Skip to main content
NCBI home page
Plant Physiology logoLink to Plant Physiology
. 1997 Nov;115(3):891–899. doi: 10.1104/pp.115.3.891

Evidence for the Presence of a Porin in the Membrane of Glyoxysomes of Castor Bean.

S Reumann 1, M Bettermann 1, R Benz 1, H W Heldt 1
PMCID: PMC158552  PMID: 12223852

Abstract

Glyoxysomes of endosperm tissue of castor bean (Ricinus communis L.) seedlings were solubilized in a detergent and added to a lipid bilayer. Conductivity measurements revealed that the glyoxysomal preparation contained a porin-like channel. Using an electrophysiological method, which we established for semiquantitative determination of porin activity, we were able to demonstrate that glyoxysomal membranes purified by sucrose density gradient centrifugation contain an integral membrane protein with porin activity. The porin of glyoxysomes was shown to have a relatively small single-channel conductance of about 330 picosiemens in 1 M KCl and to be strongly anion selective. Thus, the glyoxysomal porin differs from the other previously characterized porins in the outer membrane of mitochondria or plastids, but is similar to the porin of spinach (Spinacia oleracea L.) leaf peroxisomes. Our results suggest that, in analogy to the porin of leaf peroxisomes, the glyoxysomal porin facilitates the passage of small metabolites, such as succinate, citrate, malate, and aspartate, through the membrane.

Full Text

The Full Text of this article is available as a PDF (1.9 MB).

