Hostname: page-component-669899f699-8p65j Total loading time: 0 Render date: 2025-04-30T09:17:16.153Z Has data issue: false hasContentIssue false
  • English
  • Français

Hormone action and plant adaptations to poor aeration

Published online by Cambridge University Press:  05 December 2011

Michael B. Jackson
Michael B. Jackson
Affiliation:
Department of Agricultural Sciences, University of Bristol, AFRC Institute of Arable Crops Research, Long Ashton Research Station, Bristol, BS18 9AF, UK
Get access

Synopsis

The actions of endogenous plant hormones are invoked to explain several morphological adaptations to poor aeration. These include changes to the growth and internal morphology of inundated roots, the promotion of extension growth by stems or leaves of aquatic and semi-aquatic species by submergence, and morphological changes in shoots where only the roots and lower shoot are inundated. This article considers ethylene-promoted aerenchyma formation in maize (Zea mays) and compares the promoting action of ethylene, low oxygen partial pressures and carbon dioxide on shoot extension in rice (Oryza sativa), a rice mimic Echinochloa oryzoides and a submersed aquatic monocot Potamogeton pecrinatus. Different kinds of hormonal messages (positive, negative, accumulative and debit) passing between roots and shoots co-ordinate shoot development with the roots and their environment. Recent progress in quantifying the delivery of abscisic acid (ABA) or the ethylene precursor 1-aminocyclopropane-1-car-boxylic acid (ACC) from roots to shoots in the transpiration stream is summarised in relation to control of stomatal closure and leaf epinastic curvature in flooded plants.

Type
Research Article
Information
Proceedings of the Royal Society of Edinburgh, Section B: Biological Sciences , Volume 102: Oxygen and Environmental Stress in Plants , 1994 , pp. 391 - 405
Copyright
Copyright © Royal Society of Edinburgh 1994

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Anderson, L. W. J. 1978. Abscisic acid induces formation of floating leaves in the heterophyllous aquatic angiosperm Potamogeton nodosus. Science 210, 1135–8.CrossRefGoogle Scholar
Armstrong, W., Cringle, S., Brown, M. & Greenway, H. 1993. In Jackson, M. B. & Black, C. R. (Ed.) Interacting stresses in plants in a changing climate, pp. 287–304. Heidelberg: Springer-Verlag.CrossRefGoogle Scholar
Armstrong, W., Beckett, P. M., Justin, S. H. F. W. & Lythe, S. 1991. Modelling, and other aspects of root aeration by diffusion. In Jackson, M. B., Davies, D. D. & Lambers, H. (Eds), Plant life under oxygen deprivation. Ecology, physiology and biochemistry, pp. 267–82. The Hague: SPB Academic.Google Scholar
Attwood, P. A. 1993 Tolerance and growth of willow (Salix viminalis) and willow mycorrhiza in oxygen deficient environments. PhD Thesis, University of Bristol.Google Scholar
Atwell, B. J., Drew, M. C. & Jackson, M. B. 1988. The influence of oxygen deficiency on ethylene synthesis, 1-aminocyclopropane-1-carboxylic acid levels and aerenchyma formation in roots of Zea mays. Physiologia Plantarum 72, 15–22.CrossRefGoogle Scholar
Baluška, F., Brailsford, R. W., Hauskrecht, M., Jackson, M. B. & Barlow, P. W. 1994. Differential morphogenesis in the maize root cortex: involvement of microtubules and phytohormones during post-mitotic cell growth in relation to aerenchyma formation and other responses to environmental stress. Botanica Ada 106, 394–404.CrossRefGoogle Scholar
