18.1.1  Root-zone aeration

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Soil waterlogging arises from excessive rain or irrigation, poor internal drainage or impeded runoff. Two major problems for plant growth ensue. O2 becomes scarce around roots while other gases like CO2 build up, sometimes damaging plants. Through depletion of O2, which stimulates the activity of anaerobic microbes, soil redox potential becomes very low (below –200 mV) and toxic forms of microelements such as iron and manganese appear.

(a)  Chemistry of anaerobic soils


Table 18.1

When soil becomes waterlogged, air is displaced from soil pores by water and the chemistry of the soil alters radically. Gas exchange between soil and the atmosphere is inhibited because the diffusivity of gases in water is about 10 000 times slower than that in air. Consequently, O2 depleted by respirat-ory activity of soil organisms is not replaced, and eventually all but the top few millimetres of the soil becomes anaerobic. Mean-while, gases produced by the metabolic activity of these soil organisms accumulate, most notably CO2 and ethylene (Chapter 9). Bacteria adapted to these anaerobic conditions can proliferate, generating energy by catabolism of organic compounds and reducing electron acceptors other than O2, such as iron (Fe3+), manganese (Mn4+) and, under very reducing conditions, sulphate (SO42–). The reduced forms, Fe2+, Mn2+ and the gas hydrogen sulphide (H2S) are phytotoxic. Because Fe2+ and Mn2+ are particularly soluble they are taken up by plants in toxic amounts. Reduced forms of nitrogen also become dominant: denitrification of nitrate (NO3) to gaseous N2 occurs and ammonium (NH4+) often accumulates following mineralisation of organic nitrogen. After prolonged water-logging, the gas methane (CH4) is produced as a consequence of the reduction of organic compounds. Production of noxious gases is referred to in the opening quote where ‘foul damps’ were believed to render the air ‘unfit for respiration’. This sequence of events following flooding and the rates of change measured in two soil types differing in temperature and organic matter are illustrated in Table 18.1.

O2 is a fundamental requirement for root growth. Without O2, plant roots and aerobic microorganisms lose 85–95% of their capacity to produce energy and they stop growing. During temporary soil waterlogging, leaf and shoot extension of herbaceous and woody species often slows and older leaves become yellow, suggesting premature senescence. More prolonged waterlogging kills those plants which lack a genetic capacity to adapt to the changes in metabolism and external chemistry described.

(b)  Soil–root interface

Characteristic red-brown deposits are frequently observed on roots of flood-tolerant species such as rice when grown under waterlogged conditions. These deposits are precipitates of iron oxides (ferric form), and they occur as a consequence of O2 leaking from roots into the rhizosphere. The process, known as radial oxygen loss, is made possible through gas spaces that are continuous from shoots through roots: once O2 reaches the roots it leaks passively from intercellular gas spaces into the anaerobic root environment under its concentration gradient. This serves the important function of oxygenating the rhizo-sphere, thereby oxidising phytotoxic, reduced forms of microelements and allowing growth of aerobic microbes such as nitrifying and nitrogen-fixing bacteria. Oxygenation of the rhizosphere by radial O2 loss from roots of one species may benefit a second species growing in close proximity. For example, radial O2 loss from roots of kikuyu grass appears to enhance the survival of subterranean clovers during transient waterlogging of west Australian pastures. Radial O2 loss from roots has also been demonstrated in tree and herbaceous species by placing platinum O2 electrodes around roots or observing the reoxidation of reduced dyes.

Two principal factors control the rate of radial O2 loss. These are permeability to O2 of the outer cell layers of roots (exodermis and epidermis) and concentration gradient of O2 from internal gas spaces of roots to surrounding soil; the latter depends heavily on how much O2 is used in root and microbial respiration. Despite its benefits, loss of O2 from roots into soil restricts the amount of O2 that reaches the root apex via O2 transport from shoots (Section 18.1.2a). Excessive O2 leakage from basal root tissues leads to anoxia in apical regions of long roots. A balance must therefore be achieved between the competing demands of rhizosphere oxidation and root apex aeration.

