Conditions leading to high CO2 (>5 kPa) in waterlogged-flooded soils and possible effects on root growth and metabolism

Annals of Botany

Volumn 98, Issue 1, 2006, Pages 9-32

  Greenway, Hank ^a   Armstrong, William ^b   Colmer, Timothy D ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b UNIVERSITY OF HULL   (United Kingdom)

Author keywords

Acid load; Aerenchyma; Bicarbonate; Carbon dioxide; Cytochrome c; Metabolism; O2 deficiency; pH regulation; Respiration; Waterlogging; Wetland plants

Indexed keywords

BICARBONATE; CARBON DIOXIDE; CYTOCHROME C OXIDASE; OXYGEN; WATER;

ADAPTATION; CARBON DIOXIDE; CYTOPLASM; DIFFUSION; FLOODED SOIL; FLOODING; GAS EXCHANGE; GROWTH RATE; PADDY FIELD; RHIZOME; SOIL; SOIL-VEGETATION INTERACTION;

ACCLIMATIZATION; BIOLOGICAL MODEL; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; MAIZE; METABOLISM; PH; PHYSIOLOGY; PLANT ROOT; REVIEW; RICE; SOIL;

ACCLIMATIZATION; BICARBONATES; CARBON DIOXIDE; ELECTRON TRANSPORT COMPLEX IV; HYDROGEN-ION CONCENTRATION; MODELS, BIOLOGICAL; ORYZA SATIVA; OXYGEN; PLANT ROOTS; SOIL; WATER; ZEA MAYS;

ZEA MAYS;

EID: 33646696485     PISSN: 03057364     EISSN: 10958290     Source Type: Journal    
DOI: 10.1093/aob/mcl076     Document Type: Review

References (128)

