Abstract
Class 1 hemoglobins (Hbs) have a wide distribution in the plant kingdom and have been demonstrated in root, seed, stem, and leaf tissues. They are present at low concentrations in aerobic tissue, but their synthesis is rapidly induced by hypoxic stress. The pattern of expression of the maize Hb gene in roots of young maize plants exposed to hypoxia has been examined. Root Hb gene expression increased rapidly to a maximum within first two hours of hypoxia, then declining to prehypoxia levels within 48-h hypoxic exposure. Limiting oxygen supply to the roots by total plant immersion and darkness did not alter the time course of hemoglobin expression. Hb gene expression was about 20-fold higher in the stele than in the cortex of control, aerobically grown roots. Stele Hb expression increased about fourfold under hypoxic conditions, whereas its expression in the cortex increased about 60-fold. In these samples, alcohol dehydrogenase (Adh) gene expression increased about four- and ten fold in the stele and cortex, respectively. The effect of the state of the Hb on anoxic survival of maize root tips was assessed by exposing root tips to a carbon monoxide atmosphere to maximize the proportion of hemoglobin in the carbonmonoxy form. Carbon monoxide had no significant effect on the survival or the ATP levels in anoxic maize roots, regardless of whether they had been acclimated by exposure to a hypoxic pretreatment. This would suggest that the presence of oxyhemoglobin is not essential for the survival of anoxic root tips.
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REFERENCES
Saglio, P., Drew, M.C., and Pradet, A., Metabolic Adaptation to Anoxia Induced by Low (2-4 kPa Partial Pressure) Oxygen Pretreatment (Hypoxia) in Root Tips of Zea mays, Plant Physiol., 1988, vol. 86, pp. 61–66.
Bouny, J.M. and Saglio, P.H., Glycolytic Flux and Hexokinase Activities in Anoxic Maize Root Tips Acclimated by Hypoxic Pretreatment, Plant Physiol., 1996, vol. 111, pp. 187–194.
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., 1994, vol. 24, pp. 853–862.
Andersson, C.R., Jensen, E.O., Llewellyn, D.J., Dennis, E.S., and Peacock, W.J., A New Hemoglobin Gene from Soybean: A Role for Hemoglobin in All Plants, Proc. Natl. Acad. Sci. USA, 1996, vol. 93, pp. 5682–5687.
Trevaskis, B., Watts, R.A., Andersson, C., Llewellyn, D., Hargrove, M.S., Olson, J.S., Dennis, E.S., and Peacock, W.J., Two Hemoglobin Genes in Arabidopsis thaliana: The Evolutionary Origins of Leghemoglobins., Proc. Natl. Acad. Sci. USA, 1997, vol. 94, pp. 12230–12234.
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 Oxygen-Binding Kinetics of a Recombinant Protein Synthesized in Escherichia coli, Plant Physiol., 1997, vol. 115, pp. 1259–1266.
Duff, S.M.G., 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., 1997, vol. 272, pp. 16746–16752.
Hill, R.D., What Are Hemoglobins Doing in Plants? Can. J. Bot., 1998, vol. 76, pp. 707–712.
Nie, X.Z. and Hill, R.D., Mitochondrial Respiration and Hemoglobin Gene Expression in Barley Aleurone Tissue, Plant Physiol., 1997, vol. 114, pp. 835–840.
Sowa, A., Duff, S.M.G., Guy, P.A., and Hill, R.D., Altering Hemoglobin Levels Changes Energy Status in Maize Cells under Hypoxia, Proc. Natl. Acad. Sci. USA, 1998, vol. 95, pp. 10 317–10 321.
Mohapatra, S.S., Poole, R.J., and Dhindsa, R.S., Changes in Protein Patterns and Translatable Messenger RNA Populations during Cold Acclimation of Alfalfa, Plant Physiol., 1987, vol. 84, pp. 1172–1176.
Verwoerd, T.C., Dekker, B.M., and Hoekema, A., A Small-Scale Procedure for the Rapid Isolation of Plant RNAs, Nucleic Acids Res., 1989, vol. 17, p. 2362.
Saglio, P. and Pradet, A., Soluble Sugars, Respiration, and Energy Charge during Aging of Excised Maize Root Tips, Plant Physiol., 1980, vol. 66, pp. 516–519.
