I

Synthesis of Preservation of Metabolism of adaptive enzymes membrane integrity anaerobic products

Increase in relative use of pentose phosphate pathway

Reversal of end stages of fermentation

Reversal of parts of the TCA cycle increase in role of glycolysis in maintaining ATP levels

Fig. 8.5 Diagrammatic representation of the diversity of adaptations in higher plants that can contribute to their tolerance of flooding. (Reproduced from Crawford & Braendle, 1996.)

Table 8.2. Summary of aspects of anaerobic physiology that impact on flooding tolerance and that can vary in their effect at different seasons of the year in wetland and dryland species

Event

Wetland species

Dryland species

References

Survival under anoxia

Ethanol accumulation

Alcohol dehydrogenase induction

Acetaldehyde generation and toxicity

Carbohydrate utilization

Post-anoxic lipid destruction

Seed reserves

Germination phenology

Perennating organs of amphibious species (e.g. rhizomes, stolons and turions) have prolonged tolerance of anoxia

In intact amphibious species some accumulation on initial flooding then stabilization due to ethanol dispersal mechanisms

Less active induction in comparison with intolerant species

Rice during early stages of germination is tolerant of acetaldehyde up to 200 mM

Slow usage of carbohydrates and maintenance of high levels of free sugars

Little damage in species tolerant of prolonged anoxia

Exclusively carbohydrates, fructans in grasses

Inhibited by water; requiring oscillating temperatures

Rhizomes when flooded become unviable and are readily killed by short periods of anoxia (less than 1 week)

Continued accumulation to high levels in roots and rhizomes of species with only a short-term tolerance of anoxia

Normally rapid response with marked increases

Highly damaging in Avena sativa and most other crop species

Crawford & Braendle, 1996

Schlüter & Crawford, 2001; Wuebker et al., 2001

Baxter-Burrell et al., 2002; Fukao et al., 2003; Tamura et al., 1996; Bertrand et al., 2001, 2003

Kato-Noguchi, 2002; Boamfa et al., 2003

Rapid depletion of carbohydrate Braendle, 1991; Hanhijarvi &

reserves including free sugars under Fagerstedt, 1995 low oxygen stress

Massive damage in anoxia-sensitive Hunter et al., 1983; Kolb et al., 2002 species

Various

Bertrand et al, 2003; Crawford, 1992

Rapid germination on imbibition for Baskin & Baskin, 1998; Jutila, 2001 crop species

Event

Wetland species

Dryland species

References

Germination physiology

Seedling response to anoxia

Metabolic response of mature plant to anoxia

Ice encasement

Elevated alcohol dehydrogenase activity; availability of free sugars under anoxia; ability to disperse ethanol and lactate

Rice coleoptile and first leaf tolerant of anoxia; also tolerant of acetaldehyde. Weeds of rice crops have also evolved tolerance of anoxia over the germination period

Down-regulation of metabolism during prolonged anoxia

Highest frequency of tolerance of ice encasement and anoxia tolerance found in plants of the High Arctic flora

Seeds require prompt rupture of testa to ensure adequate access to oxygen

Most seedlings are intolerant of

Acceleration of glycolysis to overcome short-term oxygen shortages

Crop plants that are damaged by ice encasement have higher rates of winter anaerobic metabolism and glycolytic activity under anoxia than those that survive ice encasement

Kolb et al, 2002; Crawford, 1992; Legesse & Powell, 1992, 1996

Biswas et al., 2002; Kato-Noguchi, 2002; Crawford, 1989

Schlüter & Crawford, 2001, 2003; Crawford et al., 1987

Crawford et al., 1994; Bertrand et al., 2003

growth is renewed, the acrotelm becomes shallower, and trees disappear from the surface of the bog. Raised bogs appear to be more sensitive to climatic change than Atlantic blanket bogs. There is a greater synchrony of the carbon dates for the buried layers of pine stumps in raised than in the Atlantic blanket bogs in Ireland, presumably due to the lower rainfall that is experienced by raised bogs (McNally & Doyle, 1984).

