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 Journal

Volumn 33, Issue 4, 2003, Pages 651-663

  Hirai, Masami Yokota ^a   Fujiwara, Toru ^b   Awazuhara, Motoko ^a   Kimura, Tomoko ^b   Noji, Masaaki ^a   Saito, Kazuki ^a  

^a CHIBA UNIVERSITY   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

Adaptive response; Arabidopsis; Macroarray; O acetyl L serine; Sulfur deficiency; Transcriptome analysis

Indexed keywords

CLONING; DNA; GENES; METABOLISM; SULFUR;

SULFUR DEFICIENCY;

PLANTS (BOTANY);

ADAPTATION, PHYSIOLOGICAL; ANION TRANSPORT PROTEINS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CARRIER PROTEINS; CYSTEINE; EXPRESSED SEQUENCE TAGS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GLUTATHIONE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLANT LEAVES; PLANT ROOTS; SERINE; STATISTICS; SULFATES; SULFUR;

ARABIDOPSIS; ARABIDOPSIS THALIANA; EMBRYOPHYTA; EUKARYOTA;

EID: 0344177200     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-313X.2003.01658.x     Document Type: Article

References (52)

1. Anderson, M.E. (1985) Determination of glutathione and glutathione disulfide in biological samples. Meth. Enzymol. 113, 548-555.
2. Asamizu, E., Nakamura, Y., Sato, S. and Tabata, S. (2000) A large scale analysis of cDNA in Arabidopsis thaliana: generation of 12,028 non-redundant expressed sequence tags from normalized and size-selected cDNA libraries. DNA Res. 7, 175-180.
3. Awazuhara, M., Hirai, M.Y., Hayashi, H., Chino, M., Naito, S. and Fujiwara, T. (2000) O-acetyl-L-serine content in rosette leaves of Arabidopsis thaliana affected by S and N nutrition. In Sulfur Nutrition and Sulfur Assimilation in Higher Plants (Brunold, C., Rennenberg, H., De Kok, L.J., Stulen, I. and Davidian, J.-C., eds). Bern, Switzerland: Paul Haupt, pp. 331-333.
4. Berger, S., Bell, E., Sadka, A. and Mullet, J.E. (1995) Arabidopsis thaliana Atvsp is homologous to soybean VspA and VspB, genes encoding vegetative storage protein acid phosphatases, and is regulated similarly by methyl jasmonate, wounding, sugars, light and phosphate. Plant Mol. Biol. 27, 933-942.
5. Blanchard, R.K., Moore, J.B., Green, C.L. and Cousins, R.J. (2001) Modulation of intestinal gene expression by dietary zinc status: effectiveness of cDNA arrays for expression profiling of a single nutrient deficiency. Proc. Natl. Acad. Sci. USA, 98, 13507-13513.
6. Bolchi, A., Petrucco, S., Tenca, P.L., Foroni, C. and Ottonello, S. (1999) Coordinate modulation of maize sulfate permease and ATP sulfurylase mRNAs in response to variations in sulfur nutritional status: stereospecific down-regulation by L-cysteine. Plant Mol. Biol. 39, 527-537.
7. Carpenter, C.D., Kreps, J.A. and Simon, A.E. (1994) Genes encoding glycine-rich Arabidopsis thaliana proteins with RNA-binding motifs are influenced by cold treatment and an endogenous circadian rhythm. Plant Physiol. 104, 1015-1025.
8. Church, G.M. and Gilbert, W. (1984) Genomic sequencing. Proc. Natl. Acad. Sci. USA, 81, 1991-1995.
9. Clarkson, D.T., Diogo, E. and Amâncio, S. (1999) Uptake and assimilation of sulphate by sulphur deficient Zea mays cells: the role of O-acetyl-L-serine in the interaction between nitrogen and sulphur assimilatory pathways. Plant Physiol. Biochem. 37, 283-290.
10. Detweiler, C.S., Cunanan, D.B. and Falkow, S. (2001) Host microarray analysis reveals a role for the Salmonella response regulator phoP in human macrophage cell death. Proc. Natl. Acad. Sci. USA, 98, 5850-5855.
11. Fahey, R.C. and Newton, G.L. (1987) Determination of low-molecular-weight thiols using monobromobimane fluorescent labeling and high-performance liquid chromatography. Meth. Enzymol. 143, 85-96.
12. Finkelstein, D., Ewing, R., Gollub, J., Sterky, F., Cherry, J.M. and Somerville, S. (2002) Microarray data quality analysis: lessons from the AFGC project. Plant Mol. Biol. 48, 119-131.
13. Fujiwara, T., Hirai, M.Y., Chino, M., Komeda, Y. and Naito, S. (1992) Effects of sulfur nutrition on expression of the soybean seed storage protein genes in transgenic petunia. Plant Physiol. 99, 263-268.
