18.1.2  Adaptive responses to waterlogging

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What mechanisms do plants use to adapt to the hostile en-vironment of waterlogged soils and to submergence of shoots during floods? Anatomical and morphological adaptations in roots, shoots and stems allow ventilation of submerged organs and lessen or even avoid the impact of waterlogging and flooding. In some plants, such as grasses, these structural adap-tations are linked to the action of plant growth regulators, in particular the gaseous hormone ethylene. A common view of how ethylene exerts its effect on flooded tissues entails several factors: ethylene synthesis accelerates under O2 deficits, diffusion of ethylene away from tissues is impeded when surrounding gases are replaced by water and perception of ethylene by receptor molecules also changes developmentally.

There are also metabolic adaptations which confer tolerance to anoxia, prolong tissue survival and, in a few exceptional cases, even allow growth in the absence of O2. When tissues are completely submerged and O2 is exhausted by respiration, complete anoxia can occur. The few higher plant species which tolerate this condition are rhizomes, tubers and shoots of some wetland species and germinating seeds of rice, barnyard grass and other weeds found in paddy fields. More commonly, submerged plant organs (e.g. roots and tubers) form anoxic ‘cores’ deep within the tissue, surrounded by zones of hypoxic or aerobic tissue, which derive O2 by diffusion from adjacent waterlogged soil or airspaces (aerenchyma) within the ground tissues. For example, coexistence of an anoxic stele and aerobic cortex in maize roots exposed to intermediate O2 deficiency has been demonstrated using microelectrodes (Figure 18.3) and biochemical indicators of fermentative metabolism (Thomson and Greenway 1991). In keeping with the view that ‘plants are unlikely to adapt to their environment in a single-minded manner’ (Davies 1980) one might expect that plants tolerant to waterlogging and flooding would engage a combination of adaptive mechanisms.

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Figure 18.3 O2 concentration (mM) measured across a maize root by using an O2 - sensitive microelectrode. The transect was through differentiated tissues 75 mm from the apex of a 135 mm long root. O2 concentration in the bathing medium was about 0.05 mM (hypoxia), causing the abrupt gradient in oxygen status observed. (Courtesy W. Armstrong)

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Figure 18.4 Transverse sections of adventitious roots of (a) rice an (b) maize taken 50 mm from the root apex and showing lysigenous aerenchyma formation. Note the cubic cell packing in the rice cortex contrasting with the hexagonal packing in maize. (Micrographs courtesy E. Armstrong)

(a)  Anatomical adaptations

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Figure 18.5 Transverse sections of a lateral root of Rumex hydrolapathum showing schizogenous aerenchyma formation about 5 mm from the apex (Micrograph courtesy W. Armstrong)

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Figure 18.6 Root growth of rice seedlings relies on transport of O2 from the atmosphere surrounding shoots. Elongation of a 7cm long root was measured in an anoxic solution using a travelling microscope while O2 concentrations denoted by arrows below the growth curve (kPa). Note air contains about 21 kPa O2. O2 supply to roots through aerenchyma decreased accordingly, resulting in lower O2 concentrations (kPa) at the surface of root tips, denoted by arrows above the growth curve (Based on Armstrong and Webb 1985)

Armstrong and co-workers from the University of Hull, UK, have made the most thorough analysis of O2 transport from shoots to roots in waterlogged soils, giving quantitative argu-ments for internal ventilation as a factor in flood tolerance (Armstrong et al. 1993). Adequate supply of O2 to submerged organs requires enhanced development of internal gas spaces, principally by formation of large interconnected lacunae called aerenchyma (Figures 18.4 and 18.5). The geometry of cell packing prior to gas spaces forming also affects how porous aerenchymatous tissues can become. For example, cubic cell packing, observed in rice roots (Figure 18.4a), has a maximum porosity of 22% while hexagonal cell packing, as in maize (Figure 18.4b), has a maximum of only 9%. Greatly enhanced root porosity achieved through formation of aerenchyma improves gas movement, mostly by diffusion but in some species of reeds and waterlilies also by convection. Improved delivery of O2 to roots by simple diffusion through aerenchyma can be demonstrated in rice, a species with exceptional tolerance to O2 deficiency. When O2 concen-trations in the gas phase around shoots were lowered, O2 release at the root tip decreased within minutes, reflecting successively smaller concentration gradients driving O2 diffusion downwards through aerenchyma (Figure 18.6).