(c)  Root respiration and anaerobic metabolism


Figure 18.1 Scheme denoting the important metabolic reactions during anaerobic carbohydrate catabolism. Anoxia prevents pyruvate from entering the TCA cycle because O2 is unavailable as a terminal electron acceptor. Carbon is diverted to fermentative end-products, allowing oxidation of NADH and sustained catabolism of carbohydrates. The enzyme that catalyses oxidation of NADH as oyvuvate is converted to alanine has not been identifed. Key enzymes are: 1. ATP-dependent phosphofructokinase; 2, Ppi-dependent phosphofructokinase; 3, lactate dehydrogenase; 4, pyruvate decarboxylase; 5, alcohol dehydrogenase; 6, glutamate-pyruvate transaminase; 7, pyruvate dehydrogenase. Note that some reactions are reversible (two-way arrows)

Roots growing in well-drained soils respire by catabolising carbohydrates in the tricarboxylic acid (TCA) cycle; energy in the form of ATP is generated, predominantly through oxidative phosphorylation in mitochondria (Section 2.4). However, in waterlogged soils O2 is scarce and as aerobic respiration becomes inhibited carbohydrates are broken down via fermentative pathways (Figure 18.1). This causes two problems in root tissues. First, anaerobic cells often generate insufficient energy, even for cell maintenance, because of the 85–95% decrease in energy production per hexose unit following engagement of fermentative pathways. Second, end-products of anaerobic carbo-hydrate catabolism are sometimes toxic if left to accumulate in plant cells. Fermentative pathways use their own inter-mediates as hydrogen acceptors; coupling of these reductive steps to oxidation of NADH to NAD+ is an essential feature of fermentation. Breakdown of carbohydrates to ethanol and CO2 is the principal fermentative pathway in plants. Some lactate and alanine are also produced but in contrast to fer-men-tation leading to lactate and alanine, alcoholic fermentation can be sustained over days in anoxic tissues, end-product toxicity being minimised by leakage of ethanol and CO2 to the root medium.


Figure 18.2 Curves showing pH optima of enzymes at the branch point for carbon flow to aerobic and anaerobic pathways. These in vitro determinations from extracts of rice coleoptiles indicate how cytoplasmic pH controls carbon flow. In aerobic coleoptiles, pyruvate dehydrogenase (PDH) catalyses entry of pyruvate to the TCA cycle when pH is above 7 whereas pyruvate decorboxylase (PDC) becomes engaged at pH below 7. Anoxia has two effects on metabolism. Cytoplasmic pH drops below 7, causing PDH activity to give way to PDC and fermentation to commence. In addition, PDC extracted from coleoptiles previously exposed to anoxia is in more active form, enhancing pyruvate consumption for ethanol production. (Based on Morrell et al. 1989)

Carbon flow from pyruvate to ethanol and CO2 occurs via the fermentative enzymes pyruvate decarboxylase (PDC) and alcohol dehydrogenase (ADH) (Figure 18.1). This flow is probably regulated by the activity of PDC which catalyses the first step of alcoholic fermentation. Increases in the amount of PDC and ADH through synthesis (transcriptional control) has been observed in a range of plant genotypes in response to O2 deficiency. Indeed, these enzymes form part of a suite of ‘anaerobic’ proteins, enzymes synthesised during anoxia (Section 18.1.2c). In addition to coarse control, the activity of PDC already present in a cell is regulated by fine control (post-translational regulation) exerted by subtle changes in cytoplasmic pH, which decreases from around 7.5 in aerated tissue to around 6.8–7.2 in anoxic tissue. Below pH 7.2, the activity of PDC reaches its optimum. For example, PDC extracted from anoxic rice coleoptiles becomes very active as pH drops below 7 according to the broad pH response curve in Figure 18.2. Following a return to aerobic conditions, cytoplasmic pH increases, the activity of PDC decreases and carbon flows via pyruvate dehydrogenase (PDH) to the TCA cycle. Energy yield increases by at least an order of magnitude. During anoxia, the rate of carbohydrate catabolism is regulated by activity of a few key enzymes. In wheat roots, PDC is likely to be the main rate-controlling enzyme because its in vitro activity closely approximates the measured in vivo rate of fermentation. In rice coleoptiles the glycolytic enzyme, ATP-dependent phosphofructokinase (PFK), might also contribute to control (Section 2.4.2), providing carbohydrate supply to glycolysis is adequate. Low light and deep submergence can conspire to reduce carbohydrate levels to a point where they limit the rate of anaerobic carbohydrate catabolism.

O2 is required in a number of metabolic processes in addition to aerobic breakdown of carbohydrates, for example in the synthesis of unsaturated fatty acids, which are essential components in the maintenance of membrane structure in plants. The enzymes involved in these O2-requiring processes generally have a higher Km for O2 than cytochrome oxidase so they are inhibited at higher O2 concentrations than that which inhibits carbohydrate catabolism. Metabolism of water-logged plants is therefore altered by inhibition of oxidative reactions not directly linked to energy production, as well as an energy shortfall caused by inhibition of oxidative phosphorylation.