Formation of aerenchyma and the processes of plant ventilation in relation to soil flooding and submergence

Plant Biology

Volumn 1, Issue 3, 1999, Pages 274-287

  Jackson, M B ^a   Armstrong, W ^b  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b UNIVERSITY OF HULL   (United Kingdom)

Author keywords

Aerenchyma; Anaerobiosis; Apoptosis; Environmental stress; Ethylene; Gas transport; Plant aeration; Pressure flow; Programmed cell death; Review; Roots; Water plants

Indexed keywords

ANIMALIA;

EID: 0033039942     PISSN: 14358603     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1438-8677.1999.tb00253.x     Document Type: Review

References (159)

1. Allen, L. H. (1997) Mechanisms and rates of oxygen transfer to and through submerged rhizomes and roots via aerenchyma. Soil and Crop Science Society of Florida Proceedings 56, 41-54.
2. Arber, A. (1920) Water Plants: a study of aquatic angiosperms. Cambridge: Cambridge University Press.
3. Arikado, H. and Adachi, Y. (1955) Anatomical and ecological responses of barley and some forage crops to the flooding treatment. Bulletin Faculty of Agriculture, Mie University Tsu Mie 11, 1-29.
4. Armstrong, J., Afreen-Zobayed, F., and Armstrong, W. (1996a) Phragmites die-back: sulphide-and acetic acid-induced bud and root death, lignifications, and blockages with the aeration and vascular systems. The New Phytologist 134, 601-614.
5. Armstrong, W. (1979) Aeration in higher plants. In Advances in Botanical Research, Vol. 7 (Woolhouse, H. W., ed.), London: Academic Press, pp. 225-332.
6. Armstrong, J., ed. (1996) Ventilation in macrophytes. Aquatic Botany 54 (2, 3; Special Issue), 85-264.
7. Armstrong, J. and Armstrong, W. (1994) Chlorophyll development in mature lysigenous and schizogenous root aerenchyma provides evidence of continuing cortical cell viability. The New Phytologist 126, 493-497.
8. Armstrong, J., Armstrong, W., and van der Putten, W. H. (1996b) Phragmites die-back: bud and root death, blockages within the aeration and vascular systems and the possible role of phytotoxins. The New Phytologist 133, 399-413.
9. Armstrong, J., Armstrong, W., and Beckett, P. M. (1992) Phragmites australis: Venturi-and humidity-induced convections enhance rhizome aeration and rhizosphere oxidation. The New Phytologist 120, 197-207.
10. Armstrong, J., Armstrong, W., Wu, Z., and Afreen-Zobayed, F. (1996c) A role for phytotoxins in the Phragmites die-back syndrome? Folia Geobotanica and Phytotaxonomica 31, 127-142.
11. Armstrong, J., Armstrong, W., Beckett, P. M., Halder, J. E., Lythe, S., Holt, R., and Sinclair, A. (1996d) Pathways of aeration and the mechanisms and beneficial effects of humidity-and Venturi-induced convections in Phragmites australis. Aquatic Botany 54, 177-198.
12. Armstrong, W. (1994) Polarographic oxygen electrodes and their use in plant aeration studies. Proceedings of the Royal Society of Edinburgh 102 B, 511-528.
13. Armstrong, W. and Beckett, P. M. (1987) Internal aeration and the development of stelar 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.The New Phytologist 105, 221-245.
14. Armstrong, W., Armstrong, J., and Beckett, P. M. (1990) Measurement and modelling of oxygen release from roots of Phragmites australis. In The use of constructed wetlands in water pollution control (Cooper, P. and Finklater, B. C., eds.), Oxford: Pergamon Press, pp. 41-54.
15. Armstrong, W., Armstrong, J., and Beckett, P. M. (1996e) Pressurized ventilation in emergent macrophytes: the mechanism and mathematical modelling of humidity-induced convection. Aquatic Botany 54, 121-136.
16. Armstrong, W., Brändle, R., and Jackson, M. B. (1994) Mechanisms of flood tolerance in plants. Acta Botanica Neerlandica 43, 1-52.
17. Armstrong, W., Armstrong, J., and Beckett, P. M. (1996f) Pressurized aeration in wetland macrophytes: some theoretical aspects of humidity-induced convection and thermal transpiration. Folia Geobotanica and Phytotaxonomica 31, 25-36.