Selected References

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

  1. Beeckmans S., Khan A. S., Van Driessche E., Kanarek L. A specific association between the glyoxylic-acid-cycle enzymes isocitrate lyase and malate synthase. Eur J Biochem. 1994 Aug 15;224(1):197–201. doi: 10.1111/j.1432-1033.1994.tb20012.x. [DOI] [PubMed] [Google Scholar]
  2. Benz R., Hancock R. E. Mechanism of ion transport through the anion-selective channel of the Pseudomonas aeruginosa outer membrane. J Gen Physiol. 1987 Feb;89(2):275–295. doi: 10.1085/jgp.89.2.275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Benz R., Ishii J., Nakae T. Determination of ion permeability through the channels made of porins from the outer membrane of Salmonella typhimurium in lipid bilayer membranes. J Membr Biol. 1980 Aug 21;56(1):19–29. doi: 10.1007/BF01869348. [DOI] [PubMed] [Google Scholar]
  4. Benz R. Permeation of hydrophilic solutes through mitochondrial outer membranes: review on mitochondrial porins. Biochim Biophys Acta. 1994 Jun 29;1197(2):167–196. doi: 10.1016/0304-4157(94)90004-3. [DOI] [PubMed] [Google Scholar]
  5. Benz R., Schmid A., Vos-Scheperkeuter G. H. Mechanism of sugar transport through the sugar-specific LamB channel of Escherichia coli outer membrane. J Membr Biol. 1987;100(1):21–29. doi: 10.1007/BF02209137. [DOI] [PubMed] [Google Scholar]
  6. Breidenbach R. W., Beevers H. Association of the glyoxylate cycle enzymes in a novel subcellular particle from castor bean endosperm. Biochem Biophys Res Commun. 1967 May 25;27(4):462–469. doi: 10.1016/s0006-291x(67)80007-x. [DOI] [PubMed] [Google Scholar]
  7. Courtois-Verniquet F., Douce R. Lack of aconitase in glyoxysomes and peroxisomes. Biochem J. 1993 Aug 15;294(Pt 1):103–107. doi: 10.1042/bj2940103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. De Duve C., Baudhuin P. Peroxisomes (microbodies and related particles). Physiol Rev. 1966 Apr;46(2):323–357. doi: 10.1152/physrev.1966.46.2.323. [DOI] [PubMed] [Google Scholar]
  9. Donaldson R. P. Organelle Membranes from Germinating Castor Bean Endosperm: II. ENZYMES, CYTOCHROMES, AND PERMEABILITY OF THE GLYOXYSOME MEMBRANE. Plant Physiol. 1981 Jan;67(1):21–25. doi: 10.1104/pp.67.1.21. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Douce R., Holtz R. B., Benson A. A. Isolation and properties of the envelope of spinach chloroplasts. J Biol Chem. 1973 Oct 25;248(20):7215–7222. [PubMed] [Google Scholar]
  11. Fischer K., Weber A., Brink S., Arbinger B., Schünemann D., Borchert S., Heldt H. W., Popp B., Benz R., Link T. A. Porins from plants. Molecular cloning and functional characterization of two new members of the porin family. J Biol Chem. 1994 Oct 14;269(41):25754–25760. [PubMed] [Google Scholar]
  12. Guex N., Henry H., Flach J., Richter H., Widmer F. Glyoxysomal malate dehydrogenase and malate synthase from soybean cotyledons (Glycine max L.): enzyme association, antibody production and cDNA cloning. Planta. 1995;197(2):369–375. doi: 10.1007/BF00202659. [DOI] [PubMed] [Google Scholar]
  13. Hancock R. E., Poole K., Benz R. Outer membrane protein P of Pseudomonas aeruginosa: regulation by phosphate deficiency and formation of small anion-specific channels in lipid bilayer membranes. J Bacteriol. 1982 May;150(2):730–738. doi: 10.1128/jb.150.2.730-738.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hayashi M., De Bellis L., Alpi A., Nishimura M. Cytosolic aconitase participates in the glyoxylate cycle in etiolated pumpkin cotyledons. Plant Cell Physiol. 1995 Jun;36(4):669–680. [PubMed] [Google Scholar]
  15. Heldt H. W., Sauer F. The inner membrane of the chloroplast envelope as the site of specific metabolite transport. Biochim Biophys Acta. 1971 Apr 6;234(1):83–91. doi: 10.1016/0005-2728(71)90133-2. [DOI] [PubMed] [Google Scholar]
  16. Heupel R., Heldt H. W. Protein organization in the matrix of leaf peroxisomes. A multi-enzyme complex involved in photorespiratory metabolism. Eur J Biochem. 1994 Feb 15;220(1):165–172. doi: 10.1111/j.1432-1033.1994.tb18611.x. [DOI] [PubMed] [Google Scholar]
  17. Hicks D. B., Donaldson R. P. Electron transport in glyoxysomal membranes. Arch Biochem Biophys. 1982 Apr 15;215(1):280–288. doi: 10.1016/0003-9861(82)90306-x. [DOI] [PubMed] [Google Scholar]
  18. Lemmens M., Verheyden K., Van Veldhoven P., Vereecke J., Mannaerts G. P., Carmeliet E. Single-channel analysis of a large conductance channel in peroxisomes from rat liver. Biochim Biophys Acta. 1989 Sep 18;984(3):351–359. doi: 10.1016/0005-2736(89)90302-7. [DOI] [PubMed] [Google Scholar]
  19. Miernyk J. A., Trelease R. N., Choinski J. S. Malate synthase activity in cotton and other ungerminated oilseeds: a survey. Plant Physiol. 1979 Jun;63(6):1068–1071. doi: 10.1104/pp.63.6.1068. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Miflin B. J., Beevers H. Isolation of intact plastids from a range of plant tissues. Plant Physiol. 1974 Jun;53(6):870–874. doi: 10.1104/pp.53.6.870. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Reumann S., Maier E., Benz R., Heldt H. W. A specific porin is involved in the malate shuttle of leaf peroxisomes. Biochem Soc Trans. 1996 Aug;24(3):754–757. doi: 10.1042/bst0240754. [DOI] [PubMed] [Google Scholar]
  22. Roos N., Benz R., Brdiczka D. Identification and characterization of the pore-forming protein in the outer membrane of rat liver mitochondria. Biochim Biophys Acta. 1982 Apr 7;686(2):204–214. doi: 10.1016/0005-2736(82)90114-6. [DOI] [PubMed] [Google Scholar]
  23. Schmid A., Krömer S., Heldt H. W., Benz R. Identification of two general diffusion channels in the outer membrane of pea mitochondria. Biochim Biophys Acta. 1992 Dec 9;1112(2):174–180. doi: 10.1016/0005-2736(92)90389-4. [DOI] [PubMed] [Google Scholar]
  24. Sulter G. J., Verheyden K., Mannaerts G., Harder W., Veenhuis M. The in vitro permeability of yeast peroxisomal membranes is caused by a 31 kDa integral membrane protein. Yeast. 1993 Jul;9(7):733–742. doi: 10.1002/yea.320090707. [DOI] [PubMed] [Google Scholar]
  25. Van Veldhoven P. P., Just W. W., Mannaerts G. P. Permeability of the peroxisomal membrane to cofactors of beta-oxidation. Evidence for the presence of a pore-forming protein. J Biol Chem. 1987 Mar 25;262(9):4310–4318. [PubMed] [Google Scholar]
  26. Wessel D., Flügge U. I. A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal Biochem. 1984 Apr;138(1):141–143. doi: 10.1016/0003-2697(84)90782-6. [DOI] [PubMed] [Google Scholar]
  27. van Roermund C. W., Elgersma Y., Singh N., Wanders R. J., Tabak H. F. The membrane of peroxisomes in Saccharomyces cerevisiae is impermeable to NAD(H) and acetyl-CoA under in vivo conditions. EMBO J. 1995 Jul 17;14(14):3480–3486. doi: 10.1002/j.1460-2075.1995.tb07354.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES