Plant Hemoglobins: A Molecular Fossil Record for the Evolution of Oxygen Transport

Journal of Molecular Biology

Volumn 371, Issue 1, 2007, Pages 168-179

  Hoy, Julie A ^a   Robinson, Howard ^b   Trent III, James T ^a   Kakar, Smita ^a   Smagghe, Benoit J ^a   Hargrove, Mark S ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b BROOKHAVEN NATIONAL LABORATORY   (United States)

Author keywords

barley hemoglobin; evolution; hexacoordinate hemoglobin; oxygen transport; plant hemoglobins

Indexed keywords

CYANIDE; HEMOGLOBIN;

ARTICLE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; EVOLUTION; FOSSIL PLANT; LIGAND BINDING; OXYGEN AFFINITY; OXYGEN TRANSPORT; PRIORITY JOURNAL; STRUCTURE ANALYSIS;

ANIMALIA; HORDEUM;

EID: 34447108659     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.05.029     Document Type: Article

References (68)

1. Hardison R. A brief history of hemoglobins: plant, animal, protist, and bacteria. Proc. Natl Acad. Sci. USA 93 (1996) 5675-5679
2. Hardison R. Hemoglobins from bacteria to man: evolution of different patterns of gene expression. J. Exp. Biol. 201 (1998) 1099-1117
3. Hardison R. The evolution of hemoglobin. Am. Sci. 87 (1999) 126-137
4. Raymond J., and Segre D. The effect of oxygen on biochemical networks and the evolution of complex life. Science 311 (2006) 1764-1767
5. Falkowski P.G. Evolution. Tracing oxygen's imprint on earth's metabolic evolution. Science 311 (2006) 1724-1725
6. Appleby C.A., Bogusz D., Dennis E.S., and Peacock W.J. A role for haemoglobin in all plant roots?. Plant Cell Environ. 11 (1988) 359-367
7. Dewilde S., Kiger L., Burmester T., Hankeln T., Baudin-Creuza V., Aerts T., et al. Biochemical characterization and ligand binding properties of neuroglobin, a novel member of the globin family. J. Biol. Chem. 276 (2001) 38949-38955
8. Trent III J.T., Watts R.A., and Hargrove M.S. Human neuroglobin, a hexacoordinate hemoglobin that reversibly binds oxygen. J. Biol. Chem. 276 (2001) 30106-30110
9. Burmester T., Ebner B., Welch B., and Hankeln T. Cytoglobin: a novel globin type ubiquitously expressed in vertebrate tissues. Mol. Biol. Evol. 19 (2002) 416-421
10. Trent III J.T., and Hargrove M.S. A ubiquitously expressed human hexacoordinate hemoglobin. J. Biol. Chem. 277 (2002) 19538-19545
11. Kawada N., Kristensen D., Asahina K., Nakatani K., Minamiyama Y., Seki S., and Yoshizato K. Characterization of a stellate cell activation-associated protein (STAP) with peroxidase activity found in rat hepatic stellate cells. J. Biol. Chem. 276 (2001) 25318-25323
12. Wittenberg J.B. The molecular mechanism of hemoglobin-facilitated oxygen diffusion. J. Biol. Chem. 241 (1966) 104-114
13. Delgado-Nixon V., Gonzalez G., and Gilles-Gonzalez M. DOS, a heme-binding PAS protein from Escherichia coli, is a direct oxygen sensor. Biochemistry 39 (2000) 2685-2691
14. Freitas T.A., Hou S., Dioum E.M., Saito J.A., Newhouse J., Gonzalez G., et al. Ancestral hemoglobins in Archaea. Proc. Natl Acad. Sci. USA 101 (2004) 6675-6680
15. Taylor E.R., Nie X.Z., MacGregor A.W., and Hill R.D. A cereal haemoglobin gene is expressed in seed and root tissues under anaerobic conditions. Plant Mol. Biol. 24 (1994) 853-862
16. Guldner E., Godelle B., and Galtier N. Molecular adaptation in plant hemoglobin, a duplicated gene involved in plant-bacteria symbiosis. J. Mol. Evol. 59 (2004) 416-425
17. Trevaskis B., Watts R.A., Andersson C.R., Llewellyn D.J., Hargrove M.S., Olson J.S., et al. Two hemoglobin genes in Arabidopsis thaliana: the evolutionary origins of leghemoglobins. Proc. Natl Acad. Sci. USA 94 (1997) 12230-12234
18. Guldner E., Desmarais E., Galtier N., and Godelle B. Molecular evolution of plant haemoglobin: two haemoglobin genes in Nymphaeaceae Euryale ferox. J. Evol. Biol. 17 (2004) 48-54
19. Hunt P.W., Watts R.A., Trevaskis B., Llewellyn D.J., Burnell J., Dennis E.S., and Peacock W.J. Expression and evolution of functionally distinct haemoglobin genes in plants. Plant Mol. Biol. 47 (2001) 677-692
20. Olson J.S., Mathews A.J., Rohlfs R.J., Springer B.A., Egeberg K.D., Sligar S.G., et al. The role of the distal histidine in myoglobin and haemoglobin. Nature 336 (1988) 265-266