14. Furlong, E.E.M., Andersen, E.C., Null, B., White, K.P. and Scott, M.P. (2001) Patterns of gene expression during Drosophila mesoderm development. Science, 293, 1629-1633.
15. Gamborg, O.L., Miller, R.A. and Ojima, K. (1968) Nutrient requirements of suspension cultures of soybean root cells. Exp. Cell Res. 50, 151-158.
16. Gayler, K.R. and Sykes, G.E. (1985) Effects of nutritional stress on the storage proteins of soybeans. Plant Physiol. 78, 582-585.
17. Gray, W.M. and Estelle, M. (2000) Function of the ubiquitin-proteasome pathway in auxin response. Trends Biochem. Sci. 25, 133-138.
18. Gutierrez-Marcos, J.F., Roberts, M.A., Campbell, E.I. and Wray, J.L. (1996) Three members of a novel small gene-family from Arabidopsis thaliana able to complement functionally an Escherichia coli mutant defective in PAPS reductase activity encode proteins with a thioredoxin-like domain and 'APS reductase' activity. Proc. Natl. Acad. Sci. USA, 93, 13377-13382.
19. Harms, K., von Ballmoos, P., Brunold, C., Höfgen, R. and Hesse, H. (2000) Expression of a bacterial serine acetyltransferase in transgenic potato plants leads to increased levels of cysteine and glutathione. Plant J. 22, 335-343.
20. Hatzfeld, Y. and Saito, K. (2000) Regulation of sulfate transporter genes in Arabidopsis thaliana. In Sulfur Nutrition and Sulfur Assimilation in Higher Plants. (Brunold, C., Rennenberg, H., De Kok, L.J., Stulen, I. and Davidian, J.-C., eds). Bern, Switzerland: Paul Haupt, pp. 269-271.
21. Hawkesford, M.J. (2000) Plant responses to sulphur deficiency and the genetic manipulation of sulphate transporters to improve S-utilization efficiency. J. Exp. Bot. 51, 131-138.
22. He, Y., Fukushige, H., Hildebrand, D.F. and Gan, S. (2002) Evidence supporting a role of jasmonic acid in Arabidopsis leaf senescence. Plant Physiol. 128, 876-884.
23. Hirai, M.Y., Fujiwara, T., Chino, M. and Naito, S. (1995) Effects of sulfate concentrations on the expression of a soybean seed storage protein gene and its reversibility in transgenic Arabidopsis thaliana. Plant Cell Physiol. 36, 1331-1339.
24. Hirai, M.Y., Kim, H., Hayashi, H., Chino, M., Naito, S. and Fujiwara, T. (2002) Independent roles of methionine and O-acetyl-L-serine in the regulation of the β subunit gene of β-conglycinin. Soil Sci. Plant Nutr. 48, 87-94.
25. Kim, H., Awazuhara, M., Hayashi, H., Chino, M. and Fujiwara, T. (1997) Analysis of O-acetyl-L-serine in in vitro cultured soybean cotyledons. In Suphfur Metabolism in Higher Plants (Cram, W.J., De Kok, L.J., Stulen, I., Brunold, C. and Rennenberg, H., eds). Leiden, the Netherlands: Backhuys Publishers, pp. 307-309.
26. Kim, H., Hirai, M.Y., Hayashi, H., Chino, M., Naito, S. and Fujiwara, T. (1999) Role of O-acetyl-L-serine in the coordinated regulation of the expression of a soybean seed storage-protein gene by sulfur and nitrogen nutrition. Planta, 209, 282-289.
27. 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.
28. Kredich, N.M. (1993) Gene regulation of sulfur assimilation. In Sulfur Nutrition and Assimilation in Higher Plants (De Kok, L.J., Stulen, I., Rennenberg, H., Brunoid, C. and Rauser, W.E., eds). The Hague, the Netherlands: SPB Academic Publishers, pp. 37-47.
29. Kutz, A., Müller, A., Hennig, P., Kaiser, W.M., Piotrowski, M. and Weiler, E.W. (2002) A role for nitrilase 3 in the regulation of root morphology in sulphur-starving Arabidopsis thaliana. Plant J. 30, 95-106.
30. Lappartient, A.G., Vidmar, J.J., Leustek, T., Glass, A.D.M. 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. Plant J. 18, 89-95.
31. Leustek, T. and Saito, K. (1999) Sulfate transport and assimilation in plants. Plant Physiol. 120, 637-643.
32. Murashige, T. and Skoog, F. (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant. 15, 473-497.
33. Naito, S., Hirai, M.Y., Chino, M. and Komeda, Y. (1994) Expression of a soybean (Glycine max [L.] Merr.) seed storage protein gene in transgenic Arabidopsis thaliana and its response to nutritional stress and abscisic acid mutations. Plant Physiol. 104, 497-503.
