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Stimulation of ethylene production and gas-space (aerenchyma) formation in adventitious roots of Zea mays L. by small partial pressures of oxygen

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Abstract

Adventitious roots of two to four-weekold intact plants of Zea mays L. (cv. LG11) were shorter but less dense after extending into stagnant, non-aerated nutrient solution than into solution continuously aerated with air. Dissolved oxygen in the non-aerated solutions decreased from 21 kPa to 3–9 kPa within 24 h. When oxygen partial pressures similar to those found in non-aerated solutions (3, 5 and 12 kPa) were applied for 7 d to root systems growing in vigorously bubbled solutions, the volume of gas-space in the cortex (aerenchyma) was increased several fold. This stimulation of aerenchyma was associated with faster ethylene production by 45-mm-long apical root segments. When ethylene production by roots exposed to 5 kPa oxygen was inhibited by aminoethoxyvinylglycine (AVG) dissolved in the nutrient solution, aerenchyma formation was also retarded. The effect of AVG was reversible by concomitant applications of 1-aminocyclopropane-1-carboxylic acid, an immediate precursor of ethylene. Addition of silver nitrate, an inhibitor of ethylene action, to the nutrient solution also prevented the development of aerenchyma in roots given 5 kPa oxygen. Treating roots with only 1 kPa oxygen stimulated ethylene production but failed to promote gas-space formation. These severely oxygen-deficient roots seemed insensitive to the ethylene produced since a supplement of exogeneous ethylene that promoted aerenchyma development in nutrient solution aerated with air (21 kPa oxygen) failed to do so in nutrient solution supplied with 1 kPa oxygen. Both ethylene production and aerenchyma formation were almost completely halted when roots were exposed to nutrient solutions devoid of oxygen. Thus both processes require oxygen and are stimulated by oxygen-deficient surroundings in the 3-to 12-kPa range of oxygen partial pressures when compared with rates observed in air (21 kPa oxygen).

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Abbreviations

ACC:

1-aminocyclopropane-1-carboxylic acid

AVG:

aminoethoxyvinylglycine

References

  • Armstrong, W. (1971) Oxygen diffusion from the roots of rice grown under non-waterlogged conditions. Physiol. Plant. 24, 242–247

    Google Scholar 

  • Armstrong, W. (1979) Aeration in higher plants. Adv. Bot. Res. 7, 225–231

    Google Scholar 

  • Barber, D.A., Lee, R.B. (1974) The effect of micro-organisms on the absorption of manganese by plants. New Phytol. 73, 97–106

    Google Scholar 

  • Bertani, A., Brambilla, I. (1982) Effect of decreasing oxygen concentration on wheat roots: growth and induction of anaerobic metabolism. Z. Pflanzenphysiol. 108, 283–288

    Google Scholar 

  • Bradford, K.J., Dilley, D.R. (1978) Effects of root anaerobiosis on ethylene production, epinasty and growth of tomato plants. Plant Physiol. 61, 506–509

    Google Scholar 

  • Bradford, K.J., Yang, S.F. (1981) Physiological responses of plants to waterlogging. HortScience 16, 25–30

    Google Scholar 

  • Burg, S.P. (1973) Ethylene in plant growth. Proc. Natl. Acad. Sci. USA 70, 591–597

    Google Scholar 

  • Burg, S.P., Burg, E.A. (1965) Gas exchange in fruits. Physiol. Plant. 18, 870–884

    Google Scholar 

  • Campbell, R., Drew, M.C. (1983) Electron microscopy of gas space (aerenchyma) formation in adventitious roots of Zea mays L. subjected to oxygen shortage. Planta 157, 350–357

    Google Scholar 

  • Drew, M.C., Jackson, M.B., Giffard, S. (1979) Ethylene-promoted adventitious rooting and development of cortical air spaces (aerenchyma) in roots may be adaptive responses to flooding in Zea mays L. Planta 147, 83–88

    Google Scholar 

  • Drew, M.C., Jackson, M.B., Giffard, S.C., Campbell, R. (1981) Inhibition by silver ions of gas space (aerenchyma) formation in adventitious roots of Zea mays L. subjected to exogenous ethylene or to oxygen deficiency. Planta 153, 217–224

    Google Scholar 

  • Drew, M.C., Saglio, P.H., Pradet, A. (1985) Larger adenylate energy charge and ATP/ADP ratios in aerenchymatous roots of Zea mays in anaerobic media as a consequence of improved internal oxygen transport. Planta 165, 51–58

    Google Scholar 

  • Hall, K.C. (1978) A gas chromatographic method for the determination of oxygen dissolved in water using an electron capture detector. J. Chromatogr. Sci. 16, 311–313

    Google Scholar 

  • Imaseki, H., Watanabe, A., Odawara, S. (1977) Role of oxygen in auxin-induced ethylene production. Plant Cell Physiol. 18, 577–586

