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

Molecular Plant

Volumn 3, Issue 2, 2010, Pages 347-360

  Lewandowska, Małgorzata ^a   Wawrzyńska, Anna ^a   Moniuszko, Grzegorz ^a   Łukomska, Jolanta ^a   Zientara, Katarzyna ^a   Piecho, Marta ^a   Hodurek, Paweł ^a   Zhukov, Igor ^a,b   Liszewska, Frantz ^a   Nikiforova, Victoria ^c,d   Sirko, Agnieszka ^a  

^a INSTITUTE OF BIOCHEMISTRY AND BIOPHYSICS   (Poland)

^b NATIONAL INSTITUTE OF CHEMISTRY   (Slovenia)

^c MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^d TIMIRYAZEV INSTITUTE OF PLANT PHYSIOLOGY   (Russian Federation)

Author keywords

Arabidopsis; Gene expression; Sulfate assimilation; Sulfur deficit; Tobacco; Transcription regulators

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; NICOTIANA OBTUSIFOLIA; NICOTIANA TABACUM;

EID: 77950255670     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1093/mp/ssq007     Document Type: Article

References (50)

1. Andrade, M.A., Chacon, P., Merelo, J.J., and Moran, F. (1993). Evaluation of secondary structure of proteins from UV circular dichroism spectra using an unsupervised learning neural network. Protein Eng. 6, 383-390.
2. Becher, M., Talke, I.N., Krall, L., and Kramer, U. (2004). Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri. Plant J. 37, 251-268.
3. Carrington, J.C., Freed, D.D., and Leinicke, A.J. (1991). Bipartite signal sequence mediates nuclear translocation of the plant potyviral NIa protein. Plant Cell. 3, 953-962.
4. Chico, J.M., Chini, A., Fonseca, S., and Solano, R. (2008). JAZ repressors set the rhythm in jasmonate signaling. Curr. Opin. Plant Biol. 11, 486-494.
5. Chintapakorn, Y., and Hamill, J.D. (2003). Antisense-mediated down-regulation of putrescine N-methyltransferase activity in transgenic Nicotiana tabacum L. can lead to elevated levels of anatabine at the expense of nicotine. Plant Mol. Biol. 53, 87-105.
6. Combet, C., Blanchet, C., Geourjon, C., and Deleage, G. (2000). NPS@: network protein sequence analysis. Trends Biochem. Sci. 25, 147-150.
7. 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.
8. Ellman, G.L. (1959). Tissue sulfhydryl groups. Arch Biochem Biophys. 82, 70-77.
9. Falquet, L., Pagni, M., Bucher, P., Hulo, N., Sigrist, C.J., Hofmann, K., and Bairoch, A. (2002). The PROSITE database, its status in 2002. Nucleic Acids Res. 30, 235-238.
10. Halitschke, R., and Baldwin, I.T. (2003). Antisense LOX expression increases herbivore performance by decreasing defense responses and inhibiting growth-related transcriptional reorganization in Nicotiana attenuata. Plant J. 36, 794-807.
11. Haneklaus, S., Kerr, C.W., and Schnug, E. (2005). A chronicle of sulfur research in agriculture. In Sulfur Transport and Assimilation in Plants in the Post Genomic Era, Saito, K.,et al.,eds (Leiden, The Netherlands: Backhuys Publishers), pp. 249-256.
12. Hellens, R.P., Edwards, E.A., Leyland, N.R., Bean, S., and Mullineaux, P.M. (2000). pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation. Plant Mol. Biol. 42, 819-832.
13. 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-Lserine as a general regulator of gene expression in response to sulfur nutrition. Plant J. 33, 651-663.
14. Horton, P., and Nakai, K. (1997). Better prediction of protein cellular localization sites with the k nearest neighbors classifier. Proc. Int. Conf. Intell. Syst. Mol. Biol. 5, 147-152.
