A novel regulatory pathway of sulfate uptake in Arabidopsis roots: Implication of CRE1/WOL/AHK4-mediated cytokinin-dependent regulation

Plant Journal

Volumn 38, Issue 5, 2004, Pages 779-789

  Maruyama Nakashita, Akiko ^a   Nakamura, Yumiko ^a   Yamaya, Tomoyuki ^a,b   Takahashi, Hideki ^a  

^a RIKEN Center for Sustainable Resource Science   (Japan)

^b TOHOKU UNIVERSITY   (Japan)

Author keywords

Arabidopsis; Cytokinin; Sulfate transporter; Sulfate uptake; Sulfur assimilation

Indexed keywords

FLUORESCENCE; GENETIC ENGINEERING; GREENHOUSES; HORMONES; PLANT CELL CULTURE; PROTEINS; RNA;

CYTOKININ; PLANT CELL DIVISION; SULFUR ACQUISITION;

PLANTS (BOTANY);

ARABIDOPSIS PROTEIN; CELL SURFACE RECEPTOR; CYTOKININ; GREEN FLUORESCENT PROTEIN; INDOLEACETIC ACID DERIVATIVE; PHOTOPROTEIN; PHYTOHORMONE; PRIMER DNA; PROTEIN HISTIDINE KINASE; PROTEIN KINASE; PROTEIN-HISTIDINE KINASE; SULFATE; WOL PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; ARTICLE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PLANT ROOT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSGENIC PLANT; TRANSPORT AT THE CELLULAR LEVEL;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASE SEQUENCE; BIOLOGICAL TRANSPORT; CYTOKININS; DNA PRIMERS; GENE EXPRESSION REGULATION, PLANT; GREEN FLUORESCENT PROTEINS; INDOLEACETIC ACIDS; LUMINESCENT PROTEINS; PLANT GROWTH REGULATORS; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; PROTEIN KINASES; RECEPTORS, CELL SURFACE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SULFATES;

ARABIDOPSIS;

EID: 2542568102     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2004.02079.x     Document Type: Article

References (55)

