Abstract
All flowering plants produce S-methylmethionine (SMM) from Met and have a separate mechanism to convert SMM back to Met. The functions of SMM and the reasons for its interconversion with Met are not known. In this study, by using the aphid stylet collection method together with mass spectral and radiolabeling analyses, we established that l-SMM is a major constituent of the phloem sap moving to wheat ears. The SMM level in the phloem ( approximately 2% of free amino acids) was 1.5-fold that of glutathione, indicating that SMM could contribute approximately half the sulfur needed for grain protein synthesis. Similarly, l-SMM was a prominently labeled product in phloem exudates obtained by EDTA treatment of detached leaves from plants of the Poaceae, Fabaceae, Asteraceae, Brassicaceae, and Cucurbitaceae that were given l-(35)S-Met. cDNA clones for the enzyme that catalyzes SMM synthesis (S-adenosylMet:Met S-methyltransferase; EC 2.1.1.12) were isolated from Wollastonia biflora, maize, and Arabidopsis. The deduced amino acid sequences revealed the expected methyltransferase domain ( approximately 300 residues at the N terminus), plus an 800-residue C-terminal region sharing significant similarity with aminotransferases and other pyridoxal 5'-phosphate-dependent enzymes. These results indicate that SMM has a previously unrecognized but often major role in sulfur transport in flowering plants and that evolution of SMM synthesis in this group involved a gene fusion event. The resulting bipartite enzyme is unlike any other known methyltransferase.
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- Abraham D. G., Cooper A. J. Cloning and expression of a rat kidney cytosolic glutamine transaminase K that has strong sequence homology to kynurenine pyruvate aminotransferase. Arch Biochem Biophys. 1996 Nov 15;335(2):311–320. doi: 10.1006/abbi.1996.0512. [DOI] [PubMed] [Google Scholar]
- Alexander F. W., Sandmeier E., Mehta P. K., Christen P. Evolutionary relationships among pyridoxal-5'-phosphate-dependent enzymes. Regio-specific alpha, beta and gamma families. Eur J Biochem. 1994 Feb 1;219(3):953–960. doi: 10.1111/j.1432-1033.1994.tb18577.x. [DOI] [PubMed] [Google Scholar]
- Altschul S. F., Madden T. L., Schäffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997 Sep 1;25(17):3389–3402. doi: 10.1093/nar/25.17.3389. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Balaghi M., Horne D. W., Wagner C. Hepatic one-carbon metabolism in early folate deficiency in rats. Biochem J. 1993 Apr 1;291(Pt 1):145–149. doi: 10.1042/bj2910145. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
- Chen L., Bush D. R. LHT1, a lysine- and histidine-specific amino acid transporter in arabidopsis. Plant Physiol. 1997 Nov;115(3):1127–1134. doi: 10.1104/pp.115.3.1127. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Corpet F. Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res. 1988 Nov 25;16(22):10881–10890. doi: 10.1093/nar/16.22.10881. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fisher D. B., Gifford R. M. Accumulation and Conversion of Sugars by Developing Wheat Grains : VI. Gradients Along the Transport Pathway from the Peduncle to the Endosperm Cavity during Grain Filling. Plant Physiol. 1986 Dec;82(4):1024–1030. doi: 10.1104/pp.82.4.1024. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fisher D. B., Macnicol P. K. Amino Acid Composition Along the Transport Pathway during Grain Filling in Wheat. Plant Physiol. 1986 Dec;82(4):1019–1023. doi: 10.1104/pp.82.4.1019. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fisher D. B. Measurement of Phloem transport rates by an indicator-dilution technique. Plant Physiol. 1990 Oct;94(2):455–462. doi: 10.1104/pp.94.2.455. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fisher D. B., Wu Y., Ku M. S. Turnover of soluble proteins in the wheat sieve tube. Plant Physiol. 1992 Nov;100(3):1433–1441. doi: 10.1104/pp.100.3.1433. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fujioka M. Mammalian small molecule methyltransferases: their structural and functional features. Int J Biochem. 1992 Dec;24(12):1917–1924. doi: 10.1016/0020-711x(92)90287-b. [DOI] [PubMed] [Google Scholar]
- Gary J. D., Lin W. J., Yang M. C., Herschman H. R., Clarke S. The predominant protein-arginine methyltransferase from Saccharomyces cerevisiae. J Biol Chem. 1996 May 24;271(21):12585–12594. doi: 10.1074/jbc.271.21.12585. [DOI] [PubMed] [Google Scholar]
- Hanson A. D., Rivoal J., Paquet L., Gage D. A. Biosynthesis of 3-dimethylsulfoniopropionate in Wollastonia biflora (L.) DC. Evidence that S-methylmethionine is an intermediate. Plant Physiol. 1994 May;105(1):103–110. doi: 10.1104/pp.105.1.103. [DOI] [PMC free article] [PubMed] [Google Scholar]
- James F., Nolte K. D., Hanson A. D. Purification and properties of S-adenosyl-L-methionine:L-methionine S-methyltransferase from Wollastonia biflora leaves. J Biol Chem. 1995 Sep 22;270(38):22344–22350. doi: 10.1074/jbc.270.38.22344. [DOI] [PubMed] [Google Scholar]
- Jensen R. A., Gu W. Evolutionary recruitment of biochemically specialized subdivisions of Family I within the protein superfamily of aminotransferases. J Bacteriol. 1996 Apr;178(8):2161–2171. doi: 10.1128/jb.178.8.2161-2171.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Joshi C. P., Chiang V. L. Conserved sequence motifs in plant S-adenosyl-L-methionine-dependent methyltransferases. Plant Mol Biol. 1998 Jul;37(4):663–674. doi: 10.1023/a:1006035210889. [DOI] [PubMed] [Google Scholar]
