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PMID: 15365836 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Identification of an ascorbate-dependent cytochrome b of the tonoplast membrane sharing biochemical features with members of the cytochrome b561 family.

Planta ·Vol. 220 ·No. 3 ·2005-01-00 ·Pages 365-75

Preger V, Scagliarini S, Pupillo P, Trost P

Abstract

Two membrane-bound, ascorbate-dependent b-type cytochromes were identified in etiolated bean (Phaseolus vulgaris L.) hypocotyls. Following solubilization of microsomal membranes and anion-exchange chromatography at pH 8.0, two major cytochrome peaks (P-I and P-II) were separated. Both cytochromes were reduced by ascorbate and re-oxidized by monodehydroascorbate, but P-I reduction by ascorbate was higher and saturated at far lower concentrations of ascorbate with respect to P-II. The alpha-band was symmetrically centered at 561 nm in P-I, but it was asymmetric in P-II with a maximum at 562 nm and shoulder at 557 nm. Ascorbate reduction of P-II, but not P-I, was inhibited by diethyl pyrocarbonate. Reduced P-II but not P-I was readily oxidized by certain ferric chelates, including FeEDTA and Fe-nitrilotriacetic acid. Purified P-I, associated with the plasma membrane, showed up as a 63-kDa glycosylated protein during sodium dodecyl sulfate-polyacrylamide gel electrophoresis (SDS-PAGE) and behaved as a monomer of about 70 kDa during size-exclusion chromatography. P-I identified with a previously purified ascorbate-dependent b-type cytochrome of bean hypocotyl plasma membranes. Partially purified P-II, on the other hand, correlated with a heme-protein of 27 kDa in SDS-PAGE gels, was dimeric (60 kDa) during size-exclusion chromatography, and was associated with the tonoplast marker V-ATPase in sucrose gradients. The sequence of a peptide of 11 residues obtained by tryptic digestion of P-II was found to be identical to a segment of a putative cytochrome b561 of Zea mays and highly conserved in other related plant sequences, including that of Arabidopsis thaliana cytochrome b561-1 (CAA18169). The biochemical features fully support the assignment of P-II cytochrome to the family of cytochrome b561, ascorbate-dependent (CYBASC) cytochromes, which also includes cytochrome b561 of animal chromaffin granules. The presence of a cytochrome reducing ferric chelates on the tonoplast is consistent with the role of plant vacuoles in iron homeostasis.

