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PMID: 11526234 Published · ppublish English Comparative Study Journal Article

A hemoglobin from plants homologous to truncated hemoglobins of microorganisms.

Watts RA, Hunt PW, Hvitved AN, Hargrove MS, Peacock WJ, Dennis ES

Abstract

We have identified a nuclear-encoded Hb from plants (GLB3) that has a central domain similar to the "truncated" Hbs of bacteria, protozoa, and algae. The three-dimensional structure of these Hbs is a 2-on-2 arrangement of alpha-helices, distinct from the 3-on-3 arrangement of the standard globin fold [Pesce, A., Couture, M., Dewilde, S., Guertin, M., Yamauchi, K., Ascenzi, P., Moens, L. & Bolognesi, M. (2000) EMBO J. 19, 2424-2434]. GLB3-like genes are not found in animals or yeast, but our analysis reveals that they are present in a wide range of Angiosperms and a Bryophyte. Although cyanobacteria and Chlamydomonas have 2-on-2 Hbs (GLBN), GLB3 is more likely related to GLBO-type 2-on-2 Hbs from bacteria. Consequently, GLB3 is unlikely to have arisen from a horizontal transfer between the chloroplast and nuclear genomes. Arabidopsis thaliana GLB3 protein exhibits unusual concentration-independent binding of O(2) and CO. The absorbance spectrum of deoxy-GLB3 is unique; the protein forms a transient six-coordinate structure after reduction and deoxygenation, which slowly converts to a five-coordinate structure. In A. thaliana, GLB3 is expressed throughout the plant but responds to none of the treatments that induce plant 3-on-3 Hbs. Our analysis of the sequence, ligand interactions, and expression profile of GLB3 indicates that this protein has unique biochemical properties, evolutionary history, and, most likely, a function distinct from those of other plant Hbs.

