Plant haemoglobins, nitric oxide and hypoxic stress

Annals of Botany

Volumn 91, Issue SPEC. ISS. JAN., 2003, Pages 173-178

  Dordas, Christos ^a   Rivoal, Jean ^a   Hill, Robert D ^a  

^a UNIVERSITY OF MANITOBA   (Canada)

Author keywords

Flooding tolerance; Haemoglobins; Hypoxic stress; Nitric oxide; Nonsymbiotic haemoglobins; Review

Indexed keywords

HEMOGLOBIN; NITRIC OXIDE; OXYGEN;

ADAPTATION; HEMOGLOBIN; HYPOXIA; PLANT; FLOODING; TOLERANCE;

EVOLUTION; METABOLISM; PLANT PHYSIOLOGY; REVIEW;

EVOLUTION; HEMOGLOBINS; NITRIC OXIDE; OXYGEN; PLANT PHYSIOLOGY;

DICOTYLEDONEAE;

EID: 0037239014     PISSN: 03057364     EISSN: None     Source Type: Journal    
DOI: 10.1093/aob/mcf115     Document Type: Review

References (65)

1. Andersson CR, Jensen EO, Llewellyn DJ, Dennis ES, Peacock WJ. 1996. A new hemoglobin gene from soybean: a role for hemoglobin in all plants. Proceedings of the National Academy of Sciences of the USA 93: 5682-5687.
2. Antonini E, Brunori M, Wyman J, Noble RW. 1966. Preparation and kinetic properties of intermediates in the reaction of hemoglobin with ligands. Journal of Biological Chemistry 241: 3236-3238.
3. Appleby CA. 1992. The origin and functions of haemoglobin in plants. Science in Progress 76: 365-398.
4. Appleby CA, Tjepkema JD, Trinick MJ. 1983. Hemoglobin in a nonleguminous plant, Parasponia: possible genetic origin and function in nitrogen fixation. Science 220: 951-953.
5. Arechaga-Ocampo E, Saenz-Rivera J, Sarath G, Klucas RV, Arredondo-Peter R. 2001. Cloning and expression analysis of hemoglobin genes from maize (Zea mays ssp. mays) and teosinte (Zea mays ssp. parviglumis). Biochimica et Biophysica Acta 1522: 1-8.
6. Arredondo-Peter R, Hargrove MS, Moran JF, Sarath G, Klucas RV. 1998. Plant hemoglobins. Plant Physiology 118: 1121-1126.
7. Arredondo-Peter R, Hargrove MS, Sarath G, Moran JF, Lohrman J, Olson JS, Klucas RV. 1997. Rice hemoglobins: gene cloning, analysis and oxygen-binding kinetics of a recombinant protein synthesized in Escherichia coli. Plant Physiology 115: 1259-1266.
8. Barroso JB, Corpas FJ, Carreras A, Sandalio LM, Valderrama R, Palma JM, Lupianez JA, del Rio LA. 1999. Localization of nitric-oxide synthase in plant peroxisomes. Journal of Biological Chemistry 274: 36729-36733.
9. Bogusz D, Appleby CA, Landsmann J, Dennis ES, Trinick MJ, Peacock WJ. 1988. Functioning haemoglobin genes in non-nodulating plants. Nature 331: 178-180.
10. Bogusz D, Llewellyn J, Craig S, Dennis ES, Appleby CA, Peacock WJ. 1990. Nonlegume hemoglobin genes retain organ-specific expression in heterologous transgenic plants. Plant Cell 2: 633-641.
11. Botrel A, Kaiser WM. 1997. Nitrate reductase activation state in barley roots in relation to the energy and carbohydrate status. Planta 201: 496-501.
12. Cassoly R, Gibson Q. 1975. Conformation, co-operativity and ligand binding in human hemoglobin. Journal of Molecular Biology 91: 301-313.
13. Christensen T, Dennis ES, Peacock WJ, Landsmann J, Marcker KA. 1991. Hemoglobin genes in non-legumes: cloning and characterization of a Casuarina glauca hemoglobin gene. Plant Molecular Biology 16: 339-344.
14. Clarke A, Desikan R, Hurst RD, Hancock JT, Neill SJ. 2000. NO way back: nitric oxide and programmed cell death in Arabidopsis thaliana suspension cultures. Plant Journal 24: 667-677.