1. Ahuja LR, Rawls WJ, Nielsen DR, Williams RD. 1999. Determining soil hydraulic properties and their field variability from simpler measurements. In: Skaggs RW, van Schilfgaarde J, eds. Agricultural drainage. Madison: American Society of Agronomy, 1207-1233.
2. Alberts B, Johnson A, Lewis J, Raff M, Roberts K. 2002. Molecular biology of the cell, 4th edn. New York: Garland Science Publishers.
3. Amthor JS. 1997. Plant respiratory responses to elevated carbon dioxide partial pressure. In: Allen LH, Kirkham MB, Olszyk DM, Whitman CE, eds. Advances in carbon dioxide effects research. Madison: American Society of Agronomy, 35-77.
4. Andrews DL, Drew MC, Johnson JR, Cobb BG. 1994. The response of maize seedlings of different ages to hypoxic and anoxic stress. Changes in induction of ADH1 mRNA, ADH activity, and survival of anoxia. Plant Physiology 105: 53-60.
5. Armstrong W. 1979. Aeration in higher plants. Advances in Botanical Research 7: 225-332.
6. Armstrong W. 1982. Waterlogged soils. In: Etherighton JR, ed. Environment and plant ecology. Chichester: John Wiley, 290-330.
7. Armstrong W, Beckett PM. 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. New Phytologist 105: 221-245.
8. Armstrong W, Drew MC. 2002. Root growth and metabolism under oxygen deficiency. In: Waisel Y, Eshel A, Kafkafi U, eds. Plant roots: the hidden half, 3rd edn. New York: Marcel Dekker, 729-761.
9. Armstrong W, Cousins D, Armstrong J, Turner DW, Beckett PM. 2000. Oxygen distribution in wetland plant roots and permeability barriers to gas-exchange with the rhizosphere: a microelectrode and modelling study with Phragmites australis. Annals of Botany 86: 687-703.
10. Beckett PM, Armstrong W, Justin SHFW, Armstrong J. 1988. On the relative importance of convective and diffusive gas-flows in plant aeration. New Phytologist 110: 463-468.
11. Beevers H. 1953. 2-4-dinitrophenol and plant respiration. American Journal of Botany 40: 91-95.
12. Bendall DS, Ranson SL, Walker DA. 1960. Effects of carbon dioxide on the oxidation of succinate and reduced diphosphopyridine nucleotide by Ricinus mitochondria. Biochemical Journal 76: 221-225.
13. Begg CBM, Kirk GJD, Mackenzie AF, Neue HU. 1994. Root-induced iron oxidation and pH changes in the lowland rice rhizosphere. New Phytologist 128: 469-477.
14. Blackwell PS, Ward MA, Lefevre RN, Cowan DJ. 1985. Compaction of a swelling clay soil by agricultural traffic; effects upon conditions for growth of winter cereals and evidence for some recovery of structure. Journal of Soil Science 36: 633-650.
15. Boru G, VanToai T, Alves J, Hua D, Knee M. 2003. Responses of soybean to oxygen deficiency and elevated root-zone carbon dioxide concentration. Annals of Botany 91: 447-453.
16. 2 concentration does not affect growth or root respiration in bean or citrus. Plant, Cell and Environment 20: 1495-1505.
17. 2 and intracellular pH. Plant, Cell and Environment 8: 459-465.
18. Brady CJ, Romani RJ. 1988. Respiration and protein synthesis in non-growing cultured pear fruit cells in response to ethylene and modified atmospheres. Plant Physiology 87: 571-576.
19. Brix H. 1988. Light-dependent variations in the composition of the internal atmosphere of Phragmites australis (cav.) Trin. Ex Steudel. Aquatic Botany 30: 319-329.
20. Busa WB, Crowe JH. 1983. Intracellular pH regulates transitions between dormancy and development of brine shrimp (Artemia salina) embryos. Science 221: 366-368.
21. Cerwick SF, Martin BA, Reding LD. 1995. The effect of carbon dioxide on maize seed recovery after flooding. Crop Science 35: 1116-1121.
22. 13C in Phragmites australis. Biogeochemistry 59: 287-301.
23. Cho DY, Ponnamperuma FN. 1971. Influence of soil temperature on the chemical kinetics of flooded soils and the growth of rice. Soil Science 112: 184-194.
24. Colmer TD. 2003a. Long-distance transport of gases in plants: a perspective on internal aeration and radial oxygen loss from roots. Plant, Cell and Environment 26: 17-36.