8.1.2 Seasonal responses to flooding

Flooding injury arises in winter and summer from the same basic cause, namely oxygen deprivation. Whether or not oxygen deprivation is more dangerous to plants in summer than in winter depends on the particular circumstances under which flooding occurs. In temperate regions with mild winters, summer water tables are generally lower than in winter, which makes flooding less frequent and of shorter duration. However, even though the summer flooding may be brief, the warmer conditions of the growing season will result in higher rates of metabolic oxygen demand.

Potentially acute oxygen shortages are usually avoided during the growing phase, as many species have available a range of adaptive escape mechanisms for overcoming or alleviating the dangers of hypoxia or anoxia. The principal adaptations are mainly based on phenotypic plasticity in growth responses to flooding which is possible in summer when plants are growing but is generally denied in winter. In summer, the renewed growth of adventitious roots and the speedy development of aerating tissues within the roots in response to flooding facilitate oxygen diffusion from the shoot to the root (Armstrong et al., 1996). Similarly, for species that can survive total inundation, extension of shoots and petioles enables leaves and flowers to be raised up to or above the water surface, and restores access to air for the submerged parts of the plant.

8.2 AERATION 8.2.1 Radial oxygen loss

Given the large quantities of air and oxygen that can circulate within the plant body during the growing season, it is not surprising that some is lost to the plant exterior. The extent of this loss varies with both the position and nature of the various parts of the plant. It can therefore happen, even though the vascular cylinder is hypoxic and the root meristems almost anoxic, that a radial oxygen loss from the root system takes place, as the diffusion resistance from the cortex of fine roots to the outside is often lower than that from the vascular cylinder.

Radial oxygen loss has both advantages and disadvantages for plant survival. Frequently, the loss of oxygen from the root to the soil environment in reducing soil conditions is high enough to oxidize the root environment up to a distance of several millimetres from the root surface. Laboratory investigations give some indication of the amount of oxygen that is released from the roots of wet plants into reduced soils. Experiments using individual plants of cat's tail (Typha latifolia) and soft rush (Juncus effusus) in hydroponic systems have shown that oxygen-release intensities vary between the species as well as depending on the redox state of the rhizosphere. Typha latifolia had the highest release rates with mean values of 1.1 mg h—1 plant while J. effusus recorded 0.5 mg h—1 plant at Eh values approximating to —200 mV for both species. The oxygen-release state was governed by the size of the above-ground biomass and intensification of illumination for T. latifolia. However, for J. effusus the intensity of illumination was less important (Wiessner et al., 2002).

The ability to raise the redox potential at the root surface oxidizes the reduced, and potentially toxic, soluble forms of iron and manganese, which then become insoluble and form a plaque on the root surface. The formation of this plaque is a property of living roots. Dying roots (e.g. roots affected by insects, fungi, mechanical damage, or senescence) are not able to increase the redox potential. The continued formation of plaque will, however, reduce the efficiency of roots as absorbing organs for water and nutrients.

Nevertheless, despite these adaptations some reduced soil ions pose an ever-present risk. In both the common reed (Phragmites australis) and the sweet flag (Acorus calamus) the formation of non-protein thiols indicate that the detoxification of sulphides can be detected more readily in rhizomes than in roots. The capacity for detoxification is limited, however, and there is always a possibility of sulphide injury (Fiirtig et al., 1996). The plaques of iron and manganese deposited on their root surfaces have a high capacity for binding phosphorous. When water lobelia (Lobelia dortmanna; Fig. 8.6) was grown under such conditions for six months the formation of plaques on the lobelia roots restricted both phosphorous uptake and biomass production (Christensen et al., 1998). A similar situation can be found in some typically aquatic submerged rosette plants with well-developed roots (often termed isoetids although taxonomically distinct) such as shore-weed (Littorella uniflora; Fig. 8.7) and quillwort (Isoetes lacustris). This is particularly likely when they are growing at depths of 2-5 m where Eh values are low

Lobelia Dortmanna
Fig. 8.6 Water lobelia (Lobelia dortmanna) growing in a Scottish mountain loch. This species is confined to nutrient poor waters probably as a consequence of plaque formation from oxidized deposits on the roots inducing phosphate deficiency (see text).