Bradford, K. J. & Yang, S. F. 1980. Xylem transport of 1-aminocyclopropane-1-carboxylic acid, an ethylene precursor, in waterlogged plants. Plant Physiology 65, 322–6.CrossRefGoogle Scholar
Brailsford, R., Voesenek, L. A. C. J., Blom, C. W. P. M., Smith, A. R., Hall, M. A. & Jackson, M. B. 1993. Enhanced ethylene production by primary roots of Zea mays L. in response to sub-ambient partial pressures of oxygen. Plant, Cell and Environment 16 (in press).CrossRefGoogle 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, 350–7.CrossRefGoogle ScholarPubMed
Cannell, R. Q. & Jackson, M. B. 1981. Alleviating aeration stress. In Arkin, G. E. & Taylor, H. M. (Eds) Modifying the root environment to reduce crop stress, pp. 139–92. St Joseph, USA: American Society of Agricultural Engineers.Google Scholar
Cohen, E. & Kende, H. 1987. In vivo 1-aminocyclopropane-1-carboxylate synthase activity in internodes of deep-water rice. Enhancement by submergence and low oxygen levels. Plant Physiology 84, 282–6.CrossRefGoogle Scholar
Cookson, C. & Osborne, D. J. 1978. The stimulation of cell extension by ethylene and auxin in aquatic plants. Planta 144, 39–47.CrossRefGoogle ScholarPubMed
Crawford, R. M. M. 1982. The anaerobic retreat as a survival strategy for aerobic plants and animals. Transactions of the Botanical Society of Edinburgh 44, 57–63.CrossRefGoogle Scholar
English, P. J., Lycett, G. W., Roberts, K. C., Hall, K. C. & Jackson, M. B. 1993. The use of antisense transgenic tomato plants to study the role of ethylene in responses to waterlogging. In Pech, J. C., Latche, A. & Balague, C. (Eds) Cellular and molecular aspects of the plant hormone ethylene, pp. 261–2. Dordrecht: Kluwer Academic.CrossRefGoogle Scholar
Hall, K. C., Else, M. A. and Jackson, M. B. 1993. Determination of 1-aminocyclopropane-1-carboxylic acid (ACC) in leaf tissue and xylem sap using capillary column gas chromatography and a nitrogen/phosphorus detector. Plant Growth Regulation 13, 225–30.CrossRefGoogle Scholar
He, C., Morgan, P. W., Jordan, W. R. & Drew, M. C. 1993. The role of calcium in aerenchyma development in roots of maize. Plant Physiology 102, 159 (abstract 910).Google Scholar
Hiron, R. W. P. & Wright, S. T. C. 1973. The role of endogenous abscisic acid in the response of plants to stress. Journal of Experimental Botany 24, 769–81.CrossRefGoogle Scholar
Hoffmann-Benning, S. & Kende, H. 1992. On the role of abscisic acid and gibberellin in the regulation of growth in rice. Plant Physiology 99, 1156–61.CrossRefGoogle ScholarPubMed
Horton, R. F. 1987. Ethylene-induced growth in amphibious plants. In Klambt, D. (Ed.) Plant hormone receptors, NATO ASI Series vol. H10, pp. 249–56. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Horton, R. F. 1991. The effect of ethylene and other regulators on coleoptile growth of rice under anoxia. Plant Science 79, 57–62.CrossRefGoogle Scholar
Jackson, M. B. 1982. Ethylene as a growth promoting hormone under flooded conditions. In Wareing, P. F. (Ed.) Plant growth substances 1982, pp. 291–301. London: Academic Press.Google Scholar
Jackson, M. B. 1987. A structured evaluation of the involvement of ethylene and abscisic acid in plant responses to aeration stress. In Hoad, G. V., Lenton, J. R., Jackson, M. B. & Atkin, R. K. (Eds) Hormone action in plant development. A critical appraisal, pp. 189–99. London: Butterworths.CrossRefGoogle Scholar