18. Armstrong, W., Armstrong, J., Beckett, P. M., and Justin, S. H. F. W. (1991a) Convective gas-flows in wetland plant aeration. In Plant life under oxygen stress. Ecology, physiology and biochemistry (Jackson, M. B., Davies, D. D., and Lambers, H., eds.), SPB Academic, The Hague, pp. 283-302.
19. Armstrong, W., Beckett, P. M., Justin, S. H. F. W., and Lythe, S. (1991b) Modelling and other aspects of root aeration. In Plant Life under Oxygen Stress. Ecology, physiology and biochemistry (Jackson, M. B., Davies, D. D., and Lambers, H., eds.), SPB Academic, The Hague, pp. 267-282.
20. Armstrong, W., Strange, M. E., Cringle, S., and Beckett, P. M. (1994) Microelectrode and modelling study of oxygen distribution in roots. Annals of Botany 74, 287-299.
21. Ashford, A. E. and Allaway, W. G. (1995) There is a continuum of gas space in young plants of Avicennia marina. Hydrobiologia 295, 1-3.
22. Atwell, B. J., Drew, M. C., and 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 L. Physiologia Plantarum 72, 15-22.
23. Baluska, F., Brailsford, R. W., Hauskrecht, M., Jackson, M. B., and Barlow, P. W. (1993) Cellular dimorphism in the maize root cortex: involvement of microtubules, ethylene and gibberellin in the differentiation of cellular behaviour in postmitotic growth zones. Botanica Acta 106, 394-403.
24. Barlow, P. W. (1982) Cell death - an integral part of plant development. In Growth regulators in plant senescence. Monograph 8 (Jackson, M. B., Grout, B., and Mackenzie, I. A., eds.), Wantage: British Plant Growth Regulator Group, pp. 27-45.
25. Baruch, Z. and Merida, T. (1995) Effects of drought and flooding on root anatomy in four tropical forage grasses. International Journal of Plant Science 156, 514-521.
26. Beckett, P. M. and Armstrong, W. (1992) The modelling of convection and diffusion-driven aeration in plants. In Oxygen transport in biological systems. SEB Seminar Series (Eggington, S. and Ross, H. F., eds.), Cambridge: Cambridge University Press, pp. 253-293.
27. Beckett, P. M., Armstrong, W., Justin, S. H. F. W., and Armstrong, J. (1988) On the relative importance of convective and diffusive gas-flows in plant aeration. The New Phytologist 110, 463-468.
28. Bedford, B. L., Bouldin, D. R., and Beliveau, B. D. (1991) Net oxygen and carbon dioxide balances in solutions bathing the roots of wetland plants. Journal of Ecology 79, 943-959.
29. Bendix, M., Tornbjerg, T., and Brix, H. (1994) Internal gas transport in Typha latifolia, L. and Typha angustifolia, L. I. Humidity-induced pressurization and convective throughflow. Aquatic Botany 49, 75-90.
30. Berjak, P. and Lawton, J. R. (1973) Prostelar autolysis: a further example of a programmed senescence. The New Phytologist 72, 625-637.
31. Blom, C. W. P. M. (1999) Adaptations to flooding stress: from plant community to molecule. Plant Biology 1, 261-273.
32. Bowen, I. D., Bowen, S. M., and Jones, A. H. (1998) Mitosis and apoptosis. Matters of life and death. London: Chapman and Hall.
33. Brailsford, R. W. and Jackson, M. B. (1995) Aerenchyma formation in roots of maize: an example of apoptosis in plants that is hormonally regulated. Journal of Experimental Botany 46 (suppl.), 30.
34. Brailsford, R. W., Voesenek, L. A. C. J., Blom, C. W. P. M., Smith, A. R., Hall, M. A., and Jackson, M. B. (1993) Ethylene production by primary roots of Zea mays L. in response to subambient partial pressures of oxygen. Plant, Cell and Environment 16, 1071-1080.
35. Brix, H. (1990) Uptake and photosynthetic utilization of sediment-derived carbon by Phragmites australis (Cav) Trin Ex Steudel. Aquatic Botany 38, 377-389.