(<100 mV). Despite a high phosphate content in the sediment the isoetids showed low biomass and low phosphorus content (Christensen et al., 1998). In both these cases the release of oxygen from the roots of the aquatic species, although preventing the uptake of potentially toxic concentration of iron and manganese, leads eventually through plaque formation to a reduction in growth due to phosphate deficiency.

Radial oxygen loss from the upper portions of the root can also limit the effectiveness of aerenchyma in facilitating oxygen diffusion downwards. The relative distribution of aerenchyma along the root has therefore a profound effect in enabling the more distal regions of the root to have an adequate oxygen supply. Assessments of the anatomy, porosity, and radial oxygen loss profiles from adventitious roots in the Poaceae and Cyperaceae have identified a combination of features characteristic of species that inhabit wetland environments. These included a strong barrier to radial oxygen loss in the basal regions through cell suberization of the adventitious roots and extensive aerenchyma formation when grown in both stagnant and aerated nutrient solutions (McDonald et al., 2002).

8.2.2 Thermo-osmosis

A number of amphibious and aquatic species, e.g. aquatic species with floating leaves as well as the common reed (Phragmites australis), are able to use the heat energy of the sun during the growing season to pump air to their

Fig. 8.7 Shoreweed (Littorella uniflora) growing at the edge of a shallow loch in Orkney. (Left) While submerged this lake-margin species remains vegetative. (Right) Flowering when the lake level recedes. Photograph taken in late summer when the plant is seeding.

Fig. 8.8 White water lilies (Nymphaea alba), a species that uses solar energy via a process of thermo-osmosis to ventilate the submerged portions of the plant (see text).

submerged organs by thermo-osmosis (Figs. 8.8-8.9). A prerequisite for air transport by thermo-osmosis is a layer with very small pores or intercellular spaces (<0.1 im) and a high humidity inside the plant organ. Once air has passed through the small pores it is heated by the sunlight and mixed with the water vapour inside the organ. As a result of increasing temperature, the higher molecular motion of gas molecules leads to a longer critical path, which reduces the probability of escape from within the leaf. Pressure therefore increases as cool air continues to diffuse inwards. This increased internal gaseous pressure forces gas downwards which develops into a flow-through system in rhizomatous species as air can exit through the underground organs into the older leaves where the pores (dilated intercellular spaces) are much bigger (Knudsen diffusion). It has been estimated that in the common reed (Phragmites australis) the flow through rate is sufficient to maintain the oxygen concentration of the submerged rhizomes at 90% of atmospheric concentration (Armstrong et al., 1992).

The effectiveness of shoots in aerating underground rhizomes of emergent aquatic macrophytes was strikingly illustrated in a study of radial oxygen loss

Fig. 8.9 Colony of giant Amazonian water lilies (Victoria regina) growing typically in shallow nutrient rich water in a backwater (Varzea) of the River Amazon near Manaus (Brazil). A single leafand petiole of this species can aerate the submerged organs by thermo-osmotic gas flow rates of up to 5000 ml h_1 (Grosse et al, 1991).

Fig. 8.9 Colony of giant Amazonian water lilies (Victoria regina) growing typically in shallow nutrient rich water in a backwater (Varzea) of the River Amazon near Manaus (Brazil). A single leafand petiole of this species can aerate the submerged organs by thermo-osmotic gas flow rates of up to 5000 ml h_1 (Grosse et al, 1991).

from rhizome apices of Phragmites australis (Armstrong et al., 2006). Radial oxygen loss from rhizome apices of Phragmites was increased by convective gas flow through the rhizome even when only the tips of the shoot emerged above the floodwater (Fig. 8.10). It was concluded that oxygen passes via internal gas-space connections between aerial shoot, rhizome and underground buds and into the phyllosphere regions via scale-leaf stomata and surfaces on the submerged rhizome buds. It was also suggested that the oxidized phyllospheres may protect rhizome apices against phytotoxins in waterlogged soils, just as oxidized rhizospheres protect roots.

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