15. Kanyuka, K., Praekelt, U., Franklin, K.A., Billingham, O.E., Hooley, R., Whitelam, G.C., and Halliday, K.J. (2003). Mutations in the huge Arabidopsis gene BIG affect a range of hormone and light responses. Plant J. 35, 57-70.
16. Karimi, M., De Meyer, B., and Hilson, P. (2005). Modular cloning in plant cells. Trends Plant Sci. 10, 103-105.
17. Kasajima, I., Ohkama-Ohtsu, N., Ide, Y., Hayashi, H., Yoneyama, T., Suzuki, Y., Naito, S., and Fujiwara, T. (2007). The BIG gene is involved in regulation of sulfur deficiency-responsive genes in Arabidopsis thaliana. Physiol. Plant. 129, 351-363.
18. Katoh, K., Kuma, K., Toh, H., and Miyata, T. (2005). MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 33, 511-518.
19. Kopriva, S., Suter, M., von Ballmoos, P., Hesse, H., Krähenbü hl, U., Rennenberg, H., and Brunold, C. (2002). Interaction of sulfate assimilation with carbon and nitrogen metabolism in Lemna minor. Plant Physiol. 130, 1406-1413.
20. Legg, P.D., Collins, G.B., and Litton, C.C. (1970). Registration of LA Burley 21 tobacco germplasm. Crop Sci. 10, 212.
21. Letunic, I., Copley, R.R., Schmidt, S., Ciccarelli, F.D., Doerks, T., Schultz, J., Ponting, C.P., and Bork, P. (2004). SMART 4.0: towards genomic data integration. Nucleic Acids Res. 32, D142-D144.
22. Lewandowska, M., and Sirko, A. (2008). Recent advances in understanding plant response to sulfur-deficiency stress. Acta Biochim. Polon. 55, 457-471.
23. Lewandowska, M., Wawrzynska, A., Kaminska, J., Liszewska, F., and Sirko, A. (2005). Identification of novel proteins of Nicotiana tabacum regulated by short term sulfur starvation. In Sulfur Transport and Assimilation in Plants in the Post Genomic Era, Saito,K.,et al., eds (Leiden, The Netherlands: Backhuys Publishers), pp. 153-156.
24. Lin, Z., Zhong, S., and Grierson, D. (2009). Recent advances in ethylene research. J. Exp. Bot. 60, 3311-3336.
25. Lopez-Bucio, J., Hernandez-Abreu, E., Sanchez-Calderon, L., Perez- Torres, A., Rampey, R.A., Bartel, B., and Herrera-Estrella, L. (2005). An auxin transport independent pathway is involved in phosphate stress-induced root architectural alterations in Arabidopsis: identification of BIG as a mediator of auxin in pericycle cell activation. Plant Physiol. 137, 681-691.
26. 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.
27. 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. Plant Cell. 18, 3235-3251.
28. 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.
29. Migge, A., Bork, C., Hell, R., and Becker, T.W. (2000). Negative regulation of nitrate reductase gene expression by glutamine or asparagine accumulating in leaves of sulfur-deprived tobacco. Planta. 211, 587-595.
30. Murashige, T., and Skoog, F. (1962). A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol. Plant. 15, 473-493.
31. Muttucumaru, N., Halford, N.G., Elmore, J.S., Dodson, A.T., Parry, M., Shewry, P.R., and Mottram, D.S. (2006). Formation of high levels of acrylamide during the processing of flour derived from sulfate-deprived wheat. J. Agric. Food Chem. 54, 8951-8955.
32. Nikiforova, V., Freitag, J., Kempa, S., Adamik, M., Hesse, H., and Hoefgen, R. (2003). Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: interlacing of biosynthetic pathways provides response specificity. Plant J. 33, 633-650.
33. Nikiforova, V.J., Daub, C.O., Hesse, H., Willmitzer, L., and Hoefgen, R. (2005). Integrative gene-metabolite network with implemented causality deciphers informational fluxes of sulphur stress response. J. Exp. Bot. 56, 1887-1896.
