SULTR3;1 is a chloroplast-localized sulfate transporter in Arabidopsis thaliana

Plant Journal

Volumn 73, Issue 4, 2013, Pages 607-616

  Cao, Min Jie ^a   Wang, Zhen ^a   Wirtz, Markus ^b   Hell, Ruediger ^b   Oliver, David J ^c   Xiang, Cheng Bin ^a  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c IOWA STATE UNIVERSITY   (United States)

Author keywords

Arabidopsis; chloroplast; sulfate; sulfate transporter; SULTR3; 1

Indexed keywords

ARABIDOPSIS; CHLOROPLAST; SULFATE; SULFATE TRANSPORTER; SULTR3 1;

AMINO ACIDS; CHLOROPHYLL; PLANTS (BOTANY); SULFUR;

SULFUR COMPOUNDS;

ARABIDOPSIS PROTEIN; CHLOROPLAST PROTEIN; CYSTEINE; GLUTATHIONE; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; SODIUM SULFATE; SULFATE;

ARABIDOPSIS; ARTICLE; CHLOROPLAST; DRUG EFFECT; GENE INACTIVATION; GENETIC COMPLEMENTATION; GENETICS; METABOLISM; PROMOTER REGION; PROTEIN TRANSPORT; PROTOPLAST; TRANSGENIC PLANT; WESTERN BLOTTING;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BLOTTING, WESTERN; CHLOROPLAST PROTEINS; CHLOROPLASTS; CYSTEINE; GENE KNOCKOUT TECHNIQUES; GENETIC COMPLEMENTATION TEST; GLUTATHIONE; GREEN FLUORESCENT PROTEINS; PLANTS, GENETICALLY MODIFIED; PROMOTER REGIONS, GENETIC; PROTEIN TRANSPORT; PROTOPLASTS; RECOMBINANT FUSION PROTEINS; SULFATES;

ARABIDOPSIS; ARABIDOPSIS THALIANA; EMBRYOPHYTA; TRACHEOPHYTA;

EID: 84874262000     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12059     Document Type: Article

References (41)