25. Colmer TD. 2003b. Aerenchyma and an inducible barrier to radial oxygen loss facilitate root aeration in upland, paddy and deep-water rice (Oryza sativa L.). Annals of Botany 91: 301-309.
26. - net fluxes along roots of rice and maize. Plant, Cell and Environment 21: 240-246.
27. Colmer TD, Greenway H. 2005. Oxygen transport, respiration and anaerobic catabolism in roots in flooded soils. In: Lambers H, Ribas-Carbo M, eds. Plant respiration: from cell to ecosystem. Dordrecht: Springer, 137-158.
28. Cramer MD. 2002. Inorganic carbon utilization by root systems. In: Waisel Y, Eshel A, Kafkafi U, eds. Plant roots: the hidden half, 3rd edn. New York: Marcel Dekker, 699-715.
29. Currie JA. 1965. Diffusion within the soil microstructure: a structural parameter for soils. Journal of Soil Science 16: 279-289.
30. Dacey JWH. 1981. Pressurised ventilation in the yellow waterlily. Ecology 62: 1137-1147.
31. 2 transport. Phvsiologia Plantarum 56: 361-366.
32. Dacey JWH, Klug MJ. 1982b. Ventilation by floating leaves in Nuphar. American Journal of Botany 69: 999-1003.
33. Darwent MJ, Armstrong W, Armstrong J, Beckett PM. 2003. Exploring the radial and longitudinal aeration of primary maize roots by means of Clark-type oxygen microelectrodes. Russian Journal of Plant Physiology 50: 722-732.
34. Davies DD. 1980. Anaerobic metabolism and the production of organic acids. In: Davies DD, ed. The biochemistry of plants, vol. 2. London: Academic Press, 581-611.
35. Davies DD. 1986. The fine control of cytoplasmic pH. Physiologia Plantarum 67: 702-706.
36. De Datta SK. 1981. Principles and practices of rice production. New York: Wiley & Sons.
37. 2? Annual Review of Plant Physiology and Molecular Biology 48: 609-639.
38. 2 concentration inhibit mitochondrial respiration in green plants? Plant, Cell and Environment 22, 649-657.
39. Drew MC. 1997. Oxygen deficiency and root metabolism: injury and acclimation under hypoxia and anoxia. Annual Review of Plant Physiology and Plant Molecular Biology 48: 223-250.
40. Felle HH. 1996. Control of cytoplasmic pH under anoxic conditions and its implication for plasma membrane proton transport in Medicago sativa root hairs. Journal of Experimental Botany 47: 967-973.
41. Felle HH. 2005. pH regulation in anoxic plants. Annals of Botany 96: 519-532.
42. Flowers TJ, Dalmond D. 1993. Protein synthesis in halophytes: the influence of potassium, sodium and magnesium in vitro. In: Randall PJ, Delhaize E, Richards RA, Munns R, eds. Genetic aspects of plant mineral nutrition. Dordrecht: Kluwer, 195-203.
43. Gerendas J, Schurr U. 1999. Physicochemical aspects of ion relations and pH regulation in plants - a quantitative approach. Journal of Experimental Botany 50: 1101-1114.
44. Gibbs J, Greenway H. 2003. Mechanisms of anoxia tolerance in plants. I. Growth, survival and anaerobic catabolism. Functional Plant Biology 30: 1-47.
45. 2 deficiency in primary roots of maize. I. Development of oxygen deficiency in the stele reduces radial solute transport to the xylem. Australian Journal of Plant Phvsiology 25: 745-758.
46. Good BJ, Patrick WH. 1987. Gas composition and respiration of water oak (Quercus nigra L.) and green ash (Fraxinus pennsylvanica Marsh.) roots after prolonged flooding. Plant and Soil 97: 419-427.
47. 2 on growth of corn and soybean seedlings. Proceedings of the Soil Science Society of America 29: 233-238.
48. Greenland DJ. 1981. Recent progress in studies of soil structure, and its relation to properties and management of paddy soils. In: Proceedings of symposium on paddy soil. Berlin: Springer-Verlag, 42-58.
49. Greenway H, Gibbs J. 2003. Mechanisms of anoxia tolerance in plants. II. Energy requirements for maintenance and energy distribution to essential processes. Functional Plant Biology 30: 999-1036.
50. Greenwood DJ. 1973. Distribution of carbon dioxide in the aqueous phase of aerobic soils. Journal of Soil Science 21: 314-329.
