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Hemoglobin and Hypoxic Acclimation in Maize Root Tips

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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

  1. 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.

    Google Scholar 

  2. 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.

    Google Scholar 

  3. 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.

    Google Scholar 

  4. 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.

    Google Scholar 

  5. 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.

    Google Scholar 

  6. 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.

    Google Scholar 

  7. 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.

    Google Scholar 

  8. Hill, R.D., What Are Hemoglobins Doing in Plants? Can. J. Bot., 1998, vol. 76, pp. 707–712.

    Google Scholar 

  9. 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.

    Google Scholar 

  10. 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.

    Google Scholar 

  11. 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.

    Google Scholar 

  12. 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.

    Google Scholar 

  13. 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.

    Google Scholar 

  14. 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.

    Google Scholar 

  15. 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.

    Google Scholar 

  16. Armstrong, W., Aeration in Higher Plants, Adv. Bot. Res., 1979, vol. 7, pp. 225–332.

    Google Scholar 

  17. 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.

    Google Scholar 

  18. 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.

    Google Scholar 

  19. Mendelssohn, I.A. and Postek, M.T., Oxygen Deficiency in Spartina alterniflora Roots: Metabolic Adaptation to Anoxia, Science, 1982, vol. 214, pp. 181–191.

    Google Scholar 

  20. 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.

    Google Scholar 

  21. 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.

    Google Scholar 

  22. 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.

    Google Scholar 

  23. 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.

    Google Scholar 

  24. 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.

    Google Scholar 

  25. 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.

    Google Scholar 

  26. 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.

    Google Scholar 

  27. 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.

    Google Scholar 

  28. Dordas, C., Rivoal, J., and Hill, R.D., Plant Haemoglobins, Nitric Oxide and Hypoxic Stress, Ann. Bot., 2003, vol. 91, pp. 173–178.

    Google Scholar 

  29. Durner, J. and Klessig, D.F., Nitric Oxide as a Signal in Plants, Curr. Opin. Plant Biol., 1999, vol. 2, pp. 369–374.

    Google Scholar 

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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

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