15. Couture M, Chamberland H, St Pierre B, LaFontaine J, Guertin M. 1994. Nuclear gene encoding chloroplast hemoglobins in the unicellular green alga Chlamydomonas eugametos. Molecular and General Genetics 243: 185-197.
16. Crawford RMM. 1978. Metabolic adaptations to anoxia. In Hook DD, Crawford RMM, eds. Plant life in anaerobic environments. Ann Arbor: Ann Arbor Science Publishers, 119-136.
17. Cueto M, Hernandez-Perera O, Martin R, Bentura ML, Rodrigo J, Lamas S, Golvano MP. 1996. Presence of nitric oxide synthase activity in roots and nodules of Lupinus albus. FEBS Letters 398: 159-164.
18. Dordas C, Hasinoff BB, Rivoal J, Hill RD. 2002. Expression of a stress-induced hemoglobin affects NO levels produced by maize and alfalfa under hypoxic stress. Manuscript submitted.
19. Doyle MP, Hoekstra JW. 1981. Oxidation of nitrogen oxides by bound dioxygen in hemoproteins. Journal of Inorganic Biochemistry 14: 351-358.
20. Drew MC. 1997. Oxygen deficiency and root metabolism: injury and acclimation under hypoxia. Annual Review of Plant Physiology and Plant Molecular Biology 48: 223-250.
21. Drew MC, Cobb BG, Johnson JR, Andrews D, Morgan PW, Jordan W, He CJ. 1994. Metabolic acclimation of root tips to oxygen deficiency. Annals of Botany 74: 281-286.
22. Drew MC, He CJ, Morgan PW. 1989. Decreased ethylene biosynthesis, and induction of aerenchyma, by nitrogen- or phosphate-starvation in adventitious roots of Zea mays L. Plant Physiology 91: 266-271.
23. Drew MC, He I, I, Morgan PW. 2000. Programmed cell death and aerenchyma formation in roots. Trends in Plant Sciences 5: 123-127.
24. Duff SMG, Wittenberg JB, Hill RD. 1997. Expression, purification, and properties of recombinant barley (Hordeum sp.) hemoglobin: optical spectra and reactions with gaseous ligands. Journal of Biological Chemistry 272: 16746-16752.
25. Durner J, Klessig DF. 1999. Nitric oxide as a signal in plants. Current Opinion in Plant Biology 2: 369-374.
26. Durner J, Wendehenne D, Klessig DF. 1998. Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proceeding of the National Academy of Sciences of the USA 95: 10328-10333.
27. Eich RF, Li T, Lemon DD, Doherty DH, Curry SR, Aitken JF, Mathews A J, Johnson KA, Smith RD, Phillips Jr GN, Olson JS. 1996. Mechanism of NO-induced oxidation of myoglobin and hemoglobin. Biochemisty 35: 6976-6983.
28. Ferrari TE, Varner JE. 1971. Intact tissue assay for nitrite reductase in barley aleurone layers. Plant Physiology 47: 790-794.
29. Furchgott RF. 1990. The 1989 Ulf von Euler lecture. Studies on endothelium-dependent vasodilation and the endothelium-derived relaxing factor. Acta Physiologica Scandinavica 139: 257-270.
30. Gardner PR, Gardner AM, Martin LA, Salzman AL. 1998. Nitric oxide dioxygenase: an enzymic function for flavohemoglobin. Proceedings of the National Academy of Sciences of the USA 95: 10378-10383.
31. Gibson QH, Smith MH. 1965. Rates of reaction of Ascaris haemoglobins with ligands. Proceedings of the Royal Society of London. Series B Biological Sciences 163: 206-214.
32. Gibson QH, Wittenberg JB, Wittenberg BA, Bogusz D, Appleby CA. 1989. The kinetics of ligand binding to plant hemoglobins. Journal of Biological Chememistry 264: 100-107.