36. Brix, H., Sorrel, B. K., and Orr, P. T. (1992) Internal pressurisation and convective gas flow in some emergent freshwater macrophytes. Limnol. Oceanogr. 37, 1420-1433.
37. Butterbach-Bahl, K., Papen, H., and Rennenberg, H. (1998) Impact of gas transport through rice cultivars on methane emission from rice paddy fields. Plant, Cell and Environment 20, 1175-1183.
38. Callaway, R. M. and King, L. (1996) Temperature-driven variation in substrate oxygenation and the balance of competition and facilitation. Ecology 77, 1189-1195.
39. Campbell, R. and 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.
40. Chanton, J. P. and Whiting, G. J. (1996) Methane stable isotopic distributions as indicators of gas transport mechanisms in emergent aquatic plants. Aquatic Botany 54, 227-236.
41. Christensen, K. K. and Wigand, C. (1998) Formation of root plaques and their influence on tissue phosphorus content in Lobelia dortmanna. Aquatic Botany 61, 111-122.
42. Christensen, P. B., Revsbech, N. P., and Sand-Jensen, K. (1994) Microsensor analysis of oxygen in the rhizosphere of the aquatic macrophyte Littorella uniflora (L.) Aschers. Plant Physiology 105, 847-852.
43. Cleveland, R. E., Fujiwara, T., and Lucas, W. J. (1994) Plasmodesmatal-mediated cell-to-cell transport in wheat roots is modulated by anaerobic stress. Protoplasma 178, 81-85.
44. Colmer, T. D., Gibberd, M. R., Wiengweera, A., and Tinh, T. K. (1998) The barrier to radial oxygen loss from roots of rice (Oryza sativa L.) is induced by growth in stagnant solution. Journal of Experimental Botany 49, 1431-1436.
45. Comis, D. (1997) Aerenchyma. Lifelines for living underwater. Agricultural Research 45 (August 1997), 4-8.
46. Constable, J. V. H. and Longstreth, D. J. (1994) Aerenchyma carbon dioxide can be assimilated in Typha latifolia L. leaves. Plant Physiology 106, 1065-1072.
47. Coutts, M. P. and Phillipson, J. J. (1978) Tolerance of tree roots to waterlogging. II. Adaptation of Sitka Spruce and Lodgepole Pine to waterlogged soil. The New Phytologist 80, 71-77.
48. Dacey, J. W. A. (1980) Internal winds in water lilies: an adaptation for life in anaerobic sediments. Science 210, 1017-1019.
49. Dacey, J. W. A. (1981) Pressurized ventilation in the yellow water lily. Ecology 62, 1137-1147.
50. Dacey, J. W. H. and Klug, M. J. (1979) Methane efflux from lake sediments through water lilies. Science 203, 1253-1255.
51. Darwent, M. J. (1997) The development and use of microelectrodes for the study of oxygen transport and distribution in roots. UK: PhD thesis, University of Hull, 282 pages.
52. Deacon, J. W., Drew, M. C., and Darling, A. (1986) Progressive cortical senescence and formation of lysigenous gas space (aerenchyma) distinguished by nuclear staining in adventitious roots of Zea mays. Annals of Botany 58, 711-718.
53. DeLaune, R. D., Pezeshki, S. R., and Pardue, J. H. (1990) An oxidation-reduction buffer for evaluating the physiological responses of plants to oxygen stress. Environmental and Experimental Botany 30, 243-247.
54. Drennan, P. M. and Berjak, P. (1982) Degeneration of the salt-glands accompanying foliar maturation in Avicennia marina (Forsskal) Vierh. The New Phytologist 90, 165-176.
55. Drew, M. C. and Fourcy, A. (1986) Radial movement of cations across aerenchymatous roots of Zea mays measured by electron probe X-ray analysis. Journal of Experimental Botany 37, 823-831.
56. Drew, M. C., Jackson, M. B., and 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. Planta 147, 83-88.
57. Drew, M. C., Jackson, M. B., and Giffard, S. C. (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.
58. Drew, M. C., Saglio, P. H., and Pradet, A. (1985) Larger adenylate charge and ATP/ADP ratios in aerenchymatous roots of Zea mays in anaerobic media as a consequence of improved oxygen transport. Planta 165, 51-58.