MeSH Terms
Amino Acid Sequence Ascorbic Acid/metabolism Cytochrome b Group/chemistry,isolation & purification,metabolism Diethyl Pyrocarbonate Electron Transport Intracellular Membranes/enzymology Microsomes/enzymology Phaseolus/enzymology
Chemicals
Cytochrome b Group cytochrome b561 Diethyl Pyrocarbonate Ascorbic Acid
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Preger Valeria
Laboratory of Molecular Plant Physiology, Department of Biology, University of Bologna, Via Irnerio 42, 40126 Bologna, Italy. [email protected]
Scagliarini Sandra
Pupillo Paolo
Trost Paolo
References (46)
46 references, click to expand
  1. Tissue-specific expression and developmental regulation of cytochrome b561 genes in Arabidopsis thaliana and Raphanus sativus.
    Physiol Plant. 2004 Feb;120(2):312-318 PMID: 15032866
  2. Analysis of an Arabidopsis thaliana protein family, structurally related to cytochromes b561 and potentially involved in catecholamine biochemistry in plants.
    J Plant Physiol. 2004 Feb;161(2):175-81 PMID: 15022831
  3. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  4. Fe homeostasis in plant cells: does nicotianamine play multiple roles in the regulation of cytoplasmic Fe concentration?
    Planta. 2001 Oct;213(6):967-76 PMID: 11722133
  5. Diethyl pyrocarbonate modification abolishes fast electron accepting ability of cytochrome b561 from ascorbate but does not influence electron donation to monodehydroascorbate radical: identification of the modification sites by mass spectrometric analysis.
    Biochemistry. 2000 Mar 28;39(12):3276-84 PMID: 10727219
  6. pH-induced alteration and oxidative destruction of heme in purified chromaffin granule cytochrome b(561): implications for the oxidative stress in catecholaminergic neurons.
    Biochemistry. 2003 Apr 1;42(12):3617-26 PMID: 12653566
  7. 3,3',5,5'-tetramethylbenzidine/H2O2 staining is not specific for heme proteins separated by gel electrophoresis.
    Anal Biochem. 1984 Aug 1;140(2):577-80 PMID: 6207749
  8. Structural basis for the electron transfer across the chromaffin vesicle membranes catalyzed by cytochrome b561: analyses of cDNA nucleotide sequences and visible absorption spectra.
    Biochim Biophys Acta. 1998 Apr 2;1383(2):269-78 PMID: 9602148
  9. Ascorbate-independent electron transfer between cytochrome b561 and a 27 kDa ascorbate peroxidase of bean hypocotyls.
    Protoplasma. 2001;217(1-3):137-45 PMID: 11732331
  10. Nicotianamine chelates both FeIII and FeII. Implications for metal transport in plants
    Plant Physiol. 1999 Mar;119(3):1107-14 PMID: 10069850
  11. Structure prediction for the di-heme cytochrome b561 protein family.
    Protoplasma. 2003 May;221(1-2):31-40 PMID: 12768339
  12. Transmembrane electron transport in ascorbate-loaded plasma membrane vesicles from higher plants involves a b-type cytochrome.
    FEBS Lett. 1992 Jul 20;306(2-3):143-6 PMID: 1633869
  13. Stromal cell-derived receptor 2 and cytochrome b561 are functional ferric reductases.
    Biochim Biophys Acta. 2003 Sep 23;1651(1-2):116-23 PMID: 14499595
  14. CCC1 is a transporter that mediates vacuolar iron storage in yeast.
    J Biol Chem. 2001 Aug 3;276(31):29515-9 PMID: 11390404
  15. Higher-plant plasma membrane cytochrome b561: a protein in search of a function.
    Protoplasma. 2001;217(1-3):77-93 PMID: 11732342
  16. Chromaffin granule membranes contain at least three heme centers: direct evidence from EPR and absorption spectroscopy.
    FEBS Lett. 2001 Feb 23;491(1-2):119-22 PMID: 11226432
  17. Cloning and heterologous expression of NAD(P)H:quinone reductase of Arabidopsis thaliana, a functional homologue of animal DT-diaphorase.
    FEBS Lett. 1999 Dec 17;463(3):382-6 PMID: 10606758
  18. Cellular and subcellular localization of the Nramp2 iron transporter in the intestinal brush border and regulation by dietary iron.
    Blood. 1999 Jun 15;93(12):4406-17 PMID: 10361139
  19. An iron-regulated ferric reductase associated with the absorption of dietary iron.
    Science. 2001 Mar 2;291(5509):1755-9 PMID: 11230685
  20. Iron storage in Saccharomyces cerevisiae.
    FEBS Lett. 1988 Apr 11;231(1):253-8 PMID: 3282922
  21. Subcellular distribution of ascorbate in bovine adrenal medulla. Evidence for accumulation in chromaffin granules against a concentration gradient.
