Evidence for autoregulation of cystathionine -γ-synthase mRNA stability in Arabidopsis

Science

Volumn 286, Issue 5443, 1999, Pages 1371-1374

  Chiba, Yukako ^a   Ishikawa, Mari ^a   Kijima, Fumiko ^a,d   Huw Tyson, R ^b   Kim, Jungsup ^c   Yamamoto, Ayako ^a,e   Nambara, Eiji ^a   Leustek, Thomas ^c   Wallsgrove, Roger M ^b   Naito, Satoshi ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b IACR Rothamsted   (United Kingdom)

^c RUTGERS UNIVERSITY   (United States)

^d Fukujuen CHA Research Center   (Japan)

^e UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTATHIONINE; MESSENGER RNA; METHIONINE; SYNTHETASE;

AMINO ACID SEQUENCE; AMINO ACID SYNTHESIS; ARABIDOPSIS; ARTICLE; AUTOREGULATION; CONTROLLED STUDY; ENZYME REGULATION; FEEDBACK SYSTEM; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENETIC STABILITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL;

AMINO ACID SEQUENCE; ARABIDOPSIS; CARBON-OXYGEN LYASES; EXONS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENES, REPORTER; KINETICS; METHIONINE; MOLECULAR SEQUENCE DATA; MUTATION; RNA, MESSENGER; SEQUENCE ALIGNMENT; TRANSCRIPTION, GENETIC; TRANSFECTION;

EID: 0032696044     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.286.5443.1371     Document Type: Article

References (43)

1. C. Yanofsky, Nature 289, 751 (1981).
2. K. T. Arndt, C. Styles, G. R. Fink, Science 237, 874 (1987).
3. R. L. Last and G. R. Fink, Science 240, 305 (1988); A. B. Rose and R. L. Last, Plant J. 11, 455 (1997).
4. R. L. Last and G. R. Fink, Science 240, 305 (1988); A. B. Rose and R. L. Last, Plant J. 11, 455 (1997).
5. K. Inaba et al., Plant Physiol. 104, 881 (1994).
6. J. Giovanelli, in Sulfur Nutrition and Sulfur Assimilation in Higher Plants, H. Rennenberg, C. Brunold, L. J. De Kok, I. Stulen, Eds. (SLPB Academic, The Hague, 1990), pp. 33-48; S. Ravanel, B. Gakière, D. Job, R. Douce, Proc. Natl. Acad. Sci. U.S.A. 95, 7805 (1998); B. F. Matthews, in Plant Amino Acids, B. K. Singh Ed. (Dekker, New York, 1999), pp. 205-225.
7. J. Giovanelli, in Sulfur Nutrition and Sulfur Assimilation in Higher Plants, H. Rennenberg, C. Brunold, L. J. De Kok, I. Stulen, Eds. (SLPB Academic, The Hague, 1990), pp. 33-48; S. Ravanel, B. Gakière, D. Job, R. Douce, Proc. Natl. Acad. Sci. U.S.A. 95, 7805 (1998); B. F. Matthews, in Plant Amino Acids, B. K. Singh Ed. (Dekker, New York, 1999), pp. 205-225.
8. J. Giovanelli, in Sulfur Nutrition and Sulfur Assimilation in Higher Plants, H. Rennenberg, C. Brunold, L. J. De Kok, I. Stulen, Eds. (SLPB Academic, The Hague, 1990), pp. 33-48; S. Ravanel, B. Gakière, D. Job, R. Douce, Proc. Natl. Acad. Sci. U.S.A. 95, 7805 (1998); B. F. Matthews, in Plant Amino Acids, B. K. Singh Ed. (Dekker, New York, 1999), pp. 205-225.
9. A. H. Datko, S. H. Mudd, J. Giovanelli, P. K. MacNicol, Plant Physiol. 62, 629 (1978).
10. G. A. Thompson, A. H. Datko, S. H. Mudd, J. Giovanelli, Plant Physiol. 69, 1077 (1982); S. E. Rognes, R. M. Wallsgrove, J. S. H. Kueh, S. W. J. Bright, Plant Sci. 43, 45 (1986).
11. G. A. Thompson, A. H. Datko, S. H. Mudd, J. Giovanelli, Plant Physiol. 69, 1077 (1982); S. E. Rognes, R. M. Wallsgrove, J. S. H. Kueh, S. W. J. Bright, Plant Sci. 43, 45 (1986).
12. -1.
13. Because of the difference in experimental systems, some inconsistencies in dose response were apparent. The response to Met in calli seems to be less significant than in whole plants or electroporated protoplasts. This may result from a difference in the ability to take up Met. Also, the truncated RNA was hardly visible in whole plant samples, possibly because such RNA is more labile in whole plants than in calli.
14. Y. Chiba, M. Ishikawa, S. Naito, unpublished result.
15. T. C. Newman, M. Ohme-Takagi, C. B. Taylor, P. J. Green, Plant Cell 5, 701 (1993).
16. At 24 hours after ActD treatment, the quantities of CGS mRNA in the absence of Met were reduced to about 30% and 60%, in wild-type and mto1-1 mutant, respectively. These values in the presence of Met were about 15% and 60% for wild-type and mto1-1 mutant, respectively.
17. Mapping with simple sequence length polymorphism (SSLP) markers [C. J. Bell and J. R. Ecker, Genomics 19, 137 (1994)] located the mto1 mutation about 3 centimorgans (cM) north of nga172, which is at 6.83 cM on chromosome 3 (http://nasc.nott.ac.uk/new_ ri_map.html). In this regard, the gene order in the previous report (4) is corrected to mto1-hy2-abi3. The CGS gene was mapped about 4 cM north of nga172 (22).
18. We amplified a 6551-base pair region covering the CGS gene from the mto1-1 mutant by polymerase chain reaction (PCR) and compared the nucleotide sequence of the amplified DNA with the wild-type sequence (GenBank database accession no. AB010888). The primers were designed after the wild-type sequence. Sequencing was carried out with an ABI PRISM dye terminator cycle sequencing kit and model 377 DNA sequencer (Perkin-Elmer). Additional alleles of mtol mutants were isolated as described in (4), and mto1-2 through mto1-5, which are independent of each other, were used for further study after they were back-crossed three times to wild type. Because the mto1 mutation is semidominant over wild type (4), complementation tests were not applicable. Mapping with a SSLP-type marker in the 5′-upstream region of CGS (22) indicated that they all mapped within a few centimorgans from mto1-1. These mutants were sequenced for the exon 1 region.
19. The CGS gene has 11 exons encoding 563 amino acids (23).
20. The level of CGS mRNA in mto1-4 mutant plants was lower than in other mto1 mutants (10), which suggests that the mto1-4 mutation is leaky. The fact that the reporter activity of the mto1-4 mutant construct in the presence of Met was also lower than that of the mto1-1 mutant construct supports the idea that the reporter activity reflects the response to Met at the mRNA level.
21. The first four amino acids were included to provide the same context for the translational start site as the other constructs.