51. Guern J, Felle HH, Mathieu Y, Kurkdjian A. 1991. Regulation of intracellular pH in plant cells. International Review of Cytology 127: 111-173.
52. Hafke JB, Neff R, Huett MT, Luettge U, Thiel G. 2001. Day-to-night variations of cytoplasmic pH in a crassulacean acid metabolism plant. Protoplasma 216: 164-170.
53. Hanstein S, de Beer D, Felle HH. 2001. Minuaturised carbon dioxide sensor designed for measurements within plant leaves. Sensors and Actuators B 81: 107-114.
54. Harned HS, Bonner FT. 1945. The first ionization of carbonic acid in aqueous solutions of sodium chloride. Journal of the American Biochemical Society 67: 1926-1937.
55. Heber U, Wagner U, Kaiser W, Neimanis S, Bailey K, Walker D. 1994. Fast cytoplasmic regulation in acid-stressed leaves. Plant and Cell Physiology 35: 479-488.
56. 2 effects on plant organs. In: Weichman J, ed. Postharvest physiology of vegetables. New York: Marcel Dekker, 239-253.
57. Hofmann GE, Hand SC. 1990. Arrest of cytochrome-c oxidase synthesis coordinated with catabolic arrest in dormant Artemia embryos. American Journal of Physiology 258 (Regulatory Integrative Comparative Physiology 27): R1184-R1191.
58. Holzapfel-Pschorn A, Conrad R, Seiler W. 1986. Effect of vegetation on the emission of methane from submerged paddy soil. Plant and Soil 92: 223-233.
59. 2 enrichment and hypoxia of wheat genotypes differing in waterlogging tolerance. Crop Science 37: 464-468.
60. IRRI 2005. International Rice Research Institute Annual Report for 2004. Los Banos, Philippines: IRRI.
61. Jackson MB, Armstrong W. 1999. Formation of aerenchyma and the processes of plant ventilation in relation to soil flooding and submergence. Plant Biology 1: 274-287.
62. Jackson MB, Drew MC. 1984. Effects of flooding on growth and metabolism of herbaceous plants. In: Kozlowski TT, ed. Flooding and plant growth. London: Academic Press, 47-128.
63. Jackson MB, Ricard B. 2003. Physiology, biochemistry, and molecular biology of plant root systems subjected to flooding of the soil. In: Visser EJW, de Kroon H, eds. Root ecology. Heidelberg: Springer-Verlag, 193-213.
64. Jackson MB, Fenning TM, Jenkins W. 1985. Aerenchyma (gas-space) formation in adventitious roots of rice (Oryza sativa L.) is not controlled by ethylene or small pressures of oxygen. Journal of Experimental Botany 36: 1566-1572.
65. 2-fumigated and nitrogen-fertilised ponderosa pine. Plant and Soil 165: 129-138.
66. Justin SHFW, Armstrong W. 1987. The anatomical characteristics of roots and plant response to soil flooding. New Phytologist 106: 465-495.
67. 2 concentrations. Journal of the American Society of Horticultural Science 115: 111-114.
68. Kirk GJD. 2003. Rice root properties for internal aeration and efficient nutrient acquisition in submerged soil. New Phytologist 159: 185-194.
69. Kirk GJD. 2004. The biogeochemistry of submerged soils. Chichester: John Wiley and Sons.
70. Kirk GJD, Solivas JL, Alberto MC. 2003. Effects of flooding and redox conditions on solute diffusion in soils. European Journal of Soil Science 54: 617-624.
71. Kurkdjian A, Leguay JJ, Guern J. 1978. Measurement of intracellular pH and aspects of its control in higher plant cells cultivated in liquid media. Respiration Physiology 33: 75-89.
72. Kurkdjian A, Guern J. 1989. Intracellular pH: measurement and importance in cell activity. Annual Review of Plant Physiology and Plant Molecular Biology 40: 271-303.
73. 2, and temperature effect on respiration between 'Conference' pear protoplasts in suspension and intact pears. Journal of Experimental Botany 52: 1769-1777.
74. Leigh RA. 2001. Potassium homeostasis and membrane transport. Journal of Plant Nutrition and Soil Science 164: 193-198.
75. Lorimer GH. 1983. Carbon dioxide and carbamate formation: the makings of a biochemical control system. Trends in Biochemical Science 8: 65-68.