33. Guy PA, Hill RD. 2000. Zea Mays hemoglobin mRNA, complete cds. Genbank AF236080.
34. Guy PA, Sidaner J-P, Schroeder S, Edney M, MacGregor AW, Hill RD. 2002. Embryo phytoglobin gene expression as a measure of germination in cereals. Journal of Cereal Science (in press).
35. He CJ, Morgan PW, Drew MC. 1992. Enhanced sensitivity to ethylene in nitrogen- or phosphate-starved roots of Zea mays L. during aerenchyma formation. Plant Physiology 98: 137-142.
36. Hendriks T, Scheer I, Quillet MC, Randoux B, Delbreil B, Vasseur J, Hilbert JL. 1998. A nonsymbiotic hemoglobin gene is expressed during somatic embryogenesis in Cichorium. Biochimica et Biophysica Acta 1443: 193-197.
37. Hill RD. 1998. What are hemoglobins doing in plants? Canadian Journal of Botany 76: 707-712.
38. Hunt PW, Watts RA, Trevaskis B, Llewelyn DJ, Burnell J, Dennis ES, Peacock WJ. 2001. Expression and evolution of functionally distinct haemoglobin genes in plants. Plant Molecular Biology 47: 677-692.
39. Ignarro LJ. 1992. Haem-dependent activation of cytosolic guanylate cyclase by nitric oxide: a widespread signal transduction mechanism. Biochemical Society Transactions 20: 465-469.
40. Jackson MB. 1985. Ethylene and responses of plants to soil waterlogging and submergence. Annual Review of Plant Physiology 36: 145-174.
41. Jakob W, Webster DA, Kroneck PM. 1992. NADH-dependent methemoglobin reductase from the obligate aerobe Vitreoscilla: improved method of purification and reexamination of prosthetic groups. Archives of Biochemistry and Biophysics 292: 29-33.
42. Kiger L, Rashid AK, Griffon N, Haque M, Moens L, Gibson QH, Poyart C, Marden MC. 1998. Trematode hemoglobins show exceptionally high oxygen affinity. Biophysical Journal 75: 990-998.
43. Kim PK, Zamora R, Petrosko P, Billiar TR. 2001. The regulatory role of nitric oxide in apoptosis. International Immunopharmacology 1: 1421-1441.
44. Kubo H. 1939. Über hämoprotein aus den wurzelknöllchen von leguminosen. Acta Phytochimica (Tokyo) 11: 195-200.
45. Landsmann J, Dennis ES, Higgins TJV, Appleby CA, Kortt A, Peacock WJ. 1986. Common evolutionary origin of legume and non-legume plant haemoglobins. Nature 324: 166-168.
46. McDonald LJ, Murad F. 1996. Nitric oxide and cyclic GMP signaling. Proceeding of the Society for Experimental Biology and Medicine 211: 1-6.
47. Minning DM, Gow AJ, Bonaventura J, Braun R, Dewhirst M, Goldberg DE, Stamler JS. 1999. Ascaris haemoglobin is a nitric oxide-activated 'deoxygenase'. Nature 401: 497-502.
48. Nie XZ, Hill RD. 1997. Mitochondrial respiration and hemoglobin gene expression in barley aleurone tissue. Plant Physiology 114: 835-840.
49. Poole RK. 1994. Oxygen reactions with bacterial oxidases and globins: binding, reduction and regulation. Antonie van Leeuwenhoek 65: 289-310.
50. Poole RK, Hughes MN. 2000. New functions for the ancient globin family: bacterial responses to nitric oxide and nitrosative stress. Molecular Microbiology 36: 775-783.
51. Ribeiro EA, Jr. Cunha FQ, Tamashiro WM, Martins IS. 1999. Growth phase-dependent subcellular localization of nitric oxide synthase in maize cells. FEBS Letters 445: 283-286.