    Biochim Biophys Acta. 1980 Mar 3;628(2):182-9 PMID: 7357036
  22. Transport of Ascorbic and Dehydroascorbic Acids across Protoplast and Vacuole Membranes Isolated from Barley (Hordeum vulgare L. cv Gerbel) Leaves.
    Plant Physiol. 1994 Sep;106(1):187-193 PMID: 12232318
  23. Existence of two heme B centers in cytochrome b561 from bovine adrenal chromaffin vesicles as revealed by a new purification procedure and EPR spectroscopy.
    J Biol Chem. 1997 Sep 12;272(37):23206-10 PMID: 9287327
  24. Nramp2 is mutated in the anemic Belgrade (b) rat: evidence of a role for Nramp2 in endosomal iron transport.
    Proc Natl Acad Sci U S A. 1998 Feb 3;95(3):1148-53 PMID: 9448300
  25. Localization of an ascorbate-reducible cytochrome b561 in the plant tonoplast.
    Plant Physiol. 2004 Feb;134(2):726-34 PMID: 14730083
  26. Composition of the heme centers in chromaffin granule cytochrome b(561).
    Ann N Y Acad Sci. 2002 Oct;971:450-3 PMID: 12438163
  27. Unusual redox behaviour of cytochrome b-561 from bovine chromaffin granule membranes.
    Biochim Biophys Acta. 1984 Jan 30;764(1):8-16 PMID: 6696883
  28. Purification of octyl beta-D-glucopyranoside and re-estimation of its micellar size.
    Biochim Biophys Acta. 1990 Apr 13;1023(2):254-65 PMID: 2328249
  29. Dissecting the Diphenylene Iodonium-Sensitive NAD(P)H:Quinone Oxidoreductase of Zucchini Plasma Membrane.
    Plant Physiol. 1997 Jun;114(2):737-746 PMID: 12223742
  30. Solubilization of functional membrane proteins.
    Methods Enzymol. 1984;104:305-18 PMID: 6232441
  31. AtNRAMP3, a multispecific vacuolar metal transporter involved in plant responses to iron deficiency.
    Plant J. 2003 Jun;34(5):685-95 PMID: 12787249
  32. Mechanism of reduction of quinones by Trypanosoma congolense trypanothione reductase.
    Biochemistry. 1994 Mar 8;33(9):2509-15 PMID: 8117712
  33. Purification of cytochrome b-561 from bean hypocotyls plasma membrane. Evidence for the presence of two heme centers.
    Biochim Biophys Acta. 2000 Sep 29;1468(1-2):1-5 PMID: 11018644
  34. A phylogenetic study of cytochrome b561 proteins.
    Genome Biol. 2003;4(6):R38 PMID: 12801412
  35. b-Type Cytochromes in Higher Plant Plasma Membranes.
    Plant Physiol. 1989 Jul;90(3):1077-83 PMID: 16666854
  36. 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;72:248-54 PMID: 942051
  37. The secretory-vesicle ascorbate-regenerating system: a chain of concerted H+/e(-)-transfer reactions.
    Biochim Biophys Acta. 1993 Oct 4;1144(3):235-48 PMID: 8399278
  38. Tonoplast subcellular localization of maize cytochrome b5 reductases.
    Plant J. 2000 Dec;24(5):645-54 PMID: 11123803
  39. Domain homologues of dopamine beta-hydroxylase and ferric reductase: roles for iron metabolism in neurodegenerative disorders?
    Hum Mol Genet. 2001 Aug 15;10(17):1853-8 PMID: 11532994
  40. An improved staining procedure for the detection of the peroxidase activity of cytochrome P-450 on sodium dodecyl sulfate polyacrylamide gels.
    Anal Biochem. 1976 Sep;75(1):168-76 PMID: 822747
  41. Systematic analysis of peptide recoveries from in-gel digestions for protein identifications in proteome studies.
    J Biomol Tech. 2000 Jun;11(2):74-86 PMID: 19499040
  42. Iron sequestration by the yeast vacuole. A study with vacuolar mutants of Saccharomyces cerevisiae.
    Eur J Biochem. 1995 Mar 1;228(2):337-42 PMID: 7705347
  43. Cloning and characterization of a mammalian proton-coupled metal-ion transporter.
    Nature. 1997 Jul 31;388(6641):482-8 PMID: 9242408
  44. The structure of cytochrome b561, a secretory vesicle-specific electron transport protein.
    EMBO J. 1988 Sep;7(9):2697-703 PMID: 2460342
  45. Modification of histidyl residues in proteins by diethylpyrocarbonate.
    Methods Enzymol. 1977;47:431-42 PMID: 22021
  46. The Role of Ascorbate Free Radical as an Electron Acceptor to Cytochrome b-Mediated Trans-Plasma Membrane Electron Transport in Higher Plants.
    Plant Physiol. 1994 Apr;104(4):1455-1458 PMID: 12232179
Article Info
Journal
Planta
Abbr.
Planta
ISSN
0032-0935
Published
2005-01-00
Epub
2004-00-09
Pages
365-75
Language
English
Region
Germany
NLM ID
1250576
Subset
IM
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