1. Chiu, W.L., Niwa, Y., Zeng, W., Hirano, T., Kobayashi, H. and Sheen, J. (1996) Engineered GFP as a vital reporter in plants. Curr. Biol. 6, 325-330.
2. Clough, S.J. and Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
3. Collier, M.D., Fotelli, M.N., Nahm, M., Kopriva, S., Rennenberg, H., Hanke, D.E. and Geßler, A. (2003) Regulation of nitrogen uptake by Fagus sylvatica on a whole plant level - interactions between cytokinins and soluble N compounds. Plant Cell Environ. 26, 1549-1560.
4. Franco-Zorrilla, J.M., Martin, A.C., Solano, R., Rubio, V., Leyva, A. and Paz-Ares, J. (2002) Mutations at CRE1 impair cytokinin-induced repression of phosphate starvation responses in Arabidopsis. Plant J. 32, 353-360.
5. 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.
6. Haberer, G. and Kieber, J.J. (2001) Cytokinins: new insights into a classic phytohormone. Plant Physiol. 128, 354-362.
7. 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.
8. Hirai, M.Y., Fujiwara, T., Awazuhara, M., Kimura, Y., 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.
9. Höfgen, R. and Willmitzer, L. (1988) Storage of competent cells for Agrobacterium transformation. Nucl. Acids Res. 16, 9877.
10. Honda, C., Fujiwara, T. and Chino, M. (1998) Sulfate uptake in Arabidopsis thaliana. J. Plant Nutr. 21, 601-614.
11. Horgan, J.M. and Wareing, P.F. (1980) Cytokinins and the growth responses of seedlings of Betula pendula Roth. & Acer pseudoplatanus L. to nitrogen and phosphorus deficiency. J. Exp. Bot. 31, 525-532.
12. Hutchinson, C.E. and Kieber, J.J. (2002) Cytokinin signaling in Arabidopsis. Plant Cell, 14, S47-S59.
13. Hwang, I. and Sheen, J. (2001) Two-component circuitry in Arabidopsis signal transduction. Nature, 413, 383-389.
14. Inaba, K., Fujiwara, T., Hayashi, H., Chino, M., Komeda, Y. and Naito, S. (1994) Isolation of an Arabidopsis thaliana mutant, mto1, that overaccumulates soluble methionine: temporal and spatial patterns of soluble methionine accumulation. Plant Physiol. 104, 881-887.
15. Inoue, T., Higuchi, M., Hashimoto, Y., Seki, M., Kobayashi, M., Kato, T., Tabata, S., Shinozaki, K. and Kakimoto, T. (2001) Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature, 409, 1060-1063.
16. Kakimoto, T. (2003) Perception and signal transduction of cytokinins. Annu. Rev. Plant Biol. 54, 605-627.
17. Karthikeyan, A.S., Varadarajan, D.K., Mukatira, U.T., D'Urzo, M.P., Damsz, B. and Raghothama, K.G. (2002) Regulated expression of Arabidopsis phosphate transporters. Plant Physiol. 130, 221-233.
18. 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 a soybean seed storage-protein gene by sulfur and nitrogen nutrition. Planta, 209, 282-289.
19. Koncz, C. and Schell, J. (1986) The promoter of T-DNA gene 5 controls the tissue-specific expression of chimaeric genes carried by a novel types of Agrobacterium binary vector. Mol. Gen. Genet. 204, 383-396.
20. Kopriva, S., Muheim, R., Koprivova, A., Trachsel, N., Catalano, C., Suter, M. and Brunold, C. (1999) Light regulation of assimilatory sulphate reduction in Arabidopsis thaliana. Plant J. 20, 37-44.
21. Koprivova, A., Suter, M., Op den Camp, R., Brunold, C. and Kopriva, S. (2000) Regulation of sulfur assimilation by nitrogen in Arabidopsis. Plant Physiol. 122, 737-746.
22. Kutz, A., Muller, 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.
23. 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.
24. Lejay, L., Gansel, X., Cerezo, M., Tillard, P., Müller, C., Krapp, A., von Wirén, N., Daniel-Vedele, F. and Gojon, A. (2003) Regulation of root ion transporters by photosynthesis: functional importance and relation with hexokinase. Plant Cell, 15, 2218-2232.
25. Leustek, T. and Saito, K. (1999) Sulfate transport and assimilation in plants. Plant Physiol. 120, 637-643.
26. Leustek, T., Martin, M.N., Bick, J. and Davies, J.P. (2000) Pathways and regulation of sulfur metabolism revealed through molecular genetic studies. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51, 141-166.
27. Mähönen, A.P., Bonke, M., Kauppinen, L., Riikonen, M., Benfey, P.N. and Helariutta, Y. (2000) A novel two-component hybrid molecule regulates vascular morphogenesis of the Arabidopsis root. Genes Dev. 14, 2938-2943.
28. Martin, A.C., del Pozo, J.C., Iglesias, J., Rubio, V., Solano, R., de la Pena, A., Leyva, A. and Paz-Ares, J. (2000) Influence of cytokinins on the expression of phosphate starvation responsive genes in Arabidopsis. Plant J. 24, 559-567.
29. Maruyama-Nakashita, A., Inoue, E., Watanabe-Takahashi, A., Yamaya, T. and Takahashi, H. (2003) Transcriptome profiling of sulfur responsive genes in Arabidopsis reveals global effects of sulfur nutrition on multiple metabolic pathways. Plant Physiol. 132, 597-605.
30. Mizuno, T. (1998) His-Asp phosphotransfer signal transduction. J. Biochem. (Tokyo), 123, 555-563.
31. Mok, D.W. and Mok, M.C. (2001) Cytokinin metabolism and action. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 89-118.
32. 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 to abscisic acid mutations. Plant Physiol. 104, 497-503.
33. 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.
34. Ohkama, N., Takei, K., Sakakibara, H., Hayashi, H., Yoneyama, T. and Fujiwara, T. (2002) Regulation of sulfur-responsive gene expression by exogenously applied cytokinins in Arabidopsis thaliana. Plant Cell Physiol. 43, 1493-1501.
35. Saito, K. (2000) Regulation of sulfate transport and synthesis of sulfur-containing amino acids. Curr. Opin. Plant Biol. 3, 188-195.
36. Sakai, H., Honma, T., Aoyama, T., Sato, S., Kato, T., Tabata, S. and Oka, A. (2001) ARR1, a transcription factor for genes immediately responsive to cytokinins. Science, 294, 1519-1521.
37. Sakakibara, H., Suzuki, M., Takei, K., Deji, A., Taniguchi, M. and Sugiyama, T. (1998) A response regulator homologue passively involved in nitrogen signal transduction mediated by cytokinin in maize. Plant J. 14, 337-344.
38. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning: a Laboratory Manual, 2nd edn. New York, USA: Cold Spring Harbor Laboratory Press.
39. Schmülling, T. (2001) CREam of cytokinin signaling: receptor identified. Trends Plant Sci. 6, 281-284.
40. 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.
41. 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.
42. 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 sulfate transporter. Plant J. 12, 875-884.
43. Suzuki, T., Miwa, K., Ishikawa, K., Yamada, H., Aiba, H. and Mizuno, T. (2001) The Arabidopsis sensor His-kinase, AHK4, can respond to cytokinin. Plant Cell Physiol. 42, 107-113.
44. Takahashi, H., Yamazaki, M., Sasakura, N., Watanabe, A., Leustek, T., de Almeida Engler, J., Engler, 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. Takahashi, H., Watanabe-Takahashi, A., Smith, F.W., Blake-Kalff, M., Hawkesford, M.J. and Saito, K. (2000) The roles of three functional sulfate transporters involved in uptake and translocation of sulfate in Arabidopsis thaliana. Plant J. 23, 171-182.
46. Takei, K., Sakakibara, H., Taniguchi, M. and Sugiyama, T. (2001) Nitrogen-dependent accumulation of cytokinins in root and the translocation to leaf: implication of cytokinin species that induces gene expression of maize response regulator. Plant Cell Physiol. 42, 85-93.
47. Taniguchi, M., Kiba, T., Sakakibara, H., Ueguchi, C., Mizuno, T. and Sugiyama, T. (1998) Expression of Arabidopsis response regulator homologs is induced by cytokinins and nitrate. FEBS Lett. 429, 259-262.
48. Valvekens, D., Van Montagu, M. and Van Lijsebettens, M. (1988) Agrobacterium-mediated transformation of Arabidopsis thaliana root explants by using kanamycin selection. Proc. Natl. Acad. Sci. USA, 85, 5536-5540.
49. 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.
50. 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.
51. 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.
52. Wagner, B.M. and Beck, E. (1993) Cytokinins in the perennial herb Urtica dioica L. as influenced by its nitrogen status. Planta, 190, 511-518.
53. Wang, R., Okamoto, M., Xing, X. and Crawford, N. (2003) Microarray analysis of the nitrate response in Arabidopsis roots and shoots reveals over 1,000 rapidly responding genes and new linkages to glucose, trehalose-6- phosphate, iron, and sulfate metabolism. Plant Physiol. 132, 556-567.
54. 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.
55. 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.