59. Ecker, J. R. (1995) The ethylene signal transduction pathway in plants. Science 268, 667-675.
60. Frenzel, P., Rothfuss, F., and Conrad, R. (1992) Oxygen profiles and methane turnover in a flooded rice microcosm. Biology and Fertility of Soils 14, 84-89.
61. Fuhr, R. (1998) Ethylene perception: from two-component signal transducers to gene induction. Trends in Plant Science 3, 141-146.
62. Gavrieli, Y., Sherman, Y., and Ben-Sasson, S. A. (1992) Identification of programmed cell death in situ via specific labelling of nuclear DNA fragmentation. Journal of Cell Biology 119, 493-501.
63. Gaynard, T. J. and Armstrong, W. (1987) Some aspects of internal plant aeration in amphibious habitats. In Plant Life in Aquatic and Amphibious Habitats, British Ecological Society Special Symposium 5 (Crawford, R. M. M., ed.), Oxford: Blackwells, pp. 303-320.
64. Gibbs, J., Turner, D. W., Armstrong, W., Darwent, M. J., and Greenway, H. (1998) Response to oxygen deficiency in primary maize roots. I. Development of oxygen deficiency in the stele reduces radial solute transport to the xylem. Australian Journal of Plant Physiology 25, 745-758.
65. Grineva, G. M. and Bragina, T. V. (1993) Formation of adaptations to flooding in corn - structural and functional parameters. Russian Plant Physiology 40, 583-587.
66. Grosse, W. (1996) The mechanism of thermal transpiration (= thermo-osmosis). Aquatic Botany 54, 101-110.
67. Grosse, W. and Schroder, P. (1985) Aeration of the roots and chloroplast-free tissues of trees. Berichte der Deutschen Botanischen Gesellschaft 98, 311-318.
68. Grosse, W. and Bauch, C. (1991) Gas transfer in floating-leaved plants. Vegetatio 97, 185-192.
69. Grosse, W., Frye, J., and Lattermann, S. (1992) Root aeration in wetland trees by pressurized gas-transport. Tree Physiology 10, 285-295.
70. Happell, J. D., Chanton, J. P., Whiting, G. J., and Showers, W. J. (1993) Stable isotopes as tracers of methane dynamics in everglades marshes with and without active populations of methane oxidising bacteria. Journal of Geophysical Research 98, 14771-14782.
71. He, C. J., Morgan, P. W., and Drew, M. C. (1992) Enhanced sensitivity to ethylene in nitrogen-or phosphate-starved roots of Zea mays L. during aerenchyma formation. Plant Physiology 98, 137-142.
72. He, C. J., Drew, M. C., and Morgan, P. W. (1994) Induction of enzymes associated with lysigenous aerenchyma formation in roots of Zea mays during hypoxia or nitrogen starvation. Plant Physiology 105, 861-865.
73. He, C. J., Finlayson, S. A., Drew, M. C., Jordan, W. R., and Morgan, P. W. (1996a) Ethylene biosynthesis during aerenchyma formation in roots of maize subjected to mechanical impedance and hypoxia. Plant Physiology 112, 1679-1685.
74. He, C. J., Morgan, P. W., and Drew, M. C. (1996b) Transduction of an ethylene signal is required for cell death and lysis in the root cortex during aerenchyma formation induced by hypoxia. Plant Physiology 112, 463-472.
75. Howes, B. L. and Teal, J. M. (1994) Oxygen loss from Spartina alterniflora and its relationship to salt marsh oxygen balance. Oecologia 97, 431-438.
76. Huang, B. R., Johnson, J. W., Box, J. E., and NeSmith, D. S. (1997) Root characteristics and hormone activity of wheat in response to hypoxia and ethylene. Crop Science 37, 812-818.
77. Huang, B. R., Johnson, J. W., NeSmith, D. S., and Bridges, D. C. (1994) Growth, physiological and anatomical responses of two wheat genotypes to waterlogging and nutrient supply. Journal of Experimental Botany 45, 193-202.
78. Jackson, M. B. (1989) Regulation of aerenchyma formation in roots and shoots by oxygen and ethylene. In Cell separation in plants. Physiology, biochemistry and molecular biology (Osborne, D. J. and Jackson, M. B., ed.), Berlin: Springer-Verlag, pp. 263-274.
