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

Abstract

Gas exchange between the plant and the environment is severely hampered when plants are submerged, leading to oxygen and energy deficits. A straightforward way to reduce these shortages of oxygen and carbohydrates would be continued photosynthesis under water, but this possibility has received only little attention. Here, we combine several techniques to investigate the consequences of anatomical and biochemical responses of the terrestrial species Rumex palustris to submergence for different aspects of photosynthesis under water. The orientation of the chloroplasts in submergence-acclimated leaves was toward the epidermis instead of the intercellular spaces, indicating that underwater CO 2 diffuses through the cuticle and epidermis. Interestingly, both the cuticle thickness and the epidermal cell wall thickness were significantly reduced upon submergence, suggesting a considerable decrease in diffusion resistance. This decrease in diffusion resistance greatly facilitated underwater photosynthesis, as indicated by higher underwater photosynthesis rates in submergence-acclimated leaves at all CO 2 concentrations investigated. The increased availability of internal CO 2 in these ''aquatic'' leaves reduced photorespiration, and furthermore reduced excitation pressure of the electron transport system and, thus, the risk of photodamage. Acclimation to submergence also altered photosynthesis biochemistry as reduced Rubisco contents were observed in aquatic leaves, indicating a lower carboxylation capacity. Electron transport capacity was also reduced in these leaves but not as strongly as the reduction in Rubisco, indicating a substantial increase of the ratio between electron transport and carboxylation capacity upon submergence. This novel finding suggests that this ratio may be less conservative than previously thought.

Adaptation to water level variation: Responses of a floating-leaved macrophyteNymphoides peltatato terrestrial habitats

“…The present study also suggests that terrestrially grown plants have thinner lamina than aquatically grown plants. A possible explanation for this is that the thinner emerged leaves also have shortened diffusion pathways within it and thus result in increased gas exchanges (Mommer et al, 2005). An analogous type of morphogenetic plasticity could occur in root systems.…”

“…In many wetland and floodplain ecosystems, periodic flooding and drought occurrences play an important role in the composition, and productivity of species (Li et al, 2004;Leira and Cantonati, 2008). Wetland plants possess various characteristics in order to survive and function in fluctuating and frequently adverse conditions of wetland ecosystems (e.g., Shangguan et al, 2000;Sultan, 2001;Li et al, 2004;Mommer et al, 2005Mommer et al, , 2006. In response to changing water levels, many species of higher plants have developed an amphibious existence (Robe and Griffiths, 1998).…”

“…In response to changing water levels, many species of higher plants have developed an amphibious existence (Robe and Griffiths, 1998). Previous works on the adaptation of aquatic plants to water level fluctuations focused mainly on how plants adapt to submersed growth, including morphological and anatomical changes in leaf, root, and shoot (Navas and Garnier, 2002;Lynn and Waldren, 2003;Mommer et al, 2005), life history adaptations (Blom et al, 1994), shortterm metabolic adaptations (Pedersen and Sand-Jensen, 1997), and hormonal regulation of adaptive responses (Voesenek et al, 1993). However, only few studies have been carried out on adaptations that allow floating-leaved plants to withstand sudden emersion.…”

A Shoot-Specific Hypoxic Response of Arabidopsis Sheds Light on the Role of the Phosphate-Responsive Transcription Factor PHOSPHATE STARVATION RESPONSE1

“…The rate of photosynthesis under hypoxia and submergence strongly differs from the situation in aerated plants (Krause et al, 1985;Mommer et al, 2005;Mustroph et al, 2006b;Colmer et al, 2011). Already 2 h after the onset of hypoxic stress, the epoxidation status of xanthophylls dramatically declined, indicating strong perturbation of photosynthesis (Fig.…”

Photosynthetic response of the floating-leaved macrophyteNymphoides peltatato a temporary terrestrial habitat and its implications for ecological recovery of Lakeside zones

“…In the lakeside zone of shallow lakes, a variety of environmental factors interact to affect the productivity, distribution and species composition of aquatic macrophyte communities, among which are water depth, light, sediment composition (Barko et al, 1986) and anthropogenic disturbance (Nishihiro et al, 2006). Previous studies on the adaptation of aquatic plants to water level fluctuations in the lakeside zone have mainly focused on how these plants adapt to submersed growth, which includes leaf, root and shoot morphology, as well as anatomic changes (Robe et al, 1998;Lynn et al, 2003;Mommer et al, 2005). A few studies have been conducted regarding adaptations that allow floating-leaved or submersed plants to withstand terrestrial habitats due to water level decline and other environmental factors.…”