    Google Scholar 

  • Jackson, M.B. (1982) Ethylene as a growth promoting hormone under flooded conditions. In: Plant growth substances 1982, pp. 291–301, Wareing, P.F. ed. Academic Press, London New York

    Google Scholar 

  • Jackson, M.B., Campbell, D.J. (1975) Movement of ethylene from roots to shoots, a factor in the responses of tomato plants to waterlogged soil conditions. New Phytol. 74, 397–406

    Google Scholar 

  • Jackson, M.B., Dobson, C.M., Herman, B., Merryweather, A. (1984) Modification of 3,5-diiodo-4-hydroxybenzoic acid (DIHB) activity and stimulation of ethylene production by small concentrations of oxygen in the root environment. Plant Growth Regul. 2, 251–262

    Google Scholar 

  • Jackson, M.B., Gales, K., Campbell, D.J. (1978) Effect of waterlogged soil conditions on the production of ethylene and on water relationships in tomato plants. J. Exp. Bot. 29, 183–193

    Google Scholar 

  • Kawase, M. (1981a) Effect of ethylene on aerenchyma development. am. J. Bot. 68, 651–658

    Google Scholar 

  • Kawase, M. (1981b) Anatomical and morphological adaptation of plants to waterlogging. HortScience 16, 30–34

    Google Scholar 

  • Konings, H. (1982) Ethylene-promoted formation of aerenchyma in seedling roots of Zea mays L. under aerated and non-aerated conditions. Physiol. Plant. 54, 119–124

    Google Scholar 

  • Konings, H., deWolf, A. (1984) Promotion and inhibition by plant growth regulators of aerenchyma formation in seedling roots of Zea mays. Physiol. Plant. 60, 309–314

    Google Scholar 

  • Konings, H., Jackson, M.B. (1979) A relationship between rates of ethylene production by roots and the promoting or inhibiting effects of exogenous ethylene and water on root elongation. Z. Pflanzenphysiol. 92, 385–397

    Google Scholar 

  • McPherson, D.C. (1939) Cortical airspaces in the roots of Zea mays L. New Phytol. 38, 190–202

    Google Scholar 

  • Norris, F. de la M. (1913) Production of air passages in the root of Zea mays by variation of the culture media. Proc. Bristol Nat. Soc. 4, 134–138

    Google Scholar 

  • Philipson, J.J., Coutts, M.P. (1978) The tolerance of tree roots to waterlogging. III. Oxygen transport in lodgepole pine and sitka spruce roots of primary structure. New Phytol. 80, 341–349

    Google Scholar 

  • Raskin, I., Kende, H. (1983a) Regulation of growth in rice seedlings. J. Plant Growth Regul. 2, 193–203

    Google Scholar 

  • Raskin, I., Kende, H. (1983b) Regulation of growth in stem sections of deep-water rice. Planta 160, 66–72

    Google Scholar 

  • Roberts, J.K.M., Callis, J., Jardetsky, O., Walbot, V., Freeling, M. (1984) Cytoplasmic acidosis as a determinant of flooding intolerance in plants. Proc. Natl. Acad. Sci. USA 81, 6029

    Google Scholar 

  • Saebø, A.S. (1974) The adaptive significance of aerenchyma in a waterlogged root environment. Blyttia 32, 21–32

    Google Scholar 

  • Saglio, P.H., Raymond, P., Pradet, A. (1983) Oxygen transport and root respiration of maize seedlings. A quantitative approach using the correlation between ATP/ADP and the respiration rate controlled by oxygen tension. Plant Physiol. 72, 1035–1039

    Google Scholar 

  • Smirnoff, N., Crawford, R.M.M. (1983) Variation in the structure and response to flooding of root aerenchyma in some wetland platns. Ann. Bot. 51, 237–249

    Google Scholar 

  • Vartapetian, B.B. (1973) Aeration of roots in relation to molecular oxygen transport in plants. In. Plant response to climatic factors. Proc. Uppsala Symp. 1970 (Ecology and conservation, 5), pp. 259–265, Unesco

  • Yang, S.F., Adams, D.O., Lizada, C., Yu, Y., Bradford, K.J., Cameron, A.C., Hoffman, N.E. (1980) Mechanism and regulation of ethylene biosynthesis. In: Plant growth substances 1979, pp. 219–229, Skoog, F., ed. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Yung, K.H., Yang, S.F., Schlenk, F. (1982) Methionine synthesis from 5-methylthioribose in apple tissue. Biochem. Biophys. Res. Commun. 105, 771–777

    Google Scholar 

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Jackson, M.B., Fenning, T.M., Drew, M.C. et al. Stimulation of ethylene production and gas-space (aerenchyma) formation in adventitious roots of Zea mays L. by small partial pressures of oxygen. Planta 165, 486–492 (1985). https://doi.org/10.1007/BF00398093

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