Jackson, M. B. 1989. Regulation of aerenchyma formation in roots and shoots by oxygen and ethylene. In Osborne, D. J. & Jackson, M. B. (Eds) Cell separation in plants. Physiology, biochemistry and molecular biology, pp. 263–74. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Jackson, M. B. 1990. Hormones and developmental changes in plants subjected to submergence or soil waterlogging. Aquatic Botany 38, 49–72.CrossRefGoogle Scholar
Jackson, M. B. 1991. Regulation of water relationships in flooded plants by ABA from leaves, roots and xylem sap. In Davies, W. J. & Jones, H. G. (Eds) Abscisic acid physiology and biochemistry, pp. 217–26. Oxford: Bios Scientific.Google Scholar
Jackson, M. B. 1993. Are plant hormones involved in root to shoot communication? Advances in Botanical Research 19, 103–87.CrossRefGoogle Scholar
Jackson, M. B. & Campbell, D. J. 1976. Waterlogging and petiole epinasty in tomato: the role of ethylene and low oxygen. The New Phytologist 76, 21–9.CrossRefGoogle Scholar
Jackson, M. B. & Drew, M. C. 1984. Effects of flooding on growth and metabolism of herbaceous plants. In Kozlowski, T. T. (Ed.) Flooding and plant growth, pp. 47–128. New York: Academic Press.CrossRefGoogle Scholar
Jackson, M. B. & Hall, K. C. 1987. Early stomatal closure in waterlogged pea plants is mediated by abscisic acid in the absence of foliar water deficits. Plant, Cell and Environment 10, 121–30.CrossRefGoogle Scholar
Jackson, M. B. & Hall, K. C. 1993. Polyamine content and action in roots of Zea mays L. under conditions of oxygen deprivation and ethylene enrichment in relation to aerenchyma development. Annals of Botany 72, 569–75.CrossRefGoogle Scholar
Jackson, M. B., Morrow, I. B. & Osborne, D. J. 1972. Abscission and dehiscence in the squirting cucumber, Ecballium elaterium. Regulation by ethylene. Canadian Journal of Botany 50, 1465–71.CrossRefGoogle 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. Journal of Experimental Botany 29, 183–93.CrossRefGoogle Scholar
Jackson, M. B., Fenning, T. M. & Jenkins, W. 1985. Aerenchyma (gas space) formation in adventitious roots of rice (Oryza sativa L.) is not controlled by ethylene or small partial pressures of oxygen. Journal of Experimental Botany 36, 1566–72.CrossRefGoogle Scholar
Jackson, M. B., Waters, I., Setter, T. & Greenway, H. 1987. Injury to rice plants by complete submergence: a contribution by ethylene (ethene). Journal of Experimental Botany 38, 1826–38.CrossRefGoogle Scholar
Jackson, M. B., Young, S. F. & Hall, K. C. 1988. Are roots a source of abscisic acid for the shoots of flooded pea plants? Journal of Experimental Botany 36, 1631–7.CrossRefGoogle Scholar
Justin, S. H. F. & Armstrong, W. 1991a. A reassessment of the influence of NAA on aerenchyma formation in maize roots. The New Phytologist 111, 607–18.CrossRefGoogle Scholar
Justin, S. H. F. & Armstrong, W. 1991b. Evidence for the involvement of ethene in aerenchyma formation of adventitious roots of rice (Oryza sativa L.). The New Phytologist 118, 49–62.CrossRefGoogle Scholar
Kang, B. G., Park, W. J., Nam, Hee & Hertel, R. 1992. Ethylene-induced increase of sensitivity to auxin in Ranunculus petioles and its implications regarding ethylene action and adaptation. In Karssen, C. M., Van Loon, L. C. & Vreugdenhil, D. (Eds) Progress in plant growth regulation, pp. 248–53. Dordrecht: Kluwer Academic.CrossRefGoogle Scholar
