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. 1991 Nov;97(3):1199–1205. doi: 10.1104/pp.97.3.1199

Comparative Physiological Evidence that β-Alanine Betaine and Choline-O-Sulfate Act as Compatible Osmolytes in Halophytic Limonium Species 1

Andrew D Hanson 1,2,3, Bala Rathinasabapathi 1,2,3, Beverly Chamberlin 1,2,3, Douglas A Gage 1,2,3
PMCID: PMC1081142  PMID: 16668509

Abstract

The quaternary ammonium compounds accumulated in saline conditions by five salt-tolerant species of Limonium (Plumbaginaceae) were analyzed by fast atom bombardment mass spectrometry. Three species accumulated β-alanine betaine and choline-O-sulfate; the others accumulated glycine betaine and choline-O-sulfate. Three lines of evidence indicated that β-alanine betaine and choline-O-sulfate replace glycine betaine as osmo-regulatory solutes. First, tests with bacteria showed that β-alanine betaine and choline-O-sulfate have osmoprotective properties comparable to glycine betaine. Second, when β-alanine betaine and glycine betaine accumulators were salinized, the levels of their respective betaines, plus that of choline-O-sulfate, were closely correlated with leaf solute potential. Third, substitution of sulfate for chloride salinity caused an increase in the level of choline-O-sulfate and a matching decrease in glycine betaine level. Experiments with 14C-labeled precursors established that β-alanine betaine accumulators did not synthesize glycine betaine and vice versa. These experiments also showed that β-alanine betaine synthesis occurs in roots as well as leaves of β-alanine betaine accumulators and that choline-O-sulfate and glycine betaine share choline as a precursor. Unlike glycine betaine, β-alanine betaine synthesis cannot interfere with conjugation of sulfate to choline by competing for choline and does not require oxygen. These features of β-alanine betaine may be advantageous in sulfate-rich salt marsh environments.

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Selected References

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

  1. Brouquisse R., Weigel P., Rhodes D., Yocum C. F., Hanson A. D. Evidence for a ferredoxin-dependent choline monooxygenase from spinach chloroplast stroma. Plant Physiol. 1989 May;90(1):322–329. doi: 10.1104/pp.90.1.322. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Csonka L. N. Physiological and genetic responses of bacteria to osmotic stress. Microbiol Rev. 1989 Mar;53(1):121–147. doi: 10.1128/mr.53.1.121-147.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Hanson A. D., Wyse R. Biosynthesis, translocation, and accumulation of betaine in sugar beet and its progenitors in relation to salinity. Plant Physiol. 1982 Oct;70(4):1191–1198. doi: 10.1104/pp.70.4.1191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Landfald B., Strøm A. R. Choline-glycine betaine pathway confers a high level of osmotic tolerance in Escherichia coli. J Bacteriol. 1986 Mar;165(3):849–855. doi: 10.1128/jb.165.3.849-855.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Lerma C., Hanson A. D., Rhodes D. Oxygen-18 and deuterium labeling studies of choline oxidation by spinach and sugar beet. Plant Physiol. 1988 Nov;88(3):695–702. doi: 10.1104/pp.88.3.695. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Rhodes D., Rich P. J., Myers A. C., Reuter C. C., Jamieson G. C. Determination of Betaines by Fast Atom Bombardment Mass Spectrometry : Identification of Glycine Betaine Deficient Genotypes of Zea mays. Plant Physiol. 1987 Jul;84(3):781–788. doi: 10.1104/pp.84.3.781. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Somero G. N. Protons, osmolytes, and fitness of internal milieu for protein function. Am J Physiol. 1986 Aug;251(2 Pt 2):R197–R213. doi: 10.1152/ajpregu.1986.251.2.R197. [DOI] [PubMed] [Google Scholar]
  8. Storey R., Jones R. G. Responses of Atriplex spongiosa and Suaeda monoica to Salinity. Plant Physiol. 1979 Jan;63(1):156–162. doi: 10.1104/pp.63.1.156. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Styrvold O. B., Falkenberg P., Landfald B., Eshoo M. W., Bjørnsen T., Strøm A. R. Selection, mapping, and characterization of osmoregulatory mutants of Escherichia coli blocked in the choline-glycine betaine pathway. J Bacteriol. 1986 Mar;165(3):856–863. doi: 10.1128/jb.165.3.856-863.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Van Wielink J. E., Duine J. A. How big is the periplasmic space? Trends Biochem Sci. 1990 Apr;15(4):136–137. doi: 10.1016/0968-0004(90)90208-s. [DOI] [PubMed] [Google Scholar]

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