21. Olson J.S., and Phillips Jr. G.N. Kinetic pathways and barriers for ligand binding to myoglobin. J. Biol. Chem. 271 (1996) 17593-17596
22. Duff S.M., Wittenberg J.B., and Hill R.D. Expression, purification, and properties of recombinant barley (Hordeum sp.) hemoglobin. Optical spectra and reactions with gaseous ligands. J. Biol. Chem. 272 (1997) 16746-16752
23. Hargrove M.S., Brucker E.A., Stec B., Sarath G., Arredondo-Peter R., Klucas R.V., et al. Crystal structure of a nonsymbiotic plant hemoglobin. Structure Fold. Des. 8 (2000) 1005-1014
24. Gardner P.R. Nitric oxide dioxygenase function and mechanism of flavohemoglobin, hemoglobin, myoglobin and their associated reductases. J. Inorg. Biochem. 99 (2005) 247-266
25. Hankeln T., Ebner B., Fuchs C., Gerlach F., Haberkamp M., Laufs T.L., et al. Neuroglobin and cytoglobin in search of their role in the vertebrate globin family. J. Inorg. Biochem. 99 (2005) 110-119
26. Smagghe B.J., Sarath G., Ross E., Hilbert J., and Hargrove M.S. Slow ligand binding kinetics dominate ferrous hexacoordinate hemoglobin reactivities and reveal differences between plants and other species. Biochemistry 45 (2006) 561-570
27. Cowley A.B., Kennedy M.L., Silchenko S., Lukat-Rodgers G.S., Rodgers K.R., and Benson D.R. Insight into heme protein redox potential control and functional aspects of six-coordinate ligand-sensing heme proteins from studies of synthetic heme peptides. Inorg. Chem. 45 (2006) 9985-10001
28. Appleby C.A. Leghemoglobin and Rhizobium respiration. Annu. Rev. Plant. Physiol. 35 (1984) 443-478
29. Vinogradov S.N., Hoogewijs D., Bailly X., Arredondo-Peter R., Gough J., Dewilde S., et al. A phylogenomic profile of globins. BMC Evol. Biol. 6 (2006) 31
30. Hargrove M.S., Barry J.K., Brucker E.A., Berry M.B., Phillips Jr. G.N., Olson J.S., et al. Characterization of recombinant soybean leghemoglobin a and apolar distal histidine mutants. J. Mol. Biol. 266 (1997) 1032-1042
31. Harutyunyan E.H., Safonova T.N., Kuranova I.P., Popov A.N., Teplyakov A.V., Obmolova G.V., et al. The structure of deoxy- and oxy-leghaemoglobin from lupin. J. Mol. Biol. 251 (1995) 104-115
32. Trent III J.T., Kundu S., Hoy J.A., and Hargrove M.S. Crystallographic analysis of synechocystis cyanoglobin reveals the structural changes accompanying ligand binding in a hexacoordinate hemoglobin. J. Mol. Biol. 341 (2004) 1097-1108
33. Goodman M.D., and Hargrove M.S. Quaternary structure of rice nonsymbiotic hemoglobin. J. Biol. Chem. 276 (2001) 6834-6839
34. Hoy J.A., Kundu S., Trent III J.T., Ramaswamy S., and Hargrove M.S. The crystal structure of Synechocystis hemoglobin with a covalent heme linkage. J. Biol. Chem. 279 (2004) 16535-16542
35. Vallone B., Nienhaus K., Brunori M., and Nienhaus G.U. The structure of murine neuroglobin: novel pathways for ligand migration and binding. Proteins: Struct. Funct. Genet. 56 (2004) 85-92
36. Vallone B., Nienhaus K., Matthes A., Brunori M., and Nienhaus G.U. The structure of carbonmonoxy neuroglobin reveals a heme-sliding mechanism for control of ligand affinity. Proc. Natl Acad. Sci. USA 101 (2004) 17351-17356
37. de Sanctis D., Dewilde S., Vonrhein C., Pesce A., Moens L., Ascenzi P., et al. Bishistidyl heme hexacoordination, a key structural property in Drosophila melanogaster hemoglobin. J. Biol. Chem. 280 (2005) 27222-27229
38. de Sanctis D., Ascenzi P., Bocedi A., Dewilde S., Burmester T., Hankeln T., et al. Cyanide binding and heme cavity conformational transitions in Drosophila melanogaster hexacoordinate hemoglobin. Biochemistry 45 (2006) 10054-10061
39. Zaric S.D., Popovic D.M., and Knapp E.W. Factors determining the orientation of axially coordinated imidazoles in heme proteins. Biochemistry 40 (2001) 7914-7928
40. Thomas A., Meurisse R., and Brasseur R. Aromatic side-chain interactions in proteins. II. Near- and far-sequence Phe-X pairs. Proteins: Struct. Funct. Genet. 48 (2002) 635-644
41. Meurisse R., Brasseur R., and Thomas A. Aromatic side-chain interactions in proteins. Near- and far-sequence His-X pairs. Biochim. Biophys. Acta 1649 (2003) 85-96
