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Oxygen Transport in Waterlogged Plants

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Waterlogging Signalling and Tolerance in Plants

Abstract

In flooded soils, roots are exposed to a reducing environment with low oxygen availability. In order to supply roots with sufficient oxygen for respiration, most wetland plants form extended gas-filled cavities known as aerenchyma (in the root) or lacunae (in the shoot). Oxygen transport can be either diffusive or convective; according to general belief, the latter is restricted to the existence of separate “inlet” and “outlet” structures, e.g. in extended rhizomes. Mainly three separate mechanisms of convective oxygen transport have been identified so far: (1) Humidity-induced pressurization/convection that is driven by a difference in vapour pressure between the water-saturated gas phase of the leaf intercellulars and the microenvironment. When a significant overpressure in the gas phase of the leaf is maintained, gas flow to a distant “outlet”, being at atmospheric pressure, is generated. (2) Thermal osmosis, a mass flow of gas into the leaf driven by heat transfer in the opposite direction and (3) Venturi-induced convection, a gas flow initiated by an underpressure in the gas phase of broken culms (e.g. of Phragmites communis) that is generated by wind passing over them. Species with extended pathways for gas transport (with formation frequently being induced by hypoxia or anoxia) dominate in wetland communities and can even provide the rhizosphere of flooded soils with oxygen.

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Abbreviations

ATP:

Adenosine triphosphate

\( {c_{{{\rm{O}}_{\rm{2}}}}} \) :

Oxygen concentration

\( {C_{{{\rm{0}}}}} \) :

Initial Oxygen concentration

COPR:

Critical oxygen pressure for respiration

D:

Diffusion coefficient

\( {k_{\rm{H}}} \) :

Henry’s gas constant for O2 in water

\( {J_{{{\rm{O}}_2}}} \) :

Oxygen flux

l :

Root length

M :

Respiratory demand

P(O2):

Oxygen partial pressure

Q :

Oxygen consumption by respiration

\( {R_0} \) :

Root radius

ROL:

Radial oxygen loss

\( {R_{\rm{SH}}} \) :

Diffusional resistance between root surface and oxygen electrode

\( {R_{\rm{T}}} \) :

Complex resistance of the root tissue (includes root porosity, consumption of O2 along the pathway by respiration and radial loss, and the diffusional resistance for radial O2 transport)

є :

Fractional porosity of the root

T :

Temperature

τ :

Tortuosity of a diffusion pathway

ρ :

Air density

v :

Wind speed

\( {\nabla^2} \) :

Laplacian operator

References

  • Afreen F, Zobayed SMA, Armstrong J, Armstrong W (2007) Pressure gradients along whole culms and leaf sheaths, and other aspects of humidity-induced gas transport in Phragmites australis. J Exp Bot 58:1651–1662

    Article  CAS  PubMed  Google Scholar 

  • Arber A (1920) Water plants. A study of aquatic angiosperms. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Armstrong J, Armstrong W (1991) A convective throughflow of gases in Phragmites australis (Cav.) Trin. ex Steud. Aquat Bot 39:75–88

    Article  Google Scholar 

  • Armstrong J, Armstrong W, Beckett PM (1992) Phragmites australis: venturi- and humidity-induced pressure flows enhance rhizome aeration and rhizosphere oxidation. New Phytol 120:197–207

    Article  Google Scholar 

  • Armstrong J, Armstrong W, Beckett PM, Halder JE, Lythe S, Holt R, Sinclair A (1996a) Pathways for aeration and the mechanisms and beneficial effects of humidity- and Venturi-induce convections in Phragmites australis (Cav.) Trin. ex. Steud. Aquat Bot 54:177–197

    Article  Google Scholar 

  • Armstrong W, Armstrong J, Beckett PM (1996b) Pressurized ventilation in emergent macrophytes: the mechanism and mathematical modelling of humidity-induced convection. Aquat Bot 54:121–135

    Article  Google Scholar 

  • Armstrong J, Jones RE, Armstrong W (2006) Rhizome phyllosphere oxygenation in Phragmites and other species in relation to redox potential, convective gas flow, submergence and aeration pathways. New Phytol 172:719–731

    Article  CAS  PubMed  Google Scholar 

  • Armstrong W (1964) Oxygen diffusion from the roots of some British bog plants. Nature (Lond) 204:801–802

    Article  CAS  Google Scholar 

  • Armstrong W (1979) Aeration in higher plants. Adv Bot Res 7:225–332

    Article  CAS  Google Scholar 

  • Armstrong W, Armstrong J (2005) Stem photosynthesis not pressurized ventilation is responsible for light-enhanced oxygen supply to submerged roots of alder (Alnus glutinosa). Ann Bot 96:591–612

    Article  CAS  PubMed  Google Scholar 

  • 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 Phytol 105:221–245

    Article  Google Scholar 

  • Armstrong W, Wright EJ (1975) Radial oxygem loss from roots: the theoretical basis for the manipulation of flux data obtained by the cylindrical plantinum electrode technique. Physiol Plant 35:21–26