22. The MTO1 region is not necessary for enzyme activity (23).
23. Although CGS is transported to chloroplasts (24), synthesis of Met and most of its direct metabolites occurs in the cytosol (5, 24).
24. T. J. Yen, P. S. Machlin, D. W. Cleveland, Nature 334, 580 (1988); N. G. Theodorakis and D. W. Cleveland, in Control of Messenger RNA Stability, J. Belasco and G. Brawerman, Eds. (Academic Press, San Diego, CA, 1993), pp. 219-238.
25. T. J. Yen, P. S. Machlin, D. W. Cleveland, Nature 334, 580 (1988); N. G. Theodorakis and D. W. Cleveland, in Control of Messenger RNA Stability, J. Belasco and G. Brawerman, Eds. (Academic Press, San Diego, CA, 1993), pp. 219-238.
26. M. Ishikawa, S. Naito, T. Ohno, J. Virol. 67, 5328 (1993); M. Yoshii, N. Yoshioka, M. Ishikawa, S. Naito, J. Virol. 72, 8731 (1998).
27. M. Ishikawa, S. Naito, T. Ohno, J. Virol. 67, 5328 (1993); M. Yoshii, N. Yoshioka, M. Ishikawa, S. Naito, J. Virol. 72, 8731 (1998).
28. J. Kim, Y. Chiba, A. Yamamoto, S. Naito, T. Leustek, Plant Physiol. 120, 635 (1999).
29. J. Kim and T. Leustek, Plant Mol. Biol. 32, 1117 (1996).
30. R. M. Wallsgrove, P. J. Lea, B. J. Miflin, Plant Physiol. 71, 780 (1983).
31. S. Ravanel, B. Gakière, D. Job, R. Douce, Biochem. J. 331, 639 (1998).
32. J. Sambrook, E. F. Fritsch, T. Maniatis, Molecular Cloning: A Laboratory Manual (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, ed. 2, 1989).
33. Plants were cultured as described in S. Naito et al. [Plant Physiol. 104, 497 (1994)]. Application of Met to plants was as described in M. Y. Hirai et al. [Plant Cell Physiol. 35, 927 (1994)] except that the treatment was started 12 days after sowing.
34. Plants were cultured as described in S. Naito et al. [Plant Physiol. 104, 497 (1994)]. Application of Met to plants was as described in M. Y. Hirai et al. [Plant Cell Physiol. 35, 927 (1994)] except that the treatment was started 12 days after sowing.
35. 32P-labeled probes were prepared with a multi-prime DNA labeling system (Amersham).
36. 32P-labeled probes were prepared with a multi-prime DNA labeling system (Amersham).
37. We determined CGS activity by phosphate release as described in (25) except that Mops replaced Tricine in the extraction buffer and the assay mixture contained 2 mM cysteine and 6 mM O-phosphohomoserine.
38. -1, respectively. Reporter activities were determined as described [Y. Sakata et al., Biosci. Biotech. Biochem. 58, 2104 (1994)].
39. + carries the firefly luciferase (LUC) gene under control of the CaMV 35S RNA promoter (K. Hiratsuka, personal communication). To obtain plasmids carrying the LUC reporter, we excised the LUC coding region from pT3/T7-LUC (Clontech, Palo Alto, CA) by Bsm I and Sac I digestion and ligated it with Xba I- and Sac I-digested pTF33 along with exon 1 DNA. The exon 1 sequences were verified by sequencing.
40. + carries the firefly luciferase (LUC) gene under control of the CaMV 35S RNA promoter (K. Hiratsuka, personal communication). To obtain plasmids carrying the LUC reporter, we excised the LUC coding region from pT3/T7-LUC (Clontech, Palo Alto, CA) by Bsm I and Sac I digestion and ligated it with Xba I- and Sac I-digested pTF33 along with exon 1 DNA. The exon 1 sequences were verified by sequencing.
41. + carries the firefly luciferase (LUC) gene under control of the CaMV 35S RNA promoter (K. Hiratsuka, personal communication). To obtain plasmids carrying the LUC reporter, we excised the LUC coding region from pT3/T7-LUC (Clontech, Palo Alto, CA) by Bsm I and Sac I digestion and ligated it with Xba I- and Sac I-digested pTF33 along with exon 1 DNA. The exon 1 sequences were verified by sequencing.
42. J. D. Thompson, D. G. Higgins, T. J. Gibson, Nucleic Acids Res. 22, 4673 (1994); http://www.genome. ad.jp/SIT/CLUSTALW.html. The gap open penalty was set at 3.
43. Supported in part by Grants-in-aid for Scientific Research from Ministry of Education, Science, Sports and Culture, Japan, to S.N. (grants 06278102, 09440262, and 11440230) and for JSPS Fellows to Y.C. (grant 0943), by the Special Coordination Fund from Science and Technology Agency, Japan, to S.N., by a grant from the U.S. National Science Foundation to T.L. (grant MCB9728661), and a RASP grant from the UK Biotechnology and Biological Sciences Research Council (BBSRC) to R.M.W. IACR received a grant-in-aid from BBSRC. Y.C. is a JSP5 Research Fellow. We thank P. McCourt, R. L. Last, and M. Ishikawa for critical reading and D. Bartlem for careful reading of the manuscript; S. Kudo for technical assistance; K. Fujiwara for general assistance; and M. Thomas and K. Hiratsuka for materials. We used the facility of the Biopolymer Analysis Laboratory, Faculty of Agriculture, Hokkaido University.