Underwater photosynthesis in flooded terrestrial plants: a matter of leaf plasticity

Abstract

Background: Flooding causes substantial stress for terrestrial plants, particularly if the floodwater completely submerges the shoot. The main problems during submergence are shortage of oxygen due to the slow diffusion rates of gases in water, and depletion of carbohydrates, which is the substrate for respiration. These two factors together lead to loss of biomass and eventually death of the submerged plants. Although conditions under water are unfavourable with respect to light and carbon dioxide supply, photosynthesis may provide both oxygen and carbohydrates, resulting in continuation of aerobic respiration.

Scope: This review focuses on evidence in the literature that photosynthesis contributes to survival of terrestrial plants during complete submergence. Furthermore, we discuss relevant morphological and physiological responses of the shoot of terrestrial plant species that enable the positive effects of light on underwater plant performance.

Conclusions: Light increases the survival of terrestrial plants under water, indicating that photosynthesis commonly occurs under these submerged conditions. Such underwater photosynthesis increases both internal oxygen concentrations and carbohydrate contents, compared with plants submerged in the dark, and thereby alleviates the adverse effects of flooding. Additionally, several terrestrial species show high plasticity with respect to their leaf development. In a number of species, leaf morphology changes in response to submergence, probably to facilitate underwater gas exchange. Such increased gas exchange may result in higher assimilation rates, and lower carbon dioxide compensation points under water, which is particularly important at the low carbon dioxide concentrations observed in the field. As a result of higher internal carbon dioxide concentrations in submergence-acclimated plants, underwater photorespiration rates are expected to be lower than in non-acclimated plants. Furthermore, the regulatory mechanisms that induce the switch from terrestrial to submergence-acclimated leaves may be controlled by the same pathways as described for heterophyllous aquatic plants.

Fig. 1.

Internal oxygen concentrations in the petiole of a submerged Rumex palustris plant, in the dark (closed bar) and in the light (open bar). Oxygen concentrations were measured with a microelectrode inserted in the petiole in close proximity to the leaf lamina (cf. Mommer et al., 2004). Light conditions were saturating (450 µmol PAR m⁻² s⁻¹ at the leaf level), and external dissolved carbon dioxide concentration was low (8 µm), at a temperature of 20 °C.

Fig. 2.

Morphology of a control (left) and submerged (right) Rumex palustris plant. Submergence took place during 14 d in 0·7 m deep containers with circulating clear tap water, with light intensities of 100 µmol PAR m⁻² s⁻¹ at leaf level and a 16 h/8 h day/night cycle; temperature 20 °C. Plants were 52 d old. Scale bar = 50 mm.

Fig. 3.

Leaf longevity of submerged plants of three plant species contrasting in flooding tolerance. Species presented are (A) Daucus carota—flooding-intolerant; (B) Rumex palustris—flooding-tolerant; (C) Mentha aquatica—flooding-tolerant. New leaves present at the subsequent censuses (t = x days) are represented by different colours. Leaves present at the onset of submergence are indicated as t = 0. Conditions of submergence were similar to those given at Fig. 2, but with lower light conditions (30 µmol PAR m⁻² s⁻¹). Measurements were performed on ten plants per species. Standard errors were typically 5 % of the mean.