Skip to main content
Plant Physiology logoLink to Plant Physiology
. 1996 Aug;111(4):965–973. doi: 10.1104/pp.111.4.965

Evidence That the Pathway of Dimethylsulfoniopropionate Biosynthesis Begins in the Cytosol and Ends in the Chloroplast.

C Trossat 1, K D Nolte 1, A D Hanson 1
PMCID: PMC160964  PMID: 12226341

Abstract

In the flowering plant Wollastonia biflora (L.) DC. the first step in 3-dimethylsulfoniopropionate (DMSP) synthesis is conversion of methionine to S-methylmethionine (SMM) and the last is oxidation of 3-dimethylsulfoniopropionaldehyde (DMSP-ald) (F. James, L. Paquet, S.A. Sparace, D.A. Gage, A.D. Hanson [1995] Plant Physiol 108: 1439-1448). DMSP-ald was shown to undergo rapid, spontaneous decomposition to dimethylsulfide and acrolein. However, it was stable enough (half-life [greater than or equal to] 1 h) in tertiary amine buffers to use as a substrate for enzyme assays. A dehydrogenase catalyzing DMSP-ald oxidation was detected in extracts of W. biflora mesophyll protoplasts. This enzyme had a high affinity for DMSP-ald (Km = 1.5 [mu]M), was subject to substrate inhibition, preferred NAD to NADP, and was immunologically related to plant betaine aldehyde dehydrogenases. After fractionation of protoplast lysates, [greater than or equal to]90% of DMSP-ald dehydrogenase activity was recovered from the chloroplast stromal fraction, whereas the enzyme that mediates SMM synthesis, S-adenosylmethionine:methionine S-methyltransferase, was found exclusively in the cytosolic fraction. Immunohistochemical analysis confirmed that the S-methyltransferase was cytosolic. Intact W. biflora chloroplasts were able to metabolize supplied [35S]SMM to [35S]DMSP. These findings indicate that SMM is made in the cytosol, imported into the chloroplast, and there converted successively to DMSP-ald and DMSP.

Full Text

The Full Text of this article is available as a PDF (2.8 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bohnert H. J., Nelson D. E., Jensen R. G. Adaptations to Environmental Stresses. Plant Cell. 1995 Jul;7(7):1099–1111. doi: 10.1105/tpc.7.7.1099. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Cline K. Import of proteins into chloroplasts. Membrane integration of a thylakoid precursor protein reconstituted in chloroplast lysates. J Biol Chem. 1986 Nov 5;261(31):14804–14810. [PubMed] [Google Scholar]
  3. Edwards G. E., Robinson S. P., Tyler N. J., Walker D. A. Photosynthesis by isolated protoplasts, protoplast extracts, and chloroplasts of wheat: influence of orthophosphate, pyrophosphate, and adenylates. Plant Physiol. 1978 Aug;62(2):313–319. doi: 10.1104/pp.62.2.313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Eichel J., González J. C., Hotze M., Matthews R. G., Schröder J. Vitamin-B12-independent methionine synthase from a higher plant (Catharanthus roseus). Molecular characterization, regulation, heterologous expression, and enzyme properties. Eur J Biochem. 1995 Jun 15;230(3):1053–1058. doi: 10.1111/j.1432-1033.1995.tb20655.x. [DOI] [PubMed] [Google Scholar]
  5. Ellis K. J., Morrison J. F. Buffers of constant ionic strength for studying pH-dependent processes. Methods Enzymol. 1982;87:405–426. doi: 10.1016/s0076-6879(82)87025-0. [DOI] [PubMed] [Google Scholar]
  6. GREENE R. C. Biosynthesis of dimethyl-beta-propiothetin. J Biol Chem. 1962 Jul;237:2251–2254. [PubMed] [Google Scholar]
  7. 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]
  8. 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]
  9. James F., Paquet L., Sparace S. A., Gage D. A., Hanson A. D. Evidence implicating dimethylsulfoniopropionaldehyde as an intermediate in dimethylsulfoniopropionate biosynthesis. Plant Physiol. 1995 Aug;108(4):1439–1448. doi: 10.1104/pp.108.4.1439. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. Nolte K. D., Koch K. E. Companion-Cell Specific Localization of Sucrose Synthase in Zones of Phloem Loading and Unloading. Plant Physiol. 1993 Mar;101(3):899–905. doi: 10.1104/pp.101.3.899. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Rathinasabapathi B., McCue K. F., Gage D. A., Hanson A. D. Metabolic engineering of glycine betaine synthesis: plant betaine aldehyde dehydrogenases lacking typical transit peptides are targeted to tobacco chloroplasts where they confer betaine aldehyde resistance. Planta. 1994;193(2):155–162. doi: 10.1007/BF00192524. [DOI] [PubMed] [Google Scholar]
  13. Wallsgrove R. M., Lea P. J., Miflin B. J. Intracellular localization of aspartate kinase and the enzymes of threonine and methionine biosynthesis in green leaves. Plant Physiol. 1983 Apr;71(4):780–784. doi: 10.1104/pp.71.4.780. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Weigel P., Lerma C., Hanson A. D. Choline oxidation by intact spinach chloroplasts. Plant Physiol. 1988 Jan;86(1):54–60. doi: 10.1104/pp.86.1.54. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Plant Physiology are provided here courtesy of Oxford University Press

RESOURCES