Flooding affects the abundance and distribution of plant species worldwide. Many plants are damaged or even killed by flooding events due to the associated oxygen deprivation in cells. Stimulated shoot elongation is an important adaptive mode that can restore contact of leaves with the atmosphere above the water surface. This strongly improves inward diffusion of oxygen and the rate of photosynthesis. Fast elongation of submerged petioles of the model plant Rumex palustris involves the integrated action of the plant hormones ethylene, auxin, gibberellin, and abscisic acid. The closely related Rumex acetosa is unable to switch on petiole elongation when submerged. In a comparative study of these two Rumex species, we found that the response to the gaseous phytohormone ethylene, which accumulates in plant tissues during submergence, explains their contrasting elongation behavior. In order to study the importance of this shoot elongation response in the distributional patterns of plants in natural floodplains, we quantified the ethylene‐induced elongation response of 22 plant species occurring in the Rhine River floodplain. These results were compared with the results of a multivariate analysis based on 84 vegetation surveys performed in the same area. The species compositions of the surveys were grouped along two environmental gradients: flooding duration and soil dehydration after the floodwater subsided. If we superimpose the ethylene‐induced elongation capacity on these vegetation data, it becomes clear that the capacity to elongate upon exposure to ethylene positively correlates with flooding duration and negatively with soil dehydration. Based on this analysis, we conclude that the capacity to elongate is an important selective trait in field distribution patterns of plants in flood‐prone environments. Fast shoot elongation under water seems to be a favorable trait only in environments with shallow and prolonged flooding events, while costs associated with this response prevent its expression in sites with deep floods, sites with floods short in duration, or in sites in which flood water recedes rapidly. The approach outlined in this paper may be more widely applicable in ecological studies that aim to understand the functional relationship between plant traits and species distributions along environmental gradients.
Abstract. The role of gibberellin (GA) and ethylene in submergence-induced petiole elongation was studied in two species of the genus R u m e x. Analysis of endogenous GAs in the flooding-tolerant R u m e x pa/ustris Sm. and the intolerant R u m e x acetosa L. by gas chromatographvmass spectrometry showed for both species the presence of GA], G A 4, G A 9, G A 19, G A 20 and G A 53. Gas chromatography-mass spectrometry analysis of R. palusiris petiole tissue of submerged plants showed an increase in levels of 13-OH GAs, especially G A h compared with drained plants. This effect could be mimicked by application of 5 f.tL L_l ethylene. In R. acetosa, no differences between levels of GAs in drained or submerged plants were found. In R. p a lu stris, both submergence and ethylene treatment sensitized petioles to exogenous gibberellic acid (GA3). In R. acetosa the effect was opposite, i.e. submergence and ethylene de-sensitized petioles to G A 3. Our results demonstrate the dual effect of ethylene in the submer gence response related to flooding tolerance, i.e. in the flooding-tolerant R. palustris ethylene causes an increased concentration of and sensitivity to GA with respect to petiole elongation while in the intolerant R. acetosa ethylene reduces growth independent of GAs.
The flooding resistance of four Ranunculus species was studied under controlled conditions and related to the tactics used by these species to survive in their natural habitat in river floodplains. R. bulbosus, a species from seldom-flooded river levées, was relatively intolerant of both waterlogging and complete submergence, due to a constitutively low level of aerenchyma in the root system. This lack of gas spaces resulted in high mortality rates during flooding treatments and an inability to use photosynthetically derived oxygen for root respiration during complete submergence. The pioneer R. sceleratus, predominantly abundant in low lying mudflats, was very resistant to waterlogging and shallow floods. Due to its constitutively high root porosity and its ability to greatly increase the elongation rate of petioles under water this species can ameliorate flooding stress. However, when leaf blades of R. sceleratus were unable to reach the water surface, this species died as quickly as the flooding-intolerant R. bulbosus. This indicates that fast elongation of petioles under water competes for energy and respirable reserves with maintenance processes. R. repens, a species from lower, frequently inundated floodplains, was very tolerant of prolonged waterlogging and submergence. Its high resistance to complete submergence under continuous darkness indicates that this species tolerates hypoxic and/or anoxic tissue conditions via metabolic adjustments. Lysigenous aerenchyma was also induced in the primary root system and in newly developed laterals, and it was able to use oxygen generated by underwater photosynthesis, for root respiration. R. acris, a species from less frequently flooded areas, was as resistant to waterlogging and submergence in the light as R. repens. However, it has a lower resistance than R. repens to complete submergence in the dark. A submergence pre-treatment increased the maximum net underwater photosynthetic rate in R. bulbosus, whereas a significant decrease of light compensation points was observed in R. repens when it had previously been submerged. This study shows that Ranunculus species exhibit various strategies to cope with different flooding conditions. R. repens responds to flooding by its tolerance mechanism and R. sceleratus by avoidance. R. acris ameliorates submergence and R. bulbosus was not able to adapt high water tables.
In a study on the mechanism of stimulated petiole elongation in submerged plants, oxygen concentrations in petioles of the flood-tolerant plant Rumex palustris were measured with micro-electrodes. Short-term submergence lowered petiole partial oxygen pressure to c. 19 kPa whereas prolonged submergence under continuous illumination depressed oxygen levels to c. 8-12 kPa after 24 h. Oxygen levels in petioles depended on the presence of the lamina, even in submerged conditions, and on available light. In darkness, petiole oxygen levels in submerged plants dropped quickly to values as low as 0.5-4 kPa. It is hypothesized that prolonged submergence in the light is accompanied by a decrease in carbon dioxide in the petiole. Submergence-enhanced petiolar elongation rate was compared with emergent plants. Peak daily elongation rates occurred at the end of the dark period in emergent plants, but in the middle of the light period in submerged plants. We suggest that this shift in daily elongation pattern is induced by dependence of growth on photosynthetically derived oxygen in submerged plants. Implications of reduced oxygen for ethylene production are raised. Levels of 1-aminocyclopropane-1-carboxylic acid synthase and 1-aminocyclopropane-1-carboxylic acid oxidase and ethylene sensitivity are cited as potential factors in hypoxia-induced ethylene release.
Abstract. The role of gibberellin (GA) and ethylene in submergence-induced petiole elongation was studied in two species of the genus R u m e x. Analysis of endogenous GAs in the flooding-tolerant R u m e x pa/ustris Sm. and the intolerant R u m e x acetosa L. by gas chromatographvmass spectrometry showed for both species the presence of GA], G A 4, G A 9, G A 19, G A 20 and G A 53. Gas chromatography-mass spectrometry analysis of R. palusiris petiole tissue of submerged plants showed an increase in levels of 13-OH GAs, especially G A h compared with drained plants. This effect could be mimicked by application of 5 f.tL L_l ethylene. In R. acetosa, no differences between levels of GAs in drained or submerged plants were found. In R. p a lu stris, both submergence and ethylene treatment sensitized petioles to exogenous gibberellic acid (GA3). In R. acetosa the effect was opposite, i.e. submergence and ethylene de-sensitized petioles to G A 3. Our results demonstrate the dual effect of ethylene in the submer gence response related to flooding tolerance, i.e. in the flooding-tolerant R. palustris ethylene causes an increased concentration of and sensitivity to GA with respect to petiole elongation while in the intolerant R. acetosa ethylene reduces growth independent of GAs.
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