Saglio, P.H., Raymond, P., and Pradet, A., Metabolic Activity and Energy Charge of Excised Maize Root Tips under Anoxia: Control by Soluble Sugars., Plant Physiol., 1980, vol. 66, pp. 1053–1057.
Williams, W.T. and Barber, D.A., The Functional Significance of Aerenchyma in Plants, in Fifteenth Symposium of the Society of Experimental Biology, London: Soc. Exp. Biol., 1961, pp. 132–144.
Armstrong, W., Aeration in Higher Plants, Adv. Bot. Res., 1979, vol. 7, pp. 225–332.
DeWit, M.C.J., Morphology and Function of Roots and Shoot Growth of Crop Plants under Oxygen Deficiency, in Plant Life in Anaerobic Environments, Hook, D.D. and Crawford, R.M.M., Eds., Ann Arbor: Ann Arbor Sci. Publ. Inc., 1979, pp. 333–350.
Drew, M.C., Jackson, M.B., and Giffard, S., Ethylene-Promoted Adventitious Rooting and Development of Cortical Air Spaces (Aerenchyma) in Roots May Be Adaptive Responses to Flooding in Zea mays L., Planta, 1979, vol. 147, pp. 83–88.
Mendelssohn, I.A. and Postek, M.T., Oxygen Deficiency in Spartina alterniflora Roots: Metabolic Adaptation to Anoxia, Science, 1982, vol. 214, pp. 181–191.
Justin, S.H.F.W. and Armstrong, W., The Anatomical Characteristics of Roots and Plant Response to Soil Flooding, New Phytol., 1987, vol. 106, pp. 465–495.
Laan, P., Berrevoets, M.J., Lythe, S., Armstrong, W., and Blom, W.P.M., Root Morphology and Aerenchyma Formation as Indicators of the Flood-Tolerance of Rumex species, J. Ecol., 1989, vol. 77, pp. 693–703.
Armstrong, W. and Beckett, P.M., Internal Aeration and the Development of Stellar Anoxia in Submerged Roots. A Multishelled Mathematical Model Combining Axial Diffusion of Oxygen in the Cortex with Radial Losses to the Stele, the Wall Layers and the Rhizosphere, New Phytol., 1987, vol. 105, pp. 221–245.
Thomson, C.J. and Greenway, H., Metabolic Evidence for Stellar Anoxia in Maize Roots Exposed to Low O2 Concentrations., Plant Physiol., 1991, vol. 96, pp. 1294–1301.
Arechaga-Ocampo, E., Saenz-Rivera, J., Sarath, G., Klucas, R. V., and Arredondo-Peter, R., Cloning and Expression Analysis of Hemoglobin Genes from Maize (Zea mays ssp. mays) and Teosinte (Zea mays ssp. parviglumis), Biochim. Biophys. Acta, 2001, vol. 1522, pp. 1–8.
Duff, S.M.G., Guy, P.A., Nie, X., Durnin, D.C., and Hill, R.D., Haemoglobin Expression in Germinating Barley, Seed Sci. Res., 1998, vol. 8, pp. 431–436.
Guy, P.A., Sidaner, J.-P., Schroeder, S., Edney, M., MacGregor, A.W., and Hill, R.D., Embryo Phytoglobin Gene Expression as a Measure of Germination in Cereals, J. Cereal Sci., 2002, vol. 36, pp. 147–156.
Lira-Ruan, V., Sarath, G., Klucas, R.V., and Arredondo-Peter, R., Synthesis of Hemoglobins in Rice (Oryza sativa var. Jackson) Plants Growing in Normal and Stress Conditions, Plant Sci., 2001, vol. 161, pp. 279–287.
Dordas, C., Rivoal, J., and Hill, R.D., Plant Haemoglobins, Nitric Oxide and Hypoxic Stress, Ann. Bot., 2003, vol. 91, pp. 173–178.
Durner, J. and Klessig, D.F., Nitric Oxide as a Signal in Plants, Curr. Opin. Plant Biol., 1999, vol. 2, pp. 369–374.
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Silva-Cardenas, R.I., Ricard, B., Saglio, P. et al. Hemoglobin and Hypoxic Acclimation in Maize Root Tips. Russian Journal of Plant Physiology 50, 821–826 (2003). https://doi.org/10.1023/B:RUPP.0000003281.33108.84
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DOI: https://doi.org/10.1023/B:RUPP.0000003281.33108.84