Kende, H. 1987. Studies on internodal growth using deep-water rice. In Cosgrove, D. J. & Knievel, D. P. (Eds) Physiology of cell expansion during growth, pp. 221–38. Rockville, USA: American Society of Plant Physiologists.Google Scholar
Konings, H. & de Wolf, A. 1984. Promotion and inhibition by plant growth regulators of aerenchyma formation in seedling roots of Zea mays. Physiologia Plantarum 60, 309–14.CrossRefGoogle Scholar
Ku, H. S., Suge, H., Rappaport, L. & Pratt, H. K. 1970. Stimulation of rice coleoptile growth by ethylene. Planta 90, 333–9.CrossRefGoogle ScholarPubMed
Kutschera, U. & Kende, H. 1988. The biophysical basis of elongation growth in internodes of deepwater rice. Plant Physiology 88, 361–6.CrossRefGoogle ScholarPubMed
McComb, A. J. 1965. The control of elongation in Callitriche shoots by environment and gibberellic acid. Annals of Botany 29, 445–58.CrossRefGoogle Scholar
Mees, G. C. & Weatherley, P. E. 1957. The mechanism of water absorption by roots II. The role of hydraulic pressure gradients across roots. Proceedings of the Royal Society (London), Series B 14, 381–91.Google Scholar
Menegus, F., Catteruzza, L. & Ragg, E. 1992. Effects of oxygen level on metabolism and development of seedlings of Trapa natans and two ecologically related species. Physiologia Plantarum 86, 168–72.CrossRefGoogle Scholar
Mujer, C. V., Rumpho, M. E., Lin, J-J. & Kennedy, R. A. 1993. Constitutive and inducible aerobic and anaerobic proteins in the Echinochloa complex and rice. Plant Physiology 101, 217–26.CrossRefGoogle ScholarPubMed
Musgrave, A., Jackson, M. B. & Ling, E. 1972. Callitriche stem elongation is controlled by ethylene and gibberellin. Nature New Biology 236, 93–6.CrossRefGoogle Scholar
Neuman, D. S. & Smit, B. 1991. The influence of leaf water status and ABA on leaf growth and stomata of Phaseolus seedlings with hypoxic roots. Journal of Experimental Botany 42, 1499–506.CrossRefGoogle Scholar
Neuman, D. S.. Rood, S. B. & Smit, B. A. 1990. Does cytokinin transport from root to shoot in the xylem regulate leaf responses to root hypoxia? Journal of Experimental Botany 41, 1325–33.CrossRefGoogle Scholar
Pearce, D. M. E. & Jackson, M. B. 1991. Comparison of growth responses of barnyard grass (Echinochloa oryzoides) and rice (Oryza sativa) to submergence, ethylene, carbon dioxide and oxygen shortage. Annals of Botany 68, 201–9.CrossRefGoogle Scholar
Pearce, D. M. E., Hall, K. C. & Jackson, M. B. 1992. The effects of oxygen, carbon dioxide and ethylene on ethylene biosynthesis in relation to shoot extension of rice (Oryza sativa) and barnyard grass (Echinochloa oryzoides). Annals of Botany 69, 441–7.CrossRefGoogle Scholar
Raskin, I. & Kende, H. 1983. Regulation of growth in rice seedlings. Journal of Plant Growth Regulation 2, 193–203.CrossRefGoogle Scholar
Raskin, I. & Kende, H. 1984. Regulation of growth in stem sections of deep-water rice. Planta 160, 66–72.CrossRefGoogle ScholarPubMed
Reggiani, R., Hochkoeppler, A. & Bertani, A. 1989. Polyamines and anaerobic elongation of rice coleoptile. Plant and Cell Physiology 30, 893–8.CrossRefGoogle Scholar
Ridge, I. 1992. Sensitivity in a wider context: ethylene and petiole growth in Nymphoides peltata. In Karssen, C. M., Van Loon, L. C. & Vreugdenhill, D. (Eds) Progress in plant growth regulation, pp. 254–63. Dordrecht: Kluwer Academic.CrossRefGoogle Scholar
Rosl, F. 1992. A simple and rapid method for detection of apoptosis in human cells. Nucleic Acids Research 20, 5243.CrossRefGoogle ScholarPubMed
