Elsevier

Aquatic Botany

Volume 89, Issue 1, July 2008, Pages 50-56
Aquatic Botany

Effect of leaf age on CAM activity in Littorella uniflora

https://doi.org/10.1016/j.aquabot.2008.02.005Get rights and content

Abstract

In this study the effect of ontogenetic drift on crassulacean acid metabolism (CAM) was investigated in the aquatic CAM-isoetid Littorella uniflora. The results of this study strengthen the general hypothesis of CAM being a carbon-conserving mechanism in aquatic plants, because high-CAM capacity (45–183 μequiv. g−1 FW) was present in all leaves of L. uniflora irrespective of age. Since possession of CAM in aquatic plants allows CO2 uptake throughout the light/dark cycle, presence of CAM in all leaves influences the carbon balance of L. uniflora positively. On average for all lakes, different leaf classes accounted for 11–36% of the total dark CO2 uptake by the individual plant.

The capacity for both CAM and photosynthesis declined with increasing leaf age, and was in the oldest leaves only 25–53% of the capacity in the youngest. The photosynthetic capacity was estimated to be sufficiently high to ensure refixation of the CO2 released from malate during decarboxylation in the daytime. In line with this, a linear coupling between CAM capacity and photosynthetic capacity was found. Parallel to the change in photosynthetic capacity, an age-related change in total ribulose-bisphosphate carboxylase/oxygenase (rubisco) activity from 732 μmol C g−1 DW h−1 in the youngest leaves to 346 μmol C g−1 DW h−1 in the oldest was observed. In contrast, no significant change in phosphoenolpyruvate carboxylase (PEPcase) activity with leaf age was observed (means ranged between 46 and 156 μmol C g−1 DW h−1).

Introduction

Aquatic isoetids are characteristic for oligotrophic softwater lakes with a low concentration of dissolved inorganic carbon (Keeley, 1991, Madsen et al., 2002). The isoetids have developed several characteristics, which are considered as traits directed towards the low nutrient and inorganic carbon availability in their habitat, such as a high root:shoot ratio (0.5–3.5 on dry weight basis), a long leaf lifetime (200–700 days), presence of mycorrhiza, use of sediment-CO2 and possession of crassulacean acid metabolism (CAM) (Keeley, 1998, Madsen et al., 2002).

Most inorganic carbon assimilated by isoetids originates from the sediment interstitial water, where the CO2 concentration is several times higher than in the bulk water (Raven et al., 1988, Sand-Jensen and Søndergaard, 1997). Access to the sediment-CO2 pool is made possible by a large root system and a nearly continuous air lacunae system in roots and leaves, where diffusion of CO2 and other gasses take place (Keeley, 1996, Keeley, 1998, Madsen et al., 2002). The possession of CAM in some of the isoetids – e.g. Littorella uniflora and Isoetes lacustris – is another adaptation that may alleviate the inorganic carbon shortage in softwater lakes (Keeley, 1998, Madsen et al., 2002). CAM enables the isoetids to take up CO2 at night, fix it via phosphoenolpyruvate carboxylase (PEPcase) and store it as malic acid in the large vacuoles, which are characteristic for CAM plants (Hostrup and Wiegleb, 