MeSH Terms
Amino Acid Sequence Animals Arabidopsis/genetics,metabolism Bacterial Proteins/genetics Eukaryota/genetics Gene Expression Genes, Plant Hemoglobins/genetics,metabolism Kinetics Molecular Sequence Data Phylogeny Plant Proteins/genetics,metabolism Plants/genetics Protozoan Proteins/genetics RNA, Messenger/genetics RNA, Plant/genetics Sequence Homology, Amino Acid Truncated Hemoglobins
Chemicals
Bacterial Proteins Hemoglobins Plant Proteins Protozoan Proteins RNA, Messenger RNA, Plant Truncated Hemoglobins
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Watts R A
CSIRO Plant Industry, Canberra, ACT 2601, Australia.
Hunt P W
Hvitved A N
Hargrove M S
Peacock W J
Dennis E S
References (27)
27 references, click to expand
  1. A cyanobacterial hemoglobin with unusual ligand binding kinetics and stability properties.
    Biochemistry. 1999 Feb 16;38(7):2117-26 PMID: 10026295
  2. A cooperative oxygen-binding hemoglobin from Mycobacterium tuberculosis.
    Proc Natl Acad Sci U S A. 1999 Sep 28;96(20):11223-8 PMID: 10500158
  3. A novel two-over-two alpha-helical sandwich fold is characteristic of the truncated hemoglobin family.
    EMBO J. 2000 Jun 1;19(11):2424-34 PMID: 10835341
  4. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence.
    J Mol Biol. 2000 Jul 21;300(4):1005-16 PMID: 10891285
  5. Structural investigations of the hemoglobin of the cyanobacterium Synechocystis PCC6803 reveal a unique distal heme pocket.
    Eur J Biochem. 2000 Aug;267(15):4770-80 PMID: 10903511
  6. A flash photolysis method to characterize hexacoordinate hemoglobin kinetics.
    Biophys J. 2000 Nov;79(5):2733-8 PMID: 11053146
  7. Ligand binding in the ferric and ferrous states of Paramecium hemoglobin.
    Biochemistry. 2000 Nov 21;39(46):14330-40 PMID: 11087382
  8. Ligand binding and hexacoordination in synechocystis hemoglobin.
    J Biol Chem. 2001 Sep 14;276(37):34714-21 PMID: 11438545
  9. The unique structure of the Paramecium caudatum hemoglobin gene: the presence of one intron in the middle of the coding region.
    Biochim Biophys Acta. 1992 Nov 15;1171(1):81-7 PMID: 1420365
  10. A cooperative hemoglobin with directly communicating hemes. The Scapharca inaequivalvis homodimer.
    Biophys Chem. 1990 Aug 31;37(1-3):287-92 PMID: 2285790
  11. High-level expression of sperm whale myoglobin in Escherichia coli.
    Proc Natl Acad Sci U S A. 1987 Dec;84(24):8961-5 PMID: 3321062
  12. A comparison of the geminate recombination kinetics of several monomeric heme proteins.
    J Biol Chem. 1988 Feb 5;263(4):1803-13 PMID: 3338995
  13. Determinants of a protein fold. Unique features of the globin amino acid sequences.
    J Mol Biol. 1987 Jul 5;196(1):199-216 PMID: 3656444
  14. Geminate recombination of carbon monoxide to myoglobin.
    J Mol Biol. 1983 May 25;166(3):443-51 PMID: 6854651
  15. Structure and evolution of Paramecium hemoglobin genes.
    Biochim Biophys Acta. 1995 Oct 17;1264(1):53-62 PMID: 7578257
  16. Genes galore: a summary of methods for accessing results from large-scale partial sequencing of anonymous Arabidopsis cDNA clones.
    Plant Physiol. 1994 Dec;106(4):1241-55 PMID: 7846151
  17. Nuclear genes encoding chloroplast hemoglobins in the unicellular green alga Chlamydomonas eugametos.
    Mol Gen Genet. 1994 Apr;243(2):185-97 PMID: 8177215
  18. Globins in nonvertebrate species: dispersal by horizontal gene transfer and evolution of the structure-function relationships.
    Mol Biol Evol. 1996 Feb;13(2):324-33 PMID: 8587498
  19. Ordered water molecules as key allosteric mediators in a cooperative dimeric hemoglobin.
    Proc Natl Acad Sci U S A. 1996 Dec 10;93(25):14526-31 PMID: 8962085
  20. Purification and spectroscopic characterization of a recombinant chloroplastic hemoglobin from the green unicellular alga Chlamydomonas eugametos.
    Eur J Biochem. 1996 Dec 15;242(3):779-87 PMID: 9022709
  21. Ligand linked assembly of Scapharca dimeric hemoglobin.
    J Biol Chem. 1997 Feb 28;272(9):5689-94 PMID: 9038179
  22. Characterization of recombinant soybean leghemoglobin a and apolar distal histidine mutants.
    J Mol Biol. 1997 Mar 14;266(5):1032-42 PMID: 9086279
  23. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
    Nucleic Acids Res. 1997 Sep 1;25(17):3389-402 PMID: 9254694
  24. Two hemoglobin genes in Arabidopsis thaliana: the evolutionary origins of leghemoglobins.
    Proc Natl Acad Sci U S A. 1997 Oct 28;94(22):12230-4 PMID: 9342391
  25. Evolution of myoglobin.
    Cell Mol Life Sci. 1998 Sep;54(9):979-1004 PMID: 9791540
  26. Protein phylogenies and signature sequences: A reappraisal of evolutionary relationships among archaebacteria, eubacteria, and eukaryotes.
    Microbiol Mol Biol Rev. 1998 Dec;62(4):1435-91 PMID: 9841678
  27. Arabidopsis roots and shoots have different mechanisms for hypoxic stress tolerance.
    Plant Physiol. 1999 Jan;119(1):57-64 PMID: 9880346
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2001-08-28
Pages
10119-24
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC56925
Subset
IM
Databases
GENBANK
AF376062, AF376063
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