79. Jackson, M. B. (1994) Root-to-shoot communication in flooded plants: Involvement of abscisic acid, ethylene, and 1-aminocyclopropane-1-carboxylic acid. Agronomy Journal 86, 775-782.
80. Jackson, M. B. and Hall, K. C. (1993) Polyamine content and action in roots of Zea mays L. in relation to aerenchyma development. Annals of Botany 72, 569-575.
81. Jackson, M. B., Fenning, T. M., Drew, M. C., and Saker, L. R. (1985) 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.
82. Jacobson, M. D., Weil, M., and Raff, M. C. (1997) Programmed cell death in animal development. Cell 88, 347-354.
83. James, E. K., Minchin, F. R., Oxborough, K., Cookson, A., Baker, N. R., Witty, J. F., Crawford, R. M. M., and Sprent, J. (1998) Photosynthetic oxygen evolution within Sesbania rostrata stem nodules. Plant Journal 13, 29-38.
84. Jespersen, D. N., Sorrell, B. K., and Brix, H. (1998) Growth and root oxygen release by Typha latifolia and its effect on sediment methanogenesis. Aquatic Botany 61, 165-180.
85. Justin, S. H. F. W. and Armstrong W. (1987) The anatomical characteristics of roots and plant response to soil flooding. The New Phytologist 105, 465-495.
86. Justin, S. H. F. W. and Armstrong W. (1991) Evidence for the involvement of ethene in aerenchyma formation in adventitious roots of rice (Oryza sativa L.). The New Phytologist 118, 49-62.
87. Kawai, M., Samarajeewa, P. K., Barrero, R. A., Nishiguchi, M., and Uchimiya, H. (1998) Cellular dissection of the degradation pattern of cortical cell death during aerenchyma formation of rice roots. Planta 204, 277-287.
88. Kawase, M. (1979) Role of cellulase in aerenchyma development in sunflower. American Journal of Botany 66, 183-190.
89. Kawase, M. and Whitmoyer, R. E. (1980) Aerenchyma development in waterlogged plants. American Journal of Botany 67, 18-22.
90. Kindinger, B., Bai, D., and Sokolov, V. (1996) Assignment of a gene(s) conferring apomixis in Tripsacum to a chromosome arm: cytological and molecular evidence. Genome 39, 1133-1141.
91. Kludze, H. K. and DeLaune, R. D. (1994) Methane emissions and growth of Spartina patens in response to soil redox intensity. Soil Science Society of America Journal 58, 1838-1845.
92. Kludze, H. K. and DeLaune, R. D. (1995) Gaseous exchange and wetland plant response to soil redox intensity and capacity. Soil Science Society of America Journal 59, 939-945.
93. Kludze, H. K., Pezeshki, S. R., and DeLaune, R. D. (1994) Evaluation of root oxygenation and growth in baldcypress in response to short-term soil hypoxia. Canadian Journal of Forest Research 24, 804-809.
94. Kludze, H. K., DeLaune, R. D., and Patrick, W. H. (1993) Aerenchyma formation and methane and oxygen exchange in rice. Soil Science Society of America Journal 57, 386-391.
95. Konings, H. and Jackson, M. B. (1978) A relationship between rates of ethylene production by roots and the promoting and inhibiting effects of exogenous ethylene and water on root elongation. Zeitschrift für Pflanzenphysiologie 92, 385-397.
96. Konings, H. and Verschuren, G. (1980) Formation of aerenchyma in roots of Zea mays in aerated solutions, and its relation to nutrient supply. Physiologia Plantarum 49, 265-270.
97. Laan, P., Berrovoets, M. J., Lythe, S., Armstrong, W., and Blom, C. W. P. M. (1989) Root morphology and aerenchyma formation as indicators for the flood-tolerance of Rumex crispus. Journal of Ecology 77, 693-703.
98. Laan, P., Tosserams, M., Blom, C. W. P. M., and Veen, B. W. (1990) Internal oxygen transport in Rumex species and its significance for respiration under hypoxic conditions. Plant and Soil 122, 39-46.
99. Lindau, C. W., Bollich, P. K., and DeLaune, R. D. (1995) Effect of rice variety on methane emission from Louisiana rice. Agricultural Ecosystems and Environment 54, 109-114.