76. Ludlow MM. 1976. Ecophysiology of C4 grasses. In: Lange OL, Kappen L, Schulze ED, eds. Water and plant life. Problems and modern approaches. New York: Springer, 364-386.
77. 2-concentrating consequences in crassulacean acid metabolism, Journal of Experimental Botany 53: 2131-2142.
78. 2 by pods of chick pea (Cicer arietinum L.) subjected to water deficits. Journal of Experimental Botany 52: 123-131.
79. 2-enriched atmospheres. Postharvest Biology and Technology 3: 225-233.
80. Mathooka FM. 1996. Regulation of respiratory metabolism in fruits and vegetables by carbon dioxide. Postharvest Biology and Technology 9: 247-264.
81. McGuire MA, Teskey RO. 2002. Microelectrode technique for in situ measurement of carbon dioxide concentrations in xylem sap of trees. Tree Physiology 22: 807-811.
82. 2. Tree Physiology 24: 571-578.
83. Miller GW, Evans HL. 1956. Inhibitions of cytochrome oxidase by bicarbonate. Nature 178: 974-976.
84. 2 biodynamics: a new concept of cellular control. Journal of Theoretical Biology 80: 537-551.
85. Neuburger M, Douce R. 1980. Effect of bicarbonate and oxaloacetate on malate oxidation by spinach leaf mitochondria. Biochimica et Biophysica Acta 589: 176-189.
86. Nobel PS. 1974. Biophysical plant physiology. San Francisco: WH Freeman and Company.
87. 2 effects on root respiration of cacti. Plant and Soil 120: 263-271.
88. Padovan AC, Dry IB, Wiskisch JT. 1989. An analysis of the control of phosphorylation-coupled respiration in isolated plant mitochondria. Plant Physiology 90: 928-933.
89. Painuli DK, Woodhead T, Pagliai M. 1988. Effective use of energy and water in rice-soil puddling. Soil and Tillage Research 12: 149-161.
90. Palet A, Ribas-Carbo M, Argiles JM, Azcon-Bieto J. 1991. Short-term effects of carbon dioxide on carnation callus cell respiration. Plant Physiology 96: 467-472.
91. 2 on root respiration for Agave deserti. Physiologia Plantarum 76: 187-192.
92. Payne D, Gregory PJ. 1988. The soil atmosphere. In: Wild A, ed. Soil conditions and plant growth, 11th edn. New York: Longman Scientific Technical, 301-314.
93. Penman HL. 1940. Gas and vapour movement in the soil. I. The diffusion of vapours through porous solids. Journal of Agricultural Science 30: 437-462.
94. Ponnamperuma FN. 1984. Effects of flooding on soils. In: Kozlowski TT, ed. Flooding and plant growth. New York: Academic Press, 9-45.
95. Prince HBA, de Guia MB. 1986. Carbon source of the water soldier, Stratiotes aloides L. Aquatic Botany 26: 225-234.
96. Qi J, Marshall JD, Mattson KG. 1994. High soil carbon dioxide concentrations inhibit root respiration of Douglas fir. New Phytologist 128: 435-442.
97. Ranathunge K, Kotula L, Steudle E, Lafitte R. 2004. Water permeability and reflection coefficient of the outer part of young rice roots are differently affected by closure of water channels (aquaporins) or blockage of apoplastic pores. Journal of Experimental Botany 35: 433-447.
98. 2 on growth and nutrition of rice seedlings. Plant and Soil 47: 313-322.
99. Ratcliffe RG. 1997. In vivo NMR studies of the metabolic response of plant tissues to anoxia. Annals of Botany 79A: 39-48.
100. Raven JA, Newman JR. 1994. Requirement for carbonic anhydrase activity in processes other than photosynthetic inorganic carbon accumulation. Plant, Cell and Environment 17: 125-130.
101. Ribas-Carbo M, Robinson SA, Giles L. 2005. The application of the oxygen-isotope technique to assess respiratory pathway partitioning. In: Lambers H, Ribas-Carbo M, eds. Plant respiration: from cell to ecosystem. Dordrecht: Springer, 31-42.
102. Rottenberg H. 1975. The measurement of transmembrane electrochemical proton gradients. Journal of Bioenergetics 7: 61-74.
103. Rowell DL. 1988. Flooded and poorly drained soils. In: Wild A, ed. Soil conditions and plant growth, 11th edn. New York: Longman Scientific Technical, 899-926.