- Kagan R. M., Clarke S. Widespread occurrence of three sequence motifs in diverse S-adenosylmethionine-dependent methyltransferases suggests a common structure for these enzymes. Arch Biochem Biophys. 1994 May 1;310(2):417–427. doi: 10.1006/abbi.1994.1187. [DOI] [PubMed] [Google Scholar]
- Khan M. A., Eggum B. O. Effect of baking on the nutritive value of Pakistani bread. J Sci Food Agric. 1978 Dec;29(12):1069–1075. doi: 10.1002/jsfa.2740291212. [DOI] [PubMed] [Google Scholar]
- King R. W., Zeevaart J. A. Enhancement of Phloem exudation from cut petioles by chelating agents. Plant Physiol. 1974 Jan;53(1):96–103. doi: 10.1104/pp.53.1.96. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kocsis M. G., Nolte K. D., Rhodes D., Shen T. L., Gage D. A., Hanson A. D. Dimethylsulfoniopropionate biosynthesis in Spartina alterniflora1. Evidence that S-methylmethionine and dimethylsulfoniopropylamine are intermediates. Plant Physiol. 1998 May;117(1):273–281. doi: 10.1104/pp.117.1.273. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Matthews R. G., Sheppard C., Goulding C. Methylenetetrahydrofolate reductase and methionine synthase: biochemistry and molecular biology. Eur J Pediatr. 1998 Apr;157 (Suppl 2):S54–S59. doi: 10.1007/pl00014305. [DOI] [PubMed] [Google Scholar]
- Mehta P. K., Hale T. I., Christen P. Aminotransferases: demonstration of homology and division into evolutionary subgroups. Eur J Biochem. 1993 Jun 1;214(2):549–561. doi: 10.1111/j.1432-1033.1993.tb17953.x. [DOI] [PubMed] [Google Scholar]
- Mudd S. H., Datko A. H. The S-Methylmethionine Cycle in Lemna paucicostata. Plant Physiol. 1990 Jun;93(2):623–630. doi: 10.1104/pp.93.2.623. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Neuhierl B., Thanbichler M., Lottspeich F., Böck A. A family of S-methylmethionine-dependent thiol/selenol methyltransferases. Role in selenium tolerance and evolutionary relation. J Biol Chem. 1999 Feb 26;274(9):5407–5414. doi: 10.1074/jbc.274.9.5407. [DOI] [PubMed] [Google Scholar]
- Penning de Vries F. W., Brunsting A. H., van Laar H. H. Products, requirements and efficiency of biosynthesis: a quantitative approach. J Theor Biol. 1974 Jun;45(2):339–377. doi: 10.1016/0022-5193(74)90119-2. [DOI] [PubMed] [Google Scholar]
- Pimenta M. J., Kaneta T., Larondelle Y., Dohmae N., Kamiya Y. S-adenosyl-L-methionine:L-methionine S-methyltransferase from germinating barley. Purification and localization. Plant Physiol. 1998 Oct;118(2):431–438. doi: 10.1104/pp.118.2.431. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rathinasabapathi B., Burnet M., Russell B. L., Gage D. A., Liao P. C., Nye G. J., Scott P., Golbeck J. H., Hanson A. D. Choline monooxygenase, an unusual iron-sulfur enzyme catalyzing the first step of glycine betaine synthesis in plants: prosthetic group characterization and cDNA cloning. Proc Natl Acad Sci U S A. 1997 Apr 1;94(7):3454–3458. doi: 10.1073/pnas.94.7.3454. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rentsch D., Boorer K. J., Frommer W. B. Structure and function of plasma membrane amino acid, oligopeptide and sucrose transporters from higher plants. J Membr Biol. 1998 Apr 1;162(3):177–190. doi: 10.1007/s002329900355. [DOI] [PubMed] [Google Scholar]
- Rhodes D., Gage D. A., Cooper AJL., Hanson A. D. S-Methylmethionine Conversion to Dimethylsulfoniopropionate: Evidence for an Unusual Transamination Reaction. Plant Physiol. 1997 Dec;115(4):1541–1548. doi: 10.1104/pp.115.4.1541. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Skodak F. I., Wong F. F., White L. M. Determination of S-methylmethionine ion in plant materials by automated amino acid analysis. Anal Biochem. 1965 Dec;13(3):568–571. doi: 10.1016/0003-2697(65)90354-4. [DOI] [PubMed] [Google Scholar]
- Thanbichler M., Neuhierl B., Böck A. S-methylmethionine metabolism in Escherichia coli. J Bacteriol. 1999 Jan;181(2):662–665. doi: 10.1128/jb.181.2.662-665.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Thompson J. D., Higgins D. G., Gibson T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994 Nov 11;22(22):4673–4680. doi: 10.1093/nar/22.22.4673. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Trossat C., Nolte K. D., Hanson A. D. Evidence That the Pathway of Dimethylsulfoniopropionate Biosynthesis Begins in the Cytosol and Ends in the Chloroplast. Plant Physiol. 1996 Aug;111(4):965–973. doi: 10.1104/pp.111.4.965. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Trossat C., Rathinasabapathi B., Weretilnyk E. A., Shen T. L., Huang Z. H., Gage D. A., Hanson A. D. Salinity promotes accumulation of 3-dimethylsulfoniopropionate and its precursor S-methylmethionine in chloroplasts. Plant Physiol. 1998 Jan;116(1):165–171. doi: 10.1104/pp.116.1.165. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Weibull J., Ronquist F., Brishammar S. Free amino Acid composition of leaf exudates and Phloem sap : a comparative study in oats and barley. Plant Physiol. 1990 Jan;92(1):222–226. doi: 10.1104/pp.92.1.222. [DOI] [PMC free article] [PubMed] [Google Scholar]