100. Loureiro, M. F., Defaria, S. M., James, E. K., Pott, A., and Franco, A. A. (1994) Nitrogen-fixing stem nodules of the legume Discolobium pulchellum Benth. The New Phytologist 128, 283-295.
101. McManus, M. T. and Osborne, D. J. (1989) Identification of leaf abscission zones as a specific class of target cells for ethylene. In Cell separation in plants. Physiology, biochemistry and molecular biology (Osborne, D. J. and Jackson, M. B., eds.), Berlin: Springer-Verlag, pp. 201-210.
102. McQueen-Mason, M. T. and Rochange, F. (1999) Expansins in plant growth and development: an update on an emerging topic. Plant Biology 1, 19-25.
103. McQueen-Mason, S. J., Durachko, D. M., and Cosgrove, D. J. (1992) Two endogenous proteins that induce cell wall extension in plants. Plant Cell 4, 1425-1433.
104. Moon, M., Rattray, M. R., Putz, F. E., and Bowes, G. (1993) Acclimatization to flooding of the herbaceous vine Mikania scandens. Functional Ecology 7, 610-615.
105. Olson, D. C., Oetiker, J. H., and Yang, S. F. (1995) Analysis of LE-AC53, a 1-aminocyclopropane-1-carboxylic acid synthase gene expressed during flooding in the roots of tomato plants. The Journal of Biological Chemistry 270, 14056-14061.
106. Panteris, E., Apostolakos, P., and Galatis, B. (1993) Microtubule organization, mesophyll cell morphogenesis, and intercellular space formation in Adiantum capillus Veneris leaves. Protoplasma 172, 97-110.
107. Pedersen, O. and Sand-Jensen, K. (1992) Adaptations of submerged Lobelia to aerial life form: morphology, carbon sources and oxygen dynamics. Oikos 65, 89-96.
108. 2 in sandy lake sediments inhabited by Lobelia dortmana. Ecology 76, 1536-1545.
109. Pennell, R. I. and Lamb, C. (1997) Programmed cell death in plants. The Plant Cell 9, 1157-1168.
110. Pezeshki, S. R., Pardue, J. H., and DeLaune, R. D. (1993) The influence of soil oxygen deficiency on alcohol dehydrogenase activity, root porosity, ethylene production and photosynthesis in Spartina patens. Environmental and Experimental Botany 33, 565-573.
111. Raskin, I. and Kende, H. (1983) How does deep-water rice solve its aeration problem? Plant Physiology 72, 447-454.
112. Raven, J. (1996) Into the voids: the distribution, function, development and maintenance of gas spaces in plants. Annals of Botany 78, 137-142.
113. Rose, J. K. C., Lee, H. H., and Bennett, A. B. (1997) Expression of a divergent expansin gene is fruit-specific and ripening-regulated. Proceedings of the National Academy of Science USA 92, 5955-5960.
114. Saab, I. N. and Sachs, M. M. (1996) A flooding-induced xyloglucan endo-transglycosylase homolog in maize is responsive to ethylene and associated with aerenchyma. Plant Physiology 112, 385-391.
115. Satoh, S. (1998) Functions of the cell wall in the interactions of plant cells: analysis using carrot cultured cells. Plant and Cell Physiology 39, 361-368.
116. Scheres, B., McKhann, H., van den Berg, C., Willemsen, V., Wolkenfelt, H., de Vrieze, G., and Weisbeek, P. (1996) Experimental and genetic analysis of root development in Arabidopsis thaliana. Plant and Soil 187, 97-105.
117. Schlüter, U., Furch, B., and Joly, C. A. (1993) Physiological and anatomical adaptations by young Astocaryum juari Mart. (Arecaceae) in periodically inundated biotypes of Central Amazonia. Biotropica 25, 384-439.
118. Schuette, J. L., Klug, M. J., and Klomparens, K. L. (1994) Influence of stem lacunar structure on gas transport: relation to the oxygen transport potential of submersed vascular plants. Plant, Cell and Environment 17, 355-365.
119. Schussler, E. E. and Longstreth, D. J. (1996) Aerenchyma develops by cell-lysis in roots and cell-separation in leaf petioles in Sagittaria lancifolia (Alismataceae). American Journal of Botany 83, 1266-1273.