1. Alonso, J.M., Stepanova, A.N., Leisse, T.J., et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science, 301, 653-657.
2. Alvarez, C., Bermudez, M.A., Romero, L.C., Gotor, C., and, Garcia, I., (2012) Cysteine homeostasis plays an essential role in plant immunity. New Phytol. 193, 165-177.
3. Bechtold, N., Ellis, J., and, Pelletier, G., (1993) In planta Agrobacterium mediated gene transfer by infiltration of adult Arabidopsis thaliana plants. C. R. Acad. Sci. Paris, Life Sciences 316, 1194-1199.
4. Bent, A.F., (2000) Arabidopsis in planta transformation. Uses, mechanisms, and prospects for transformation of other species. Plant Physiol. 124, 1540-1547.
5. Bregman, A., (1990) Laboratory Investigations in Cell and Molecular Biology. 3rd edn. New York: John Wiley and Sons.
6. Buchner, P., Stuiver, C.E., Westerman, S., Wirtz, M., Hell, R., Hawkesford, M.J., and, De Kok, L.J., (2004) Regulation of sulfate uptake and expression of sulfate transporter genes in Brassica oleracea as affected by atmospheric H(2)S and pedospheric sulfate nutrition. Plant Physiol. 136, 3396-3408.
7. Chen, H.C., and, Melis, A., (2004) Localization and function of SulP, a nuclear-encoded chloroplast sulfate permease in Chlamydomonas reinhardtii. Planta, 220, 198-210.
8. Chen, H.C., Yokthongwattana, K., Newton, A.J., and, Melis, A., (2003) SulP, a nuclear gene encoding a putative chloroplast-targeted sulfate permease in Chlamydomonas reinhardtii. Planta, 218, 98-106.
9. Cherest, H., Davidian, J.C., Thomas, D., Benes, V., Ansorge, W., and, Surdin-Kerjan, Y., (1997) Molecular characterization of two high affinity sulfate transporters in Saccharomyces cerevisiae. Genetics, 145, 627-635.
10. Demidchik, V., and, Tester, M., (2002) Sodium fluxes through nonselective cation channels in the plasma membrane of protoplasts from Arabidopsis roots. Plant Physiol. 128, 379-387.
11. Ferro, M., Brugiere, S., Salvi, D., et al. (2010) AT-CHLORO, a comprehensive chloroplast proteome database with subplastidial localization and curated information on envelope proteins. Mol. Cell. Proteomics 9, 1063-1084.
12. Forsman, C., and, Pilon, M., (1995) Chloroplast import and sequential maturation of pea carbonic anhydrase: the roles of various parts of the transit peptide. FEBS Lett. 358, 39-42.
13. Friso, G., Majeran, W., Huang, M., Sun, Q., and, van Wijk, K.J., (2010) Reconstruction of metabolic pathways, protein expression, and homeostasis machineries across maize bundle sheath and mesophyll chloroplasts: large-scale quantitative proteomics using the first maize genome assembly. Plant Physiol. 152, 1219-1250.
14. Gasber, A., Klaumann, S., Trentmann, O., et al. (2011) Identification of an Arabidopsis solute carrier critical for intracellular transport and inter-organ allocation of molybdate. Plant Biol. (Stuttg) 13, 710-718.
15. Gross, A., Brückner, G., Heldt, H.W., and, Flügge, U.-I., (1990) Comparison of the kinetic properties, inhibition and labelling of the phosphate translocators from maize and spinach mesophyll chloroplasts. Planta, 180, 262-271.
16. Hell, R., and, Wirtz, M., (2011) Molecular Biology, Biochemistry and Cellular Physiology of Cysteine Metabolism in Arabidopsis thaliana. Arabidopsis Book 9, e0154.
17. Jane K, S., (1988) Genetic Engineering:Principles and Methods. New York: Plenum Press.
18. Kataoka, T., Hayashi, N., Yamaya, T., and, Takahashi, H., (2004a) 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. 136, 4198-4204.
19. Kataoka, T., Watanabe-Takahashi, A., Hayashi, N., Ohnishi, M., Mimura, T., Buchner, P., Hawkesford, M.J., Yamaya, T., and, Takahashi, H., (2004b) Vacuolar sulfate transporters are essential determinants controlling internal distribution of sulfate in Arabidopsis. Plant Cell, 16, 2693-2704.
20. Kawashima, C.G., Matthewman, C.A., Huang, S., et al. (2011) Interplay of SLIM1 and miR395 in the regulation of sulfate assimilation in Arabidopsis. Plant J. 66, 863-876.
21. Kunst, L., (1998) Preparation of physiologically active chloroplasts from Arabidopsis. Methods Mol. Biol. (Clifton, N.J) 82, 43-48.
22. Lee, B.R., Koprivova, A., and, Kopriva, S., (2011) The key enzyme of sulfate assimilation, adenosine 5'-phosphosulfate reductase, is regulated by HY5 in Arabidopsis. Plant J. 67, 1042-1054.
23. Lei, Z.-Y., Zhao, P., Cao, M.-J., Cui, R., Chen, X., Xiong, L.-Z., Zhang, Q.-F., Oliver, D.J., and, Xiang, C.-B., (2007) High-throughput binary vectors for plant gene function analysis. J. Integr. Plant Biol. 49, 556-567.
24. Leustek, T., Martin, M.N., Bick, J.A., and, Davies, J.P., (2000) Pathways and regulation of sulfur metabolism revealed through molecular and genetic studies. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51, 141-165.
25. Mourioux, G., and, Douce, R., (1979) [Sulfate transport across the limiting double membrane or envelope, of spinach chloroplasts]. Biochimie. 61, 1283-1292.
26. Peltier, J.B., Emanuelsson, O., Kalume, D.E., et al. (2002) Central functions of the lumenal and peripheral thylakoid proteome of Arabidopsis determined by experimentation and genome-wide prediction. Plant Cell, 14, 211-236.
27. Rouached, H., Berthomieu, P., El Kassis, E., Cathala, N., Catherinot, V., Labesse, G., Davidian, J.C., and, Fourcroy, P., (2005) 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. 280, 15976-15983.
28. Saito, K., (2000) Regulation of sulfate transport and synthesis of sulfur-containing amino acids. Curr. Opin. Plant Biol. 3, 188-195.
29. Sharma, A.K., Rigby, A.C., and, Alper, S.L., (2011a) STAS domain structure and function. Cell. Physiol. Biochem. 28, 407-422.
30. Sharma, A.K., Ye, L., Baer, C.E., Shanmugasundaram, K., Alber, T., Alper, S.L., and, Rigby, A.C., (2011b) Solution structure of the guanine nucleotide-binding STAS domain of SLC26-related SulP protein Rv1739c from Mycobacterium tuberculosis. J. Biol. Chem. 286, 8534-8544.
31. Shibagaki, N., and, Grossman, A.R., (2004) Probing the function of STAS domains of the Arabidopsis sulfate transporters. J. Biol. Chem. 279, 30791-30799.
32. Shibagaki, N., Rose, A., McDermott, J.P., Fujiwara, T., Hayashi, H., Yoneyama, T., and, Davies, J.P., (2002) Selenate-resistant mutants of Arabidopsis thaliana identify Sultr1;2, a sulfate transporter required for efficient transport of sulfate into roots. Plant J. 29, 475-486.
33. Smith, F.W., Ealing, P.M., Hawkesford, M.J., and, Clarkson, D.T., (1995) Plant members of a family of sulfate transporters reveal functional subtypes. Proc. Natl Acad. Sci. USA, 92, 9373-9377.
34. 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.
35. 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.
36. Tomatsu, H., Takano, J., Takahashi, H., Watanabe-Takahashi, A., Shibagaki, N., and, Fujiwara, T., (2007) An Arabidopsis thaliana high-affinity molybdate transporter required for efficient uptake of molybdate from soil. Proc. Natl Acad. Sci. USA, 104, 18807-18812.
37. Xiang, C., and, Oliver, D.J., (1998) Glutathione metabolic genes coordinately respond to heavy metals and jasmonic acid in Arabidopsis. Plant Cell, 10, 1539-1550.
38. Xiang, C., Werner, B.L., Christensen, E.M., and, Oliver, D.J., (2001) The biological functions of glutathione revisited in arabidopsis transgenic plants with altered glutathione levels. Plant Physiol. 126, 564-574.
39. 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.
40. Yoshimoto, N., Inoue, E., Saito, K., Yamaya, T., and, Takahashi, H., (2003) Phloem-localizing sulfate transporter, Sultr1;3, mediates re-distribution of sulfur from source to sink organs in Arabidopsis. Plant Physiol. 131, 1511-1517.
41. Zuber, H., Davidian, J.C., Aubert, G., et al. (2010) The seed composition of Arabidopsis mutants for the group 3 sulfate transporters indicates a role in sulfate translocation within developing seeds. Plant Physiol. 154, 913-926.