    Article  Google Scholar 

  • Armstrong W, Healy MT, Webb T (1982) Oxygen diffusion in pea. I Pore space resistance in the primary root. New Phytol 91:647–659

    Article  Google Scholar 

  • Armstrong W, Healy MT, Lythe S (1983) Oxygen diffusion in pea II. Oxygen concentration in the primary root apex as affected by growth, the production of laterals and radial oxygen loss. New Phytol 94:549–559

    Article  Google Scholar 

  • Armstrong W, Cousins D, Armstrong J, Turner W, 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. Ann Bot 86:687–703

    Article  Google Scholar 

  • Armstrong W, Webb T, Darwent M, Beckett PM (2009) Measuring and interpreting critical oxygen pressures in roots. Ann Bot 103:281–293

    Article  PubMed  Google Scholar 

  • Bendix M, Tornberg T, Brix H (1994) Internal gas transport in Typha latifolia L and Typha angustifolia L. I. Humidity-induced pressurization and convective throughflow. Aquat Bot 49:75–90

    Article  Google Scholar 

  • Blom CWPM (1999) Adaptations to flooding stress: from plant community to single molecule. Plant Biol 1:261–273

    Article  CAS  Google Scholar 

  • Bowling DJF (1973) Measurement of a gradient of oxygen partial pressure across the intact root. Planta 111:323–328

    Article  CAS  Google Scholar 

  • Brix H (1989) Gas exchange through dead culms of reed, Phragmites australis (Cav.) Trin. ex Steudel. Aquat Bot 35:81–98

    Article  Google Scholar 

  • Brix H, Sorrell BK, Schierup H-H (1996) Gas fluxes achieved by in situ convective flow in Phragmites australis. Aquat Bot 54:151–163

    Article  Google Scholar 

  • Colmer TD (2003) Long-distance transport of gases in plants: a perspective on internal aeration and radial oxygen loss from roots. Plant Cell Environ 26:17–36

    Article  CAS  Google Scholar 

  • Colmer TD, Pedersen O (2008) Oxygen dynamics in submerged rice (Oryza sativa). New Phytol 178:326–334

    Article  CAS  PubMed  Google Scholar 

  • Colmer TD, Gibbered MR, Wiengweera A, Tinh TK (1998) The barrier to radial oxygen loss from roots of rice (Oryza sativa L) is induced by growth in stagnant solution. J Exp Bot 49:1431–1436

    Article  CAS  Google Scholar 

  • Dacey JWH (1980) Internal winds in water lilies: an adaptation for life in aerobic environments. Science 210:1017–1019

    Article  CAS  PubMed  Google Scholar 

  • Dedes D, Woermann D (1996) Convective gas flow in plant aeration and thermo-osmosis: a model experiment. Aquat Bot 54:111–120

    Article  Google Scholar 

  • De Willingen P, van Noordwijk M (1984) Mathematical models on diffusion of oxygen to and within plant roots, with special emphasis on effects of soil-root contact. I. Derivation of the models. Plant Soil 77:215–231

    Article  Google Scholar 

  • Garthwaite AJ, Armstrong W, Comer TD (2008) Assessment of O2 diffusivity across the barrier to radial O2 loss in adventitious roots of Hordeum marinum. New Phytol 179:405–416

    Article  CAS  PubMed  Google Scholar 

  • Gibbs J, Turner DW, Armstrong W, Sivasithamparam K, Greenway H (1998) Response to oxygen deficiency in primary maize roots. II. Development of oxygen deficiency in the stele has limited short-term impact on radial hydraulic conductivity. Aust J Plant Physiol 25:759–763

    Article  CAS  Google Scholar 

  • Greenwood DJ (1967) Studies on oxygen transport through mustard seedlings. New Phytol 66:597–606

    Article  Google Scholar 

  • Grosse W (1996) The mechanism of thermal transpiration (=thermal osmosis). Aquat Bot 54:101–110

    Article  Google Scholar 

  • Grosse W, Schröder P (1984) Oxygen supply of roots by gas transport in alder trees. Zeitschr Naturf 93c:1186–1188

    Google Scholar 

  • Grosse W, Frye J, Lattermann S (1992) Root aeration in wetland trees by pressurized gas transport. Tree Physiol 10:2285–2295

    Google Scholar 

  • Grosse W, Schulte A, Fujita H (1993) Pressurized gas transport in two Japanese alder species in relation to their natural habitats. Ecol Res 8:151–158

    Article  Google Scholar 

  • Jackson MB, Ishizawa K, Ito O (2009) Evolution and mechanism of plant tolerance in flooding stress. Ann Bot 103:137–142

    Article  CAS  PubMed  Google Scholar 

  • Jackson MB, Armstrong W (1999) Formation of aerenchyma and the process of plant ventilation in relation to soil flooding and submergence. Plant Biol 1:274–287

    Article  CAS  Google Scholar 

  • Justin SHFW, Armstrong W (1987) The anatomical characteristics of roots and plant response to soil flooding. New Phytol 106:465–495

    Google Scholar 

  • Kaufmann I, Jakob P, Schneider HU, Zimmermann U, Wegner LH (2010) Kinetics of water loss and re-hydration in maize roots exposed to temporal water deprivation. An MR imaging study. New Phytol, submitted