120. Schussler, E. E., Borkhsenious, O. N., and Longstreth, D. J. (1997) Formation of root aerenchyma involves programmed cell death in Saggittaria lancifolia. Plant Physiology 114 (supplement), 456.
121. Sculthorpe, C. C. (1967) The biology of aquatic vascular plants. London: Edward Arnold.
122. 2+ response to anoxia in Arabidopsis thaliana seedlings. Plant Physiology 111, 243-257.
123. Shannon, R. D., White, J. R., Lawson, J. E., and Gilmour, B. S. (1996) Methane efflux from emergent vegetation in peatlands. Journal of Ecology 84, 239-246.
124. Shimamura, S., Mochizuki, T., and Inouye, J. (1997) Formation of the lysigenous intercellular space in adventitious roots of leguminous species. Japanese Journal of Crop Science 66, 208-213.
125. 2 to the photosynthesis of emergent and submerged culms of Scirpus lacustris and Cyperus papyrus. Aquatic Botany 49, 107-116.
126. Smirnoff, N. and Crawford, R. M. M. (1983) Variation in the structure and response to flooding of root aerenchyma in some wetland plants. Annals of Botany 51, 237-249.
127. Skelton, N. J. and Alloway, W. G. (1996) Oxygen and pressure changes measured in situ during flooding in roots of the grey mangrove Avicennia marina (Forskk) Vier. Aquatic Botany 54, 165-175.
128. Sorrell, B. K. and Armstrong, W. (1994) On the difficulties of measuring oxygen release by root systems of wetland plants. Journal of Ecology 82, 177-183.
129. Sorrell, B. K. and Boon, P. I. (1994) Convective gas flow in Eleocharis sphacelata R. Br.: methane transport and release from wetlands. Aquatic Botany 47, 197-212.
130. Sorrell, B. K. and Drumgoole, F. I. (1988) Oxygen transport in the submerged freshwater macrophyte Egeria densa Planch. II. Role of lacunar gas pressures. Aquatic Botany 31, 93-106.
131. Sorrell, B. K., Brix, H., and Orr, P. T. (1993) Oxygen exchange by entire root systems of Cyperus involucratus and Eliochatis sphacelata. Journal of Aquatic Plant Management 31, 24-28.
132. Sorrell, B. K., Brix, H., and Orr, P. T. (1997) Eliochatis sphacelata: internal gas transport pathways and modelling of aeration by pressurized flow and diffusion. The New Phytologist 136, 433-442.
133. Steinburg, S. L. (1996) Mass and energy exchange between the atmosphere and leaf influence gas pressurization in aquatic plants. The New Phytologist 134, 587-600.
134. Stoecker, M. A., Smith, M., and Melton, E. D. (1995) Survival and aerenchyma development under flooded conditions of Boltonia decurrens, a threatened flood-plain species and Conyza canadensis, a widely distributed competitor. American Midlands Naturalist 134, 117-126.
135. Subbaiah, C. C., Zhang, J., and Sachs, M. M. (1994) Involvement of intracellular calcium in anaerobic gene expression and survival of maize seedlings. Plant Physiology 105, 369-376.
136. Thomas, K. L., Benstead, J., Davies, K. L., and Lloyd, D. (1996) The role of wetland plants in the diurnal control of methane and carbon dioxide fluxes in peat. Soil Biology and Biochemistry 28, 17-24.
137. 2. Plant Physiology 96, 1294-1301.
138. Trought, M. C. T. and Drew, M. C. (1980) The development of waterlogging damage in young wheat plants in anaerobic solution cultures. Journal of Experimental Botany 31, 1573-1580.
139. Uchimiya, H., Kidou, S., Shimazaki, T., Aotsuka, S., Takamatsu, S., Nishi, R., Hashimoto, H., Matsubayashi, Y., Kidou, N., Umeda, M., and Kato, A. (1992) Random sequencing of cDNA libraries reveals a variety of expressed genes in cultures cells of rice (Oryza sativa L.). Plant Journal 2, 1005-1009.
140. Ueckert, J., Hurek, T., Fendrik, I., and Neimann, E.-G. (1990) Radial gas diffusion from roots of rice (Oryza sativa L.) and Kallar grass (Leptochloa fusca L. Kunth), and effects of inoculation with Azospirillum brasilense Cd. Plant and Soil 122, 59-65.