34. Parry, D.A., Fraser, R.D., and Squire, J.M. (2008). Fifty years of coiledcoils and alpha-helical bundles: a close relationship between sequence and structure. J. Struct. Biol. 163, 258-269.
35. Petrucco, S., Bolchi, A., Foroni, C., Percudani, R., Rossi, G.L., and Ottonello, S. (1996). A maize gene encoding an NADPH binding enzyme highly homologous to isoflavone reductases is activated in response to sulfur starvation. Plant Cell. 8, 69-80.
36. Prosser, I.M., Purves, J.V., Saker, L.R., and Clarkson, D.T. (2001). Rapid disruption of nitrogen metabolism and nitrate transport in spinach plants deprived of sulphate. J. Exp. Bot. 52, 113-121.
37. Queval, G., Thominet, D., Vanacker, H., Miginiac-Maslow, M., Gakiere, B., and Noctor, G. (2009). H2O2-activated up-regulation of glutathione in Arabidopsis involves induction of genes encoding enzymes involved in cysteine synthesis in the chloroplast. Mol. Plant. 2, 344-356.
38. Sambrook, J., Frisch, E.F., and Maniattis, T. (1989). Molecular Cloning: A Laboratory Manual (Cold Spring Harbor: Cold Spring Harbor Laboratory Press).
39. Scherer, H.W. (2001). Sulphur in crop production-invited paper. Eur. J. Agron. 14, 81-111.
40. Schnug, E., Ernst, W.H.O., Kraztz, S., Knolle, F., and Haneklaus, S. (2004). Aspects of ecotoxicology of sulphur in the Harz region-a guided excursion. Landbauforschung Voelkenrode. 54, 129-143.
41. Siritunga, D., and Sayre, R.T. (2003). Generation of cyanogen-free transgenic cassava. Planta. 217, 367-373.
42. Sponsel, V.M., Schmidt, F.W., Porter, S.G., Nakayama, M., Kohlstruk, S., and Estelle, M. (1997). Characterization of new gibberellin-responsive semidwarf mutants of Arabidopsis. Plant Physiol. 115, 1009-1020.
43. Volkov, R.A., Borisjuk, N.V., Panchuk, I.I., Schweizer, D., and Hemleben, V. (1999). Elimination and rearrangement of parental rDNA in the allotetraploid Nicotiana tabacum. Mol. Biol. Evol. 16, 311-320.
44. Wawrzynski, A., Kopera, E.,Wawrzynska, A., Kaminska, J., Bal,W., and Sirko, A. (2006). Effects of simultaneous expression of heterologous genes involved in phytochelatin biosynthesis on thiol content and cadmium accumulation in tobacco plants. J. Exp. Bot. 57, 2173-2182.
45. Wawrzynska, A., Lewandowska, M., and Sirko, A. (2009). Nicotiana tabacum EIL2 directly regulates expression of at least one tobacco gene induced by sulphur starvation. J. Exp. Bot. doi: 10.1093/jxb/erp356.
46. Wawrzynska, A., Lewandowska, M., Hawkesford, M.J., and Sirko, A. (2005). Using a suppression subtractive library-based approach to identify tobacco genes regulated in response to short-term sulphur deficit. J. Exp. Bot. 56, 1575-1590.
47. Williams, J.S., Hall, S.A., Hawkesford, M.J., Beale, M.H., and Cooper, R.M. (2002). Elemental sulfur and thiol accumulation in tomato and defense against a fungal vascular pathogen. Plant Physiol. 128, 150-159.
48. Wolf, E., Kim, P.S., and Berger, B. (1997). MultiCoil: a program for predicting two- and three-stranded coiled coils. Protein Sci. 6, 1179-1189.
49. Yang, J.T., Wu, C.S., and Martinez, H.M. (1986). Calculation of protein conformation from circular dichroism. Methods Enzymol. 130, 208-269.
50. Zimmermann, P., Hirsch-Hoffmann, M., Hennig, L., and Gruissem, W. (2004). GENEVESTIGATOR: Arabidopsis microarray database and analysis toolbox. Plant Physiol. 136, 2621-2632.