Physiological Mechanisms of Flooding Tolerance in Rice: Transient Complete Submergence and Prolonged Standing Water

Abstract

Partial or complete submergence of shoots of rice (Oryza sativa L.) poses a dual challenge: the roots have to function in anoxic soil and gas exchange between shoots and air becomes restricted to a small aerial portion or is abolished during complete submergence. Adaptation of roots to anoxic and chemically reduced waterlogged soils was reviewed by Kirk et al. (Prog Bot, 2014). With deeper floods the O₂ provision to the roots may decline, because there is a high resistance for gas exchange between floodwater and the submerged part of the foliage. Floodwaters differ greatly in light levels and CO₂ concentrations, thus restricting underwater photosynthesis by varying degrees. During the day, underwater photosynthesis largely determines the O₂ concentrations within submerged rice, whereas, at night, tissue O₂ declines, particularly so in roots. Deepwater rice establishes a ‘snorkel’ via elongation of aerenchymatous internodes and leaf sheaths; these responses are triggered by ethylene, which acts on two Snorkel genes encoding ethylene-responsive factor (ERF) transcriptional regulators to elicit the action of gibberellin. In addition, aquatic roots emerge from stem nodes. Perversely, pronounced shoot elongation can be catastrophic for lowland rice completely submerged during transient floods. In these circumstances tolerance is underpinned by suppression of elongation by SUB1A-1, an ERF transcriptional regulator that blocks ethylene responsiveness. However, many aspects of survival during transient complete submergence remain unclear, such as the role of carbohydrate depletion, photosynthesis under water, and anoxia tolerance in roots. After desubmergence, possible injury to shoots from water deficits and free radicals also requires further elucidation. This review is focused on the evaluation of the physiological mechanisms involved in the acclimation–adaptation of rice to these floods.

‘Reductionism works in research provided there is a dynamic interchange between different levels of complexity as knowledge develops’ (paraphrased from Crick 1994)

Appendix: Does Appreciable O2 Deficiency Occur in Submerged Rice in Flooded Fields?

Jackson and Ram (2003) concluded that anoxia is of minor importance during complete submergence of rice, while we suggest that its contribution to the syndrome, though still far from clear, may be quite substantial. The extent and thus possible importance of anoxia would depend on environmental factors which will affect photosynthesis and hence O₂ provision, being irradiance, CO₂ concentrations, and turbulence. Hence, a detailed consideration of some of Jackson and Ram’s arguments is appropriate. This discussion also will highlight some of the difficulties in interpretation of experiments on this complex phenomenon.

The first argument was that when rice plants in soil were placed in the dark, they survived submergence at 0.05 mM O₂ for 7 days (Ellis and Setter 1999, criterion: some growth at 7 days after desubmergence), an O₂ concentration considered lower than usually encountered in the field (Jackson and Ram 2003). However, a study of the floodwaters in Indian fields showed that two out of six profiles had 0.092 mM or less O₂ at the water surface and 0–0.02 mM at the soil surface (Ram et al. 1999), indicating the likelihood of much more serious deficiencies of O₂ in the field than in the hypoxic solutions of Ellis and Setter (1999), particularly since Ellis and Setter used gas flushed solutions, rather than the usually less turbulent solutions encountered in the field.

The second set of experiments to be evaluated was with rice seedlings (Boamfa et al. 2005). There were some anoxic exposures, but also submergence in water with some O₂ available. Absence or presence of ethanol and acetaldehyde emissions was taken to indicate whether there had been anoxia during submergence. However this criterion is far from ideal. Firstly, if there is little emission of these products of anaerobic catabolism, during submergence under O₂ deficits rather than anoxia, the rate of evolution of formed ethanol and acetaldehyde may be severely underestimated when parts of the tissues receive sufficient O₂ for oxidative phosphorylation and therefore could consume the acetaldehyde and ethanol produced by the anoxic regions. Secondly, evolutions of acetaldehyde and ethanol after desubmergence, which were substantial over 6 h re-aeration after treatments longer than 18 h, may not be indicative of the rate of anaerobic catabolism during anoxia, but rather to inhibition of mitochondria due to injury incurred during the submergence, or desubmergence (cf. Gibbs and Greenway 2003).

The third line of evidence quoted by Jackson and Ram (2003) comes from an experiment with shoots of submerged rice, which were at high irradiance during the 12 h light cycle (Waters et al. 1989). In that experiment, cessation of root elongation during the night was rapidly reversed as soon as light was again available (Waters et al. 1989). However, these experiments were in clear water with high irradiance not only through the water surface but also from the sides of a 70-cm-long transparent cylinder surrounding the leaves, while nutrient agar around the roots did not provide the usual sink for O₂ encountered in soils.

In conclusion, severe O₂ deficits cannot be excluded particularly in the root tips of submerged rice in the field (see also Winkel et al. 2013).