141. Della Vecchia, F., Cuccato, F., La Rocca, N., Larcher, W., and Rascio, N. (1999) Endodermis-like sheaths in the submerged freshwater macrophyte Ranunculus trichophyllus Chaix. Annals of Botany 83, 93-97.
142. Vriezen, W. H., Van Rijn, C. P. E., Voesenek, L. A. C. J., and Mariani, C. (1997) A homologue of the Arabidopsis ERS gene is actively regulated in Rumex palustris upon flooding. Plant Journal 11, 1265-1271.
143. Van Noordwijk, M. and Brouwer, G. (1993) Gas-filled root porosity in response to temporary low-oxygen supply in different growth stages. Plant and Soil 152, 187-199.
144. van der Weele, C. M., Canny, M. J., and McCully, M. E. (1996) Water in aerenchyma spaces in roots. A fast diffusion path for solutes. Plant and Soil 184, 131-141.
145. Visser, E. J. W., Nabben, R. H. M., Blom, C. W. P. M., and Voesenek, L. A. C. J. (1997) Elongation by primary lateral root and adventitious roots during conditions of hypoxia and high ethylene concentrations. Plant, Cell and Environment 20, 647-653.
146. Walbot, V. (1992) Strategies for mutagenesis and gene cloning using transposon tagging and T-DNA insertional mutagenesis. Annual Review of Plant Physiology and Plant Molecular Biology 43, 49-82.
147. Waters, I., Armstrong, W., Thomson, C. J., Setter, T. L., Adkins, S., Gibbs, J., and Greenway, H. (1989) Diurnal changes in radial oxygen loss and ethanol metabolism in roots of submerged and non-submerged rice seedlings. The New Phytologist 113, 439-451.
148. Watkin, E. L. J., Thomson, C. J., and Greenway, H. (1998) Root development and aerenchyma formation in two wheat cultivars and one triticale cultivar grown in stagnant agar and aerated nutrient solution. Annals of Botany 81, 349-354.
149. Webb, J. and Jackson, M. B. (1986) Transmission and cryo-scanning electron microscopy study of the formation of aerenchyma (cortical gas-filled space) in adventitious roots of rice (Oryza sativa). Journal of Experimental Botany 37, 832-841.
150. Whiting, G. J. and Chanton, J. P. (1996) Control of the diurnal pattern of methane emission from emergent aquatic macrophytes by gas transport mechanisms. Aquatic Botany 54, 237-254.
151. Wiengweera, A., Greenway, H., and Thomson, C. J. (1997) The use of agar nutrient solution to simulate lack of convect on in waterlogged soils. Annals of Botany 80, 115-123.
152. Wooley, J. T. (1983) Maintenance of air in intercellular spaces of plants. Plant Physiology 72, 989-991.
153. Yaklich, R. W., Vigil, E. L., and Wergin, W. P. (1995) Morphological and fine-structural characteristics of aerenchyma cells in the soyabean seed coat. Seed Science and Technology 23, 321-330.
154. Yamamoto, F., Sakato, T., and Terazawa, K. (1995a) Physiological, morphological and anatomical responses of Fraxinus mandshurica seedlings to flooding. Tree Physiology 15, 713-719.
155. Yamamoto, F., Sakato, T., and Terazawa, K. (1995b) Growth, morphology, stem anatomy and ethylene production in flooded Alnus japonica seedlings. Iawa Journal 16, 47-59.
156. Yavitt, J. B. and Knapp, A. K. (1998) Aspects of methane flow from sediment through emergent cattail (Typha latifolia) plants. The New Phytologist 139, 495-503.
157. Young, T. E., Gallie, D. R., and DeMason, D. A. (1997) Ethylene-mediated programmed cell death during maize endosperm development of wild-type and shrunken genotypes. Plant Physiology 115, 737-751.
158. Zarembinski, T. I. and Theologis, A. (1993) Anaerobiosis and plant growth hormones induce two genes encoding 1-aminocyclopropane-1-carboxylate synthase in rice (Oryza sativa L.). Molecular Biology of the Cell 4, 363-373.
159. Schiwinski, K., Grosse, W., and Woerman, D. (1996) Convective gas flow in plant aeration and Graham's law of diffusion. Zeitschrift für Naturforschung 51 c, 681-690.