34. Nikiforova, V., Freitag, J., Kempa, S., Adamik, M., Hesse, H., and Höfgen, R. (2003) Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: interlacing of biosynthetic pathways provides response specificity. Plant J. 33, 633-650.
35. Saito, K. (2000) Regulation of sulfate transport and synthesis of sulfur-containing amino acids. Curr. Opin. Plant Biol. 3, 188-195.
36. Saito, K., Kurosawa, M., Tatsuguchi, K., Takagi, Y. and Murakoshi, I. (1994) Modulation of cysteine biosynthesis in chloroplasts of transgenic tobacco overexpressing cysteine synthase [O-acetyl-serine (thiol) -lyase]. Plant Physiol. 106, 887-895.
37. Sasaki, Y., Asamizu, E., Shibata, D. et al. (2001) Monitoring of methyl jasmonate-responsive genes in Arabidopsis by cDNA macroarray: self-activation of jasmonic acid biosynthesis and crosstalk with other phytohormone signaling pathways. DNA Res. 8, 153-161.
38. Sasaki-Sekimoto, Y., Obayashi, T., Matsuumi, M., Kobayashi, Y., Asamizu, E., Shibata, D., Nakamura, Y., Masuda, T., Shimada, H., Takamiya, K., Tabata, S. and Ohta, H. (2002) Monitoring of 12-oxo-phytodienoic acid (OPDA)-induced expression changes in Arabidopsis by cDNA macroarray. In Advanced Researches of Plant Lipids (Murata, N., Yamada, M., Nishida, I., Okuyama, H., Sekiya, J. and Wada, H., eds). Dordrecht, The Netherlands: Kluwer Academic Publishers, (in press).
39. Schenk, P.M., Kazan, K., Wilson, I., Anderson, J.P., Richmond, T., Somerville, S.C. and Manners, J.M. (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc. Natl. Acad. Sci. USA, 97, 11655-11660.
40. Smith, F.W., Hawkesford, M.J., Ealing, P.M., Clarkson, D.T., Vanden Berg, P.J., Belcher, A.R. and Warrilow, A.G.S. (1997) Regulation of expression of a cDNA from barley roots encoding a high affinity sulphate transporter. Plant J. 12, 875-884.
41. Spremulli, L. (2000) Protein synthesis, assembly, and degradation. In Biochemistry and Molecular Biology of Plants (Buchanan, B., Gruissen, W. and Jones, R., eds). Rockville, MD, USA: American Society of Plant Physiologists, pp. 412-454.
42. Takahashi, H., Braby, C.E. and Grossman, A.R. (2001) Sulfur economy and cell wall biosynthesis during sulfur limitation of Chlamydomonas reinhardtii. Plant Physiol. 127, 665-673.
43. 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.
44. Takahashi, H.,Yamazaki,M., Sasakura, N., Watanabe, A., Leustek, T., de Englar, J.A., Englar, G., Van Montagu, M. and Saito, K. (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. USA, 94, 11102-11107.
45. Tusher, V.G., Tibshiriani, R. and Chu, G. (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. USA, 98, 5116-5121(First Published April 17, 2001; 10.1073/pnas.091062498).
46. Vauclare, P., Kopriva, S., Fell, D., Suter, M., Sticher, L., von Ballmoos, P., Krähenbühl, U., Op den Camp, R. and Brunold, C. (2002) Flux control of sulphate assimilation in Arabidopsis thaliana: adenosine 5′-phosphosulphate reductase is more susceptible than ATP sulphurylase to negative control by thiols. Plant J. 31, 729-740.
47. Vidmar, J.J., Schjoerring, J.K., Touraine, B. and Glass, A.D.M. (1999) Regulation of the hvst1 gene encoding a high-affinity sulfate transporter from Hordeum vulgare. Plant Mol. Biol. 40, 883-892.
48. Vidmar, J.J., Tagmount, A., Cathala, N., Touraine, B. and Davidian, J.-C.E. (2000) Cloning and characterization of a root specific high-affinity sulfate transporter from Arabidopsis thaliana. FEBS Lett. 475, 65-69.
49. Wykoff, D.D., Davies, J.P., Melis, A. and Grossman, A.R. (1998) The regulation of photosynthetic electron transport during nutrient deprivation in Chlamydomonas reinhardtii. Plant Physiol. 117, 129-139.
50. Xie, D.-X., Feys, B.F., James, S., Nieto-Rostro, M. and Turner, J.G. (1998) COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science, 280, 1091-1094.
51. COI1 ubiquitin-ligase complexes are required for jasmonate response in Arabidopsis. Plant Cell, 14, 1919-1935.
52. 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.