    Google Scholar 

  • Lambers H, Smakman G (1978) Respiration of the roots of flood-tolerant and flood-intolerant Senecio species: affinity for oxygen and resistance to cyanide. Physiol Plant 42:163–166

    Article  CAS  Google Scholar 

  • Lambers H, Steingröver E (1978) Efficiency of root respiration of a flood-tolerant and a flood-intolerant Senecio species as affected by low oxygen tension. Physiol Plant 42:179–184

    Article  Google Scholar 

  • Lambers H, Steingröver E, Smakman G (1978) The significance of oxygen transport and of metabolic adaptation in flood-tolerance of Senecio species. Physiol Plant 43:277–281

    Article  CAS  Google Scholar 

  • Mancuso S, Papeschi G, Marras AM (2000) A polarographic, oxygen-selective vibrating-microelectrode system for the spatial and temporal characterisation of transmembrane oxygen fluxes in plants. Planta 211:384–389

    Article  CAS  PubMed  Google Scholar 

  • Mainiero R, Kazda M (2005) Effects of Carex rostrata on soil oxygen in relation to soil moisture. Plant Soil 270:311–320

    Article  CAS  Google Scholar 

  • Mevi-Schutz J, Grosse W (1988) A two-way gas transport system in Nelumbo nucifera. Plant Cell Environ 11:27–34

    Article  Google Scholar 

  • Michael W, Cholodova VP, Ehwald R (1999) Gas and liquids in intercellular spaces of maize roots. Ann Bot 84:665–673

    Article  CAS  Google Scholar 

  • Pang JY, Newman I, Mendham N, Zhou M, Shabala S (2006) Microelectrode ion and O2 fluxes measurements reveal differential sensitivity of barley root tissues to hypoxia. Plant Cell Environ 29:1107–1121

    Article  CAS  PubMed  Google Scholar 

  • Raskin I, Kende H (1983) How does deep water rice solve its aeration problem. Plant Physiol 72:447–454

    Article  CAS  PubMed  Google Scholar 

  • Seago JL, Marsh LC, Stevens KJ, Soukup A, Votrubova O, Enstone DE (2005) A re-examination of the root cortex in wetland flowering plants with respect to aerenchyma. Ann Bot 96:565–579

    Article  PubMed  Google Scholar 

  • Skelton NJ, Allaway WG (1996) Oxygen and pressure changes measured in situ during flooding in roots of the Grey Mangrove Avicennia marina (Forssk.) Vierh. Aquat Bot 54:165–175

    Article  Google Scholar 

  • Sorell BK, Brix H, Orr PT (1997) Eleocharis sphacelata: internal gas transport pathways and modelling of aeration by pressure flow and diffusion. New Phytol 136:433–442

    Article  Google Scholar 

  • Thomson CJ, Greenway H (1991) Metabolic evidence for stelar anoxia in maize roots exposed to low O2 concentrations. Plant Physiol 96:1294–1301

    Article  CAS  PubMed  Google Scholar 

  • Van Noordwijk M, De Willingen P (1984) Mathematical models on diffusion of oxygen to and within plant roots, with spezial emphasis on effects of soil-root contact. Plant Soil 77:233–241

    Article  Google Scholar 

  • Visser EJW, Colmer TD, Blom CWPM, Voesenek LACJ (2000) Changes in growth, porosity, and radial oxygen loss from adventitious roots of selected mono- and dicotyledonous wetland species with contrasting types of aerenchyma. Plant Cell Environ 23:1237–1245

    Article  Google Scholar 

  • Vretare V, Weisner SEB (2000) Influence of pressurized ventilation on performance of an emergent macrophyte (Phragmites australis). J Ecol 88:978–987

    Article  Google Scholar 

  • Westhoff M, Zimmermann D, Zimmermann G, Gessner P, Wegner LH, Bentrup FW, Zimmermann U (2009) Distribution and function of epistomatal mucilage plugs. Protoplasma 235:101–105

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

I received financial support by a grant provided by the “Karlsruhe Institute of Technology” within the framework of the “German excellence initiative”. I would also like to thank Prof Tim Colmer for the critical reading of the manuscript.

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Authors and Affiliations

  1. Plant Bioelectrics Group, Karlsruhe Institute of Technology, Institute of Botany I and Institute of Pulsed Power and Microwave Technology, Hermann-von-Helmholtz Platz 1, 76344, Eggenstein-Leopoldshafen, Germany

    Lars H. Wegner

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  1. Lars H. Wegner
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Correspondence to Lars H. Wegner .

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Editors and Affiliations

  1. Dipto. Ortoflorofrutticoltura, Università Firenze, Viale delle Idee 30, Sesto Fiorentino, 50019, Italy

    Stefano Mancuso

  2. School of Agricultural Sciences, University of Tasmania, Hobart, Australia

    Sergey Shabala

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Wegner, L.H. (2010). Oxygen Transport in Waterlogged Plants. In: Mancuso, S., Shabala, S. (eds) Waterlogging Signalling and Tolerance in Plants. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-10305-6_1

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