Submergence-Induced Morphological, Anatomical, and Biochemical Responses in a Terrestrial Species Affect Gas Diffusion Resistance and Photosynthetic Performance

Abstract

Complete submergence severely inhibits gas exchange between the plant and the environment because gas diffusion in water is approximately 10 ^{slower than in air. This can lead to oxygen deficiency in the plant and, concomitantly, energy deficits due to hampered aerobic metabolism (}Crawford and Brändle, 1996). Well-known adaptations of plants to submergence include elongation of shoot organs to restore contact with the atmosphere (Voesenek et al., 2004) and the ability to switch to anaerobic metabolism to generate ATP in the absence of O₂ (Perata and Alpi, 1993). Another, yet overlooked, phenomenon to reduce the shortages of oxygen and carbohydrates might be the potential for sustained photosynthesis under water (He et al., 1999; Vervuren et al., 1999).

The poor gas diffusion under water, however, severely limits inorganic carbon supply for photosynthesis. To reduce this limitation, specialized aquatic plant species have developed CO₂-concentrating mechanisms (Bowes et al., 2002), or can use HCO₃ ⁽Maberly and Madsen, 2002) or utilize sediment CO₂ (Pedersen et al., 1995) as a carbon source. In nonspecialized plants, however, underwater photosynthesis rates and affinity for CO₂ are expected to be low due to the high gas diffusion resistance of the leaves (Maberly and Madsen, 1998; Sand-Jensen and Frost-Christensen, 1999; Madsen and Maberly, 2003).

Recently, we observed that Rumex palustris plants submerged in water with ambient O₂ and CO₂ concentrations had subambient O₂ concentrations in their leaves in darkness. However, O₂ concentrations were much closer to ambient in leaves that were acclimated to submerged growth conditions (Mommer et al., 2004). This suggests increased diffusion of oxygen from the water column into the leaves and, thus, reduced gas diffusion resistance as result of acclimation to submergence. This finding therefore encouraged us to investigate the photosynthetic consequences of acclimation to submergence in this terrestrial species, which is a well-explored model species for terrestrial plant responses to submergence (Visser et al., 1996; Cox et al., 2003; Voesenek et al., 2003).

Photosynthetic acclimation to submergence has hardly been investigated in terrestrial species, but more is known from work on amphibious plant species. These plants grow in the transition from land to water and develop both specialized terrestrial and aquatic leaves. Sand-Jensen et al. (1992) and Frost-Christensen and Sand-Jensen (1995) showed that aquatic leaves of these species have increased underwater CO₂ assimilation rates compared to their terrestrial counterparts, as a result of the reduced gas diffusion resistance of the leaves. Frost-Christensen et al. (2003) also showed that this reduced gas diffusion resistance in aquatic leaves of amphibious plant species originates from reduced cuticle thickness and its reduced resistance for gases such as O₂. Photosynthesis rates may, however, not only be hampered by diffusional resistances (Long and Bernacchi, 2003) but also by biochemical limitations (Centritto et al., 2003). Reduced Rubisco activities have been observed in aquatic leaves of amphibious species relative to their terrestrial leaves, and the aquatic leaves therefore have a reduced carboxylation capacity (Farmer et al., 1986; Beer et al., 1991).

Here, we investigate if the terrestrial plant R. palustris shows responses to submergence that may be expected from the analogy with amphibious species, including reduced cuticle thickness in submergence-acclimated leaves and, consequently, higher underwater photosynthesis rates. Furthermore, we explore novel responses of photosynthesis in response to submergence. An aspect that has not received much attention in amphibious plants species is that under water the internal CO₂ concentration (C_i) is relatively low compared to internal O₂ concentration, which favors oxygenation reactions of Rubisco over carboxylation (Ogren, 1984). Underwater photosynthesis is therefore predicted to be characterized by high photorespiration rates (Lloyd et al., 1977; Salvucci and Bowes, 1982). Here, we report the first in vivo estimates of photorespiration rates in higher plants under water. This allows investigation of the effect of submergence acclimation on photorespiration, since decreased gas diffusion might alter the ratio between internal CO₂ and O₂ concentrations. Another consequence of an aquatic environment is the relatively low availability of electron sinks relative to photon absorption (MacKenzie et al., 2004), which may impose a large excitation pressure on the electron transport system (Niyogi, 2000). Increased C_i as a result of acclimation to submergence might lower the excitation pressure and thus reduce potential photoinhibition. Additionally, we investigate if, next to reduced diffusion resistance, submergence acclimation also involves changes at the biochemical level of photosynthesis. If acclimation to submergence in terrestrial species resembles differences between the leaf types of amphibious species (Beer et al., 1991), we would expect reduced amounts of Rubisco protein in submergence-acclimated leaves of R. palustris. As different processes of the photosynthetic machinery are highly coordinated and kinetic properties are tuned to each other (von Caemmerer, 2000), electron transport capacity was expected to show the same response to submergence as described for carboxylation capacity.

Acknowledgments

Notes

Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.105.064725.