42. Smagghe B.J., Kundu S., Hoy J.A., Halder P., Weiland T.R., Savage A., et al. Role of phenylalanine B10 in plant nonsymbiotic hemoglobins. Biochemistry 45 (2006) 9735-9745
43. 5 at 1.5 Å resolution. Acta Crystallog. sect. D 52 (1996) 65-76
44. Rodriguez J.C., and Rivera M. Conversion of mitochondrial cytochrome b5 into a species capable of performing the efficient coupled oxidation of heme. Biochemistry 37 (1998) 13082-13090
45. Ihara M., Takahashi S., Ishimori K., and Morishima I. Functions of fluctuation in the heme-binding loops of cytochrome b5 revealed in the process of heme incorporation. Biochemistry 39 (2000) 5961-5970
46. Hirota S., Kishi M., Yamauchi O., Wang Y.H., and Huang Z.X. Carbon monoxide complex of cytochrome b(5) at acidic pH. Biochem. Biophys. Res. Commun. 282 (2001) 351-355
47. Falzone C.J., Mayer M.R., Whiteman E.L., Moore C.D., and Lecomte J.T. Design challenges for hemoproteins: the solution structure of apocytochrome b5. Biochemistry 35 (1996) 6519-6526
48. Falzone C.J., Wang Y., Vu B.C., Scott N.L., Bhattacharya S., and Lecomte J.T. Structural and dynamic perturbations induced by heme binding in cytochrome b5. Biochemistry 40 (2001) 4879-4891
49. Wang W.H., Lu J.X., Yao P., Xie Y., and Huang Z.X. The distinct heme coordination environments and heme-binding stabilities of His39Ser and His39Cys mutants of cytochrome b5. Protein Eng. 16 (2003) 1047-1054
50. Kortt, A. A., Trinick, M. J., Appleby, C. A. (1988). Amino acid sequences of hemoglobins I and II from root nodules of the non-leguminous Parasponia rigida-rhizobium symbiosis, and a correction of the sequence of hemoglobin I from Parasponia andersonii. 175, 141-149.
51. Bogusz, D., Appleby, C. A., Landsmann, J., Dennis, E. S., Trinick, M. J. & Peacock, W. J. (1988). Functioning haemoglobin genes in non-nodulating plants. 331, 178-180.
52. Trent III J.T., Hvitved A.N., and Hargrove M.S. A model for ligand binding to hexacoordinate hemoglobins. Biochemistry 40 (2001) 6155-6163
53. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (1997) 307-326
54. Pape T., and Schneider T.R. HKL2MAP: a graphical user interface for macromolecular phasing with SHELX programs. J. Appl. Crystallog. 37 (2004) 843-844
55. Terwilliger T.C., and Berendzen J. Automated MAD and MIR structure solution. Acta Crystallog. sect. D 55 (1999) 849-861
56. Terwilliger T.C. Maximum likelihood density modification. Acta Crystallog. sect. D 56 (2000) 965-972
57. Terwilliger T.C. Automated main-chain model-building by template-matching and iterative fragment extension. Acta Crystallog. sect. D 59 (2002) 34-44
58. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallog. sect. D. 60 (2004) 2126-2132
59. Vagin A., and Teplyakov A. MOLREP: an automated program for molecular replacement. J. Appl. Crystallog. 30 (1997) 1022-1025
60. CCP4. The CCP4 suite: programs for protein crystallography. Acta Crystallog. sect. D 50 (1994) 760-763
61. Jones T.A., Zou J.Y., Cowan S.W., and Kjeldgaard. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallog. sect. D 47 (1991) 110-119
62. Murshudov G.N., Vagin A.A., and Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallog. sect. D 53 (1997) 240-255
63. Kleywegt G.J. Use of non-crystallographic symmetry in protein structure refinement. Acta Crystallog. sect. D 52 (1996) 842-857
64. Guex N., and Peitsch M.C. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18 (1997) 2714-2723
65. Morgenstern B. DIALIGN: multiple DNA and protein sequence alignment at BiBiServ. Nucl. Acids Res. 32 (2004) W33-W36
66. Clamp M., Cuff J., Searle S.M., and Barton G.J. The Jalview Java alignment editor. Bioinformatics 20 (2004) 426-427
67. Arredondo-Peter R., Hargrove M.S., Sarath G., Moran J.F., Lohrman J., Olson J.S., and Klucas R.V. Rice hemoglobins. Gene cloning, analysis, and O2-binding kinetics of a recombinant protein synthesized in Escherichia coli. Plant Physiol. 115 (1997) 1259-1266
68. Hargrove M.S. A flash photolysis method to characterize hexacoordinate hemoglobin kinetics. Biophys. J. 79 (2000) 2733-2738