52. Sasaki T, Song J, Koga-Ban Y, Matsui E, Fang F, Higo H, Nagasaki H, Hori M, Miya M, Murayama-Kayano E, Takiguchi T, Takasuga A, Niki T, Ishimaru K, Ikeda H, Yamamoto Y, Mukai T, Ohta I, Miyadera N, Havukkala I, Minobe Y. 1994. Toward cataloguing all rice genes: large scale sequencing of randomly chosen rice cDNAs from a callus cDNA library. Plant Journal 6: 615-624.
53. Serégelyes C, Mustárdy L, Ayaydin F, Sass L, Kovács L, Endre G, Lukács N, Kovács I, Vass I, Kiss GB, Horváth GV, Dudits D. 2000. Nuclear localization of a hypoxia-inducible novel non-symbiotic hemoglobin in cultured alfalfa cells. FEBS Letters 482: 125-130.
54. Sowa A, Duff SMG, Guy PA, Hill RD. 1998. Altering hemoglobin levels changes energy status in maize cells under hypoxia. Proceedings of the National Academy of Sciences of the USA 95: 10317-10321.
55. Springer BA, Egeberg KD, Sligar SG, Rohlfs RJ, Mathews AJ, Olson JS. 1989. Discrimination between oxygen and carbon monoxide and inhibition of autooxidation by myoglobin. Site-directed mutagenesis of the distal histidine. Journal of Biological Chemistry 264: 3057-3060.
56. Stöhr C, Strube F, Marx G, Ullrich WR, Rockel P. 2001. A plasma membrane-bound enzyme of tobacco roots catalyses the formation of nitric oxide from nitrite. Planta 212: 835-841.
57. Taylor ER, Nie XZ, MacGregor AW, Hill RD. 1994. A cereal haemoglobin gene is expressed in seed and root tissues under anaerobic conditions. Plant Molecular Biology 24: 853-862.
58. Tiedje JM, Sexstone AJ, Myrold DD, Robinson JA. 1982. Denitrification: ecological niches, competition and survival. Antonie van Leeuwenhoek 48: 569-583.
59. Trevaskis B, Watts RA, Andersson C, Llewellyn D, Hargrove MS, Olson JS, Dennis ES, Peacock WJ. 1997. Two hemoglobin genes in Arabidopsis thaliana: the evolutionary origins of leghemoglobins. Proceedings of the National Academy of Sciences of the USA 94: 12230-12234.
60. Wang R, Guegler K, LaBrie ST, Crawford NM. 2000. Genomic analysis of a nutrient response in arabidopsis reveals diverse expression patterns and novel metabolic and potential regulatory genes induced by nitrate. Plant Cell 12: 1491-1510.
61. Watts RA, Hunt PW, Hvitved AN, Hargrove MS, Peacock WJ, Dennis ES. 2001. A hemoglobin from plants homologous to truncated hemoglobins of microorganisms. Proceeding of the National Academy of Sciences of the USA 98: 10119-10124.
62. Wennmalm A, Benthin G, Petersson AS. 1992. Dependence of the metabolism of nitric oxide (NO) in healthy human whole blood on the oxygenation of its red cell haemoglobin. British Journal of Pharmacology 106: 507-508.
63. Wittenberg JB, Wittenberg BA. 1990. Mechanisms of cytoplasmic hemoglobin and myoglobin function. Annual Review of Biophysics and Biophysical Chemistry 19: 217-241.
64. Yamasaki H, Sakihama Y. 2000. Simultaneous production of nitric oxide and peroxynitrite by plant nitrate reductase: in vitro evidence for the NR-dependent formation of active nitrogen species. FEBS Letters 468: 89-92.
65. Zhu H, Riggs AF. 1992. Yeast flavohemoglobin is an ancient protein related to globins and a reductase family Fnr, a global transcriptional regulator of Escherichia coli, activates the Vitreoscilla hemoglobin (VHb) promoter and intracellular VHb expression increases cytochrome d promoter activity. Proceedings of the National Academy of Sciences of the USA 89: 5015-5019.