104. Saglio PH, Drew MC, Pradet A. 1988. Metabolic acclimation to anoxia induced by low (2-4 kPa partial pressure) oxygen pretreatment (hypoxia) in root tips of Zea mays. Plant Physiology 86: 61-66.
105. 2-rich lowland streams. Oecologia 117: 31-39.
106. Segel IH. 1976. Biochemical calculations, 2nd edn. New York: John Wiley and Sons.
107. 2 in floodwater and in internodal lacunae of floating rice growing at 1-2 meter water depths. Plant, Cell and Environment 10: 767-776.
108. Shannon RD, White JR, Lawson JE, Gilmour BS. 1996. Methane flux from emergent vegetation in peat lands. Journal of Ecology 84: 239-246.
109. Shipway MR, Bramlage WJ. 1973. Effects of carbon dioxide on activity of apple mitochondria. Plant Physiology 51: 1095-1098.
110. Stolwijk JAJ, Thimann KV. 1957. On the uptake of carbon dioxide and bicarbonate by roots, and its influence on growth. Plant Physiology 32: 513-520.
111. Summers JE, Ratcliffe RG, Jackson MB. 2000. Anoxia tolerance in the aquatic monocot Potamogeton pectinatus: absence of oxygen stimulates elongation in association with an unusually large Pasteur effect. Journal of Experimental Botany 51: 1413-1422.
112. Tanaka A, Navasero SA. 1967. Carbon dioxide and organic acids in relation to the growth of rice. Soil Science and Plant Nutrition 13: 25-30.
113. 2 uptake and synthesis of fermentative end products by root segments. Journal of Experimental Botany 40: 985-991.
114. Trought MCT, Drew MC. 1980a. The development of waterlogging damage in wheat seedlings (Triticum aestivum L.). I. Shoot and root growth in relation to changes in concentrations of dissolved gases and solutes in the soil solution. Plant and Soil 54, 77-94.
115. Trought MCT, Drew MC. 1980b. The development of waterlogging damage in young wheat plants in anaerobic solution cultures. Journal of Experimental Botany 31: 1573-1585.
116. Tyerman SD, Niemietz CM, Bramley H. 2002. Plant aquaporins: multifunctional water and solute channels with expanding roles. Plant, Cell and Environment 25: 173-194.
117. - uptake and fusicoccin in root hairs of Limnobium stoloniferum. Plant Physiology 94: 1561-1567.
118. Visser EJW, Nabben RHM, Blom CWPM, Voesenek LACJ. 1997. Elongation by primary lateral roots and adventitious roots during conditions of hypoxia and high ethylene concentrations. Plant, Cell and Environment 20: 647-653.
119. Warncke J, Slayman CL. 1980. Metabolic modulation of stoichiometry in a proton pump. Biochimica et Biophysica Acta 591: 224-233.
120. Williamson RE. 1968. Influence of gas mixtures on cell division and root elongation of broad bean, Vicia faba L. Agronomy Journal 60: 317-321.
121. Winter H, Robinson DG, Heldt HW. 1993. Subcellular volumes and metabolite concentrations in barley leaves. Planta 191: 180-190.
122. + extrusion and cytoplasmic pH in maize root tips acclimated to a low-oxygen environment. Plant Physiology 111: 227-233.
123. Yao H, Conrad R. 2000. Effect of temperature on reduction of iron and production of carbon dioxide and methane in anoxic wetland rice soils. Biology and Fertility of Soils 32: 135-141.
124. Yao H, Conrad R, Wassmann R, Neue HU. 1999. Effect of soil characteristics on sequential reduction and methane production in sixteen rice paddy soils from China, the Philippines and Italy. Biogeochemistry 47: 267-293.
125. Ying J, Peng S, He Q, Yang H, Yang C, Visperas RM, Cassman KG. 1998. Comparison of high-yield rice in tropical and subtropical environments. I. Determinants of grain and dry matter yields. Field Crops Research 57: 71-84.
126. m values of ribulose bisphosphate carboxylase to half. Presentation of a monograph and an equation for determining the pK values. Biophysical and Biochemical Research Communications 131: 1075-1079.
127. Yu PT, Stolzy LH, Letey J. 1969. Survival of plants under prolonged flooding conditions. Agronomy Journal 61: 844-847.
128. 2+ and its subcellular compartmentation in fission yeast, Schizosaccharomyces pombe. Cellular and Molecular Life Sciences 53: 69-72.