Sand-Jensen, K. 1987. Environmental control of bicarbonate use among freshwater and marine macrophytes. In Crawford, R. M. M. (Ed.) Plant life in aquatic and amphibious habitats, pp. 99–112. Oxford: Blackwells Scientific.Google Scholar
Sauter, M. & Kende, H. 1992. Gibberellin-induced growth and regulation of cell division cycle in deepwater rice. Planta 188, 362–8.CrossRefGoogle ScholarPubMed
Sauter, M., Seagull, R. W. & Kende, H. 1993. Internodal elongation and orientation of cellulose microfibrils and microtubules in deepwater rice. Planta 190, 354–62.CrossRefGoogle Scholar
Setter, T. L., Waters, I., Wallace, I., Bhekasut, P. & Greenway, H. 1989. Submergence of rice I. Growth and photosynthetic response to CO2 enrichment of flood water. Australian Journal of Plant Physiology 16, 251–64.Google Scholar
Smit, B. A., Neumann, D. S. & Stachowiak, M. L. 1990. Root hypoxia reduces leaf growth - role of factors in the transpiration stream. Plant Physiology 92, 1021–8.CrossRefGoogle ScholarPubMed
Smith, J. J. & John, P. 1993. Maximising the activity of the ethylene-forming enzyme. In Pech, J. C., Latche, A. & Balague, C. (Eds) Cellular and molecular aspects of the plant hormone ethylene, pp. 33–8. Dordrecht: Kluwer Academic.CrossRefGoogle Scholar
Suge, H. & Kusanagi, T. 1975. Ethylene and carbon dioxide: regulation of growth in two perennial aquatic plants, arrow head and pond weed. Plant and Cell Physiology 16, 65–72.CrossRefGoogle Scholar
Summers, J. E. & Jackson, M. B. 1993. Promotion of stem extension in an aquatic monocot (Potamogeton pectinatus L.) by the complete absence of oxygen and by partial oxygen shortage. In Jackson, M. B. & Black, C. R. (Eds) Interacting stresses in plants in a changing climate, pp. 315–25. Heidelberg: Springer-Verlag.CrossRefGoogle Scholar
Thomson, C. J. & Greenway, H. 1991. Metabolic evidence for stelar anoxia in maize roots exposed to low O2 concentrations. Plant Physiology 96, 1294–301.CrossRefGoogle Scholar
Van Der Sman, A. J. M., Voesenek, L. A. C. J., Blom, C. W. P. M., Harren, F. J. M. & Reuss, J. 1991. The role of ethylene in shoot elongation with respect to survival and seed output of flooded Rumex maritimus L. plants. Functional Ecology 5, 304–13.CrossRefGoogle Scholar
Wang, T-W. & Arteca, J. M. 1992. Effects of low O2 root stress on ethylene biosynthesis in tomato plants (Lycopersicon esculentum Mill. cv. Heinz 1350). Plant Physiology 92, 97–107.CrossRefGoogle Scholar
Woodrow, L., Thompson, R. G. & Grodzinski, B. 1988. Effects of ethylene on photosynthesis and partitioning in tomato, Lycopersicon esculentum Mill. Journal of Experimental Botany 39, 667–84.CrossRefGoogle Scholar
Wright, S. T. C. & Hiron, R. W. P. 1972. The accumulation of abscisic acid in plants under wilting and other stress condition. In Carr, D. J. (Ed.). Plant growth substances 1970, pp. 291–8. Heidelberg: Springer Verlag.CrossRefGoogle Scholar
Young, J. P., Dengler, N. G. & Horton, R. F. 1987. Heterophylly in Ranunculus flabellaris: the effect of abscisic acid on leaf anatomy. Annals of Botany 60, 117–25.CrossRefGoogle Scholar
Zarembinski, T. I. & Theologis, A. 1993. Anaerobiosis and plant growth hormones induce two genes encoding 1-aminocyclopropane-l-carboxylate synthase in rice (Oryza sativa L.). Molecular Biology of the Cell 4, 363–73.CrossRefGoogle Scholar
Zhang, J. & Davies, W. J. 1987. ABA in roots and leaves of flooded pea plants. Journal of Experimental Botany 39, 1649–59.Google Scholar