Physiological and molecular basis of susceptibility and tolerance of rice plants to complete submergence

Abstract

Rice plants are much damaged by several days of total submergence. The effect can be a serious problem for rice farmers in the rainfed lowlands of Asia, and runs contrary to a widespread belief amongst plant biologists that rice is highly tolerant of submergence. This article assesses the characteristics of the underwater environment that may damage rice plants, examines various physiological mechanisms of injury, and reviews recent progress achieved using linkage mapping to locate quantitative traits loci (QTL) for tolerance inherited from a submergence-tolerant cultivar FR13A. Progress towards identifying the gene(s) involved through physical mapping of a dominant tolerance locus on chromosome 9 is also summarized. Available physiological evidence points away from responses to oxygen shortage as being inextricably involved in submergence injury. An imbalance between production and consumption of assimilates is seen as being especially harmful, and is exacerbated by strongly accelerated leaf extension and leaf senescence that are ethylene-mediated and largely absent from FR13A and related cultivars. DNA markers for a major QTL for tolerance are shown to be potentially useful in breeding programmes designed to improve submergence tolerance.

Fig. 1. Effect of complete submergence for 10 d on the appearance of initially 3‐week‐old rice plants. Different rice lines are in double rows running from top to bottom of the picture. Rice lines on the right are intolerant to submergence and show evidence of leaf degeneration and collapse. The left‐hand rice line (cultivar FR13A) is relatively undamaged by 10 d of submergence. Picture taken 1 d after desub mergence by Dr Panatda Bhekasut (Prachinburi Rice Research Center, Department of Agriculture, Thailand).

Fig. 2. Influence of depth in the water on the percentage loss of incident light intensity at three field sites in eastern India. The inset values show the depth in metres at which light intensity would have been halved (taken from Ram et al., 1999).

Fig. 3. Effect of a 1‐d pre‐treatment with the growth‐inhibiting hormone abscisic acid (0, 10, 100 and 1000 mmol m^–3) applied through the roots of the submergence‐susceptible doubled haploid line 337. The number above each plant is a visual submergence tolerance score on a scale where 9 is dead and 1 is undamaged. Plants were submerged for 10 d at the three‐leaf stage at the time submergence began and photographed 7 d after desubmergence. Photograph by Dr J. E. Summers.

Fig. 4. Diagrammatic summary of several environmental components (in green) that may affect rice plants during complete submergence, and their likely physiological impact. The central assumption is that submerged plants are damaged by a shortage of energy. The relatively high tolerance shown by cultivars such as FR13A can be linked to: (1) a suppression of energy‐demanding processes such as underwater leaf extension, leaving a larger surplus for cell maintenance; and (2) retention of older leaves in a non‐senescent state. Note that: leaf elongation is promoted by ethylene but decreased by slow O₂ supply or accumulations of CO₂; leaf senescence is promoted by ethylene; evidence that submerged plants necessarily suffer severely from O₂ shortage is limited; and O₂ from daytime photosynthesis underwater or from the air at the time of desubmergence may cause oxidative damage.