In large aquatic macrophytes such as Phragmites australis, mass flow of gases (convection) is generated within the plant by both Venturi- and humidity-induced gradients. Continuity of gas spaces through leaf sheathes, rhizomes and major root axes provides a complex pathway for such a gas flow. Con-vective O2 flow can raise rhizosphere redox potential from critically low values around of –250 mV to 500 mV, keeping the medium surrounding delicate growing apices free of phytotoxins like H2S and Fe2+. Venturi-induced gradients entail wind blowing across old, broken culms to create a suction through submerged rhizomes; suction depends on the square of wind speed so gusts of wind during the day or night can ventilate root systems. Humidity-induced gradients are created through dilution of O2 in substomatal airspaces by water evaporating from cell walls; atmospheric O2 then diffuses into leaves through stomata and flows under pressure to roots through internal gas spaces. Humidity-induced flows depend on heat to evaporate water and light to keep stomata open — they are a daytime phenomenon. These pressurised flows have the added advantage of flushing excess CO2 and ethylene out of the roots of aquatic plants, preventing build up to unfavourable levels. Internal ventilation promotes survival and growth of roots in a soil environment essentially devoid of O2, in much the same way that a snorkel allows a swimmer to breathe under water. Finally, O2 transport is not the only ad-vantage of internal gas spaces for aquatic plants. By committing 10–50% of tissue volume to gas spaces, carbohydrate demand for tissue maintenance is significantly reduced, leaving reserves for the metabolic adjustments discussed in Section 18.1.2c.

Aerenchyma formation is induced by poor aeration in common plants as diverse as Rumex species, dicotyledonous marsh plants, through to dryland cereals like maize and wheat. Aerenchyma form by two distinct developmental processes: lysigeny — the collapse of files of cells (Figure 18.4) — and schizogeny — cell separation characteristic of many dicoty-ledonous wetland species (Figure 18.5). With inhibitors, Jackson and co-workers (Jackson and Drew 1984) demonstrated that lysigenous formation of aerenchyma in the cortex of poorly aerated maize is mediated by ethylene. They also showed that low O2 concentrations stimulated ethylene synthesis in maize roots, possibly through increased synthesis of the ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC) in the anoxic stele that develops within O2-deficient roots (see Figure 18.3); ACC produced in this anoxic stele can diffuse radially into the aerobic cortex where it is converted to ethylene. In tomato, two ACC synthase genes are induced by anoxia, consistent with increased ACC synthesis in flooded roots. If little is known about lysigenous aerenchyma formation, almost nothing is known of the mechanism of schizogeny. Adjacent cell walls appear to separate by weakening of the middle lamella but how any ‘wall weakening factors’ are coordinated awaits discovery.

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Table 18.2

Root systems are morphologically diverse with categories of roots having distinct capacities to form aerenchyma in waterlogged soils. For example, when wheat roots are water-logged, adventitious (nodal) roots develop a greater proportion of aerenchyma than seminal roots, allowing plants to survive even when seminal roots have died. Mathematical models based on O2 transport rates accurately predict the maximum length to which adventitious roots can grow in waterlogged soil; this length depends on the proportion of aerenchyma (Table 18.2). Logically, waterlogged plants generally have shorter roots than those in drained soil because of the restriction imposed by long-distance O2 delivery through aerenchyma.

(b)  Morphological adaptations

In addition to anatomical adaptations, plants can adapt mor-pho-logically to mitigate O2 deprivation during waterlogging or submergence. For example, fine surface roots proliferate in response to waterlogging in both dryland species (e.g. pea) and marsh plants (e.g. Melaleuca spp.). These surface roots benefit from a thin aerobic layer at the surface of waterlogged soil (Case study 18.1). Fine roots can use their large surface area to volume ratio to scavenge O2 effectively from surface water, at the same time generating energy for nutrient acquisition from this enriched zone.

In a number of flood-tolerant plant species, shoots elongate following submergence to establish a connection with the atmosphere, so allowing ventilation of the submerged plant parts. Examples include the anaerobic elongation of a rice coleoptile after its seed has been sown directly into water and elongation of stem internodes following inundation. Aquatic species capable of extraordinary stem elongation include deepwater and floating rices from Southeast Asia and the dicotyledonous Rumex species from European flood plains (see Figure 18.5). Native waterlilies like Nymphaea gigantea from tropical Australia produce petioles more than 2 m long to raise their leaves and flowers to the water surface. As with aerenchyma formation, ethylene entrapped within submerged tissues often plays a role in adaptation, for example enhancing stem elongation in rice (Raskin and Kende 1984a) and Rumex species (Blom et al. 1990). How this extraordinary elongation is achieved at the cell level is not clear but ethylene is unlikely to be the sole hormonal factor in the phenomenon. Gibberellins, for example, contribute to internode lengthening in rice by stimulating proliferation of new cells at the nodes.

(c)  Metabolic adaptations

Plant adaptation to O2-deficient environments involves the anatomical and morphological changes outlined above which allow ventilation of submerged parts. However, metabolic responses to anoxia are essential if particular cells like root apices are to survive. Mutants and transgenic plants and mol-ecular approaches such as promoter analysis open exciting possibilities for understanding the full interaction of plant response to inundation.

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Table 18.3

Drew at Texas A&M University, USA, and Greenway at the University of Western Australia demonstrated that root tissues become much more tolerant to anoxia if pretreated with intermediate O2 concentrations (hypoxic pretreatment) (Table 18.3). Apparently, metabolic adaptations set in train by hypoxia confer tolerance to anoxia. The first of these metabolic adaptations to be considered should be changes to the overall protein complement.

During anoxia, normal protein synthesis is replaced by the selective transcription and translation of a set of proteins called ‘anaerobic’ proteins. In maize roots, there are 20–22 of these proteins which include fermentative enzymes (e.g. PDC and ADH), enzymes involved in anaerobic carbohydrate catabolism (e.g. sucrose synthase and enzymes responsible for the reversible breakdown of sucrose) and several glycolytic enzymes (e.g. aldolase). This, together with the observation that exogenous sugars prolong tissue survival during anoxia, points to carbohydrate catabolism as a factor in tolerance to anoxia. Other ‘anaerobic’ proteins of maize include superoxide dismutase, responsible for scavenging O2-free radicals, and the O2-binding protein haemoglobin. ‘Anaerobic’ proteins are also formed in rice embryos, presumably associated with maintenance and growth of embryos during anoxia — one such enzyme is the tonoplast-located H+-pyrophosphatase (Carystinos et al. 1995). By maintaining an energised tonoplast capable of ion transport, this enzyme might help stabilise cytoplasmic pH. Reliance on pyrophosphate as an energy source reduces direct dependence of tonoplast ion transport on ATP regeneration. Induction of ‘anaerobic’ proteins could be promoted at the transcriptional level by a decrease in high-energy compounds such as ATP, cytoplasmic pH or O2 concentration.

The key to anoxia tolerance lies in integration of energy production via anaerobic carbohydrate catabolism and energy consumption in reactions essential for survival. Accumulating evidence suggests two modes of tolerance based on slow and rapid rates of fermentation. Lettuce seeds appear to survive anoxia by slowing anaerobic carbohydrate catabolism to less than 35% of the rate in air. After 14 d without O2, lettuce seeds germinate normally (Raymond and Pradet 1980).

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Table 18.4

By contrast, fermentation accelerates in tissues which grow rather than just survive in anoxia, for example coleoptiles of rice. Faster fermentation is sustained by accelerated glycolysis after exposure to anoxia by a phenomenon known as the Pasteur Effect. However, even in rice, glycolytic rate is only about twice as fast in anoxia as in air (Table 18.4). Two lines of evidence support the view that rapid fermentation ameliorates the energy deficit caused by anoxia. First, roots of maize and wheat survive anoxia more than three times longer if exposed first to hypoxia rather than an aerated solution (Table 18.3). Hypoxic pretreatment raised activities of the fermentative enzymes PDC and ADH, and resulted in a faster rate of alcoholic fermentation on transfer to anoxia. Second, in maize mutants deficient for the gene encoding ADH-1 (an isoform of ADH), the rate of alcoholic fermentation following hypoxic pretreatment was 30–35% slower than in the wild type. Only 70% of these mutant plants survived 24 h of anoxia whereas all wild-type plants survived 48 h of anoxia (Drew et al. 1994). Fermentative capacity was vital to survival. Root tips of mutant plants were almost all killed when anoxia was imposed abruptly (Table 18.3).

Other plant tissues which survive but do not grow in anoxia produce an initial burst of fermentative activity over 6–24 h before settling to much slower fermentation rates. This two-phase pattern of adaptation provides adequate ATP as tissues adapt to anoxia then conservation of carbohydrates for long-term survival. Slices of beetroot, a familiar storage organ, survive for 5 d in anoxia if they are pretreated with hypoxia. Glycolytic rate falls steadily in anoxia, reaching 70% of the rate in aerobic tissue after 24 h despite an adequate supply of carbohydrates and sufficient activity of the critical enzyme, PDC (Zhang and Greenway 1994). To be of adaptive value, this conservation of substrates through slower catabolism must be compatible with the smaller ATP yield available for cell maintenance. Calculations show that non-growing beetroot tissue in anoxia used 10- to 25-fold less ATP for cell maintenance than aerobic tissues.

While energy generation is important, a rapid rate of fermentation does not always endow anoxia tolerance. Pea root tips, for example, ferment 45% faster than maize tips but survive less than half as long in anoxia. Subtle aspects of energy consumption are thought to be involved in anoxia tolerance such as a reduction of energy requirements for cell maintenance and the redirection of energy flow to essential cellular processes, including maintenance of membrane integrity, regulation of cytoplasmic pH and synthesis of appropriate ‘anaerobic’ proteins.

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