-time RTPCR. Biotechniques 32, 1372-1379.
23. Murillo, M., and Leustek, T. (1995). Adenosine-5;-triphosphate-sulfurylase from Arabidopsis thaliana and Escherichia coli are functionally equivalent but structurally and kinetically divergent: nucleotide sequence of two adenosine- 5/-triphosphate-sulfurylase cDNAs from Arabidopsis thaliana and analysis of a recombinant enzyme. Arch. Biochem. Biophys. 323, 195-204 doi: 10.1006/abbi.1995.0026
24. Neuhierl, B., and Bock, A. (2002). Selenocysteine methyltransferase. Methods Enzymol. 347, 203-207. doi: 10.1016/S0076-6879(02)47019-X
25. Pilon-Smits, E. A. H., Hwang, S. B., Lytle, C. M., Zhu, Y. L., Tai, J. C., Bravo, R. C., et al. (1999). Overexpression of ATP sulphurylase in Brassica juncea leads to increased selenate uptake, reduction and tolerance. Plant Physiol. 119, 123-132. doi: 10.1104/pp.119.1.123
26. Pilon-Smits, E. A. H., and LeDuc, D. L. (2009). Phytoremediation of selenium using transgenic plants. Curr. Opin. Biotechnol. 20, 207-212. doi: 10.1016/j.copbio.2009.02.001
27. Pilon-Smits, E. A. H., Quinn, C. F., Tapken, W., Malagoli, M., and Schiavon, M.Physiological functions of beneficial elements. Curr. Opin. Plant Biol. 12, 267-274. doi: 10.1016/j.pbi.2009.04.009
28. Rayman, M. P. (2009). Selenoproteins and human health: insights from epidemiological data. Biochim. Biophys. Acta. 1790, 1533-1540. doi: 10.1016/j.bbagen.2009.03.014
29. Rayman, M. P. (2012). Selenium and human health. Lancet 379, 1256-1268. doi: 10.1016/S0140-6736(11)61452-9
30. Reilly, C. (2006). Selenium in FoodandHealth. NewYork, NY: Springer, 206.
31. 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-affinity sulfate transporters, SULTR1.1 and SULTR1.2, in Arabidopsis. Plant Physiol. 147, 897-911. doi: 10.1104/pp.108.118612
32. Saidi, I., Chtourou, Y., and Djebali, W. (2014). Selenium alleviates cadmium toxicity by preventing oxidative stress in sunflower (Helianthus annuus) seedlings. J. PlantPhysiol. 171, 85-91. doi: 10.1016/j.jplph.2013.09.024
33. Sambrook, J., and Russell, D. W. (2001). Molecular Cloning: A Laboratory Manual, Vol. 1. NewYork, NY: CSHL Press.
34. 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
35. Shibagaki, N., Rose, A., McDermott, J. P., Fujiwara, T., Hayashi, H., Yoneyama, T., et al. (2002). Selenate-resistant mutants of Arabidopsis thaliana identify Sultr1;2, a sulphate transporter required for efficient transport of sulphate into roots. Plant J. 29, 475-486. doi: 10.1046/j.0960-7412.2001.01232.x
36. Sors, T. G., Ellis, D. R., and Salt, D. E. (2005). Selenium uptake, translocation, assimilation and metabolic fate in plants. Photosynth. Res. 86, 373-389. doi: 10.1007/s11120-005-5222-9
37. Stadtman, T. C. (2000). Selenium biochemistry. Mammalian selenoenzymes. Ann. N.Y.Acad. Sci. 899,399-402. doi: 10.1111/j.1749-6632.2000.tb06203.x
38. Stadtman, T. C. (2005). Selenoproteins—tracing the role of a trace element in proteinfunction. PLoS Biol. 3:e421. doi: 10.1371/journal.pbio.0030421
39. 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
40. Terry, N., Zayed, A. M., de Souza, M. P., and Tarun, A. S. (2000). Selenium in higher plants. Ann. Rev. Plant Physiol. Mol. Biol. 51, 401-432. doi: 10.1146/annurev.arplant.51.1.401
41. USDA. (2012). USDA National Nutrient Database for Standard Reference, Release 25. Nutrient Data Laboratory Home Page. U.S. Department of Agriculture, Agricultural Research Service. Available online at: http://www.ars.usda.gov/research/publications/Publications.htm?seq_no_115=285841
42. Van Hoewyk, D. (2013). A tale of two toxicities: malformed selenoproteins and oxidative stress both contribute to selenium stress in plants. Ann. Bot. 112, 965-972. doi: 10.1093/aob/mct163
43. Van Hoewyk, D., Takahashi, H., Hess, A., Tamaoki, M., and Pilon-Smits, E. A. H. (2008). Transcriptome and biochemical analyses give insights into selenium- stress responses and selenium tolerance mechanisms in Arabidopsis. Physiol. Plant. 132, 236-253. doi: 10.1111/j.1399-3054.2007.01002.x
44. Van Huysen, T., Abdel-Ghany, S., Hale, K. L., LeDuc, D., Terry, N., and Pilon- Smits, E. A. H. (2003). Overexpression of cystathionine-gamma-synthase enhances selenium volatilization in Brassica juncea. Planta 218, 71-78. doi: 10.1007/s00425-003-1070-z
45. White, P. J., Bowen, H. C., Marshall, B., and Broadley, M. R. (2007). Extraordinarily high leaf selenium to sulphur ratios define ‘Se-accumulator’ plants. Ann. Bot. 100, 111-118. doi: 10.1093/aob/mcm084
46. White, P. J., Bowen, H. C., Parmaguru, P., Fritz, M., Spracklen, W. P., Spiby, R. E., et al. (2004). Interactions between selenium and sulphur nutrition in Arabidopsis thaliana. J. Exp. Bot. 55, 1927-1937. doi: 10.1093/jxb/erh192
47. 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
48. Zarcinas, B. A., Cartwright, B., and Spouncer, L. R. (1987). Nitric acid digestion and multi-element analysis of plant material by inductively coupled plasma spectrometry. Commun. Soil Sci. Plan. 18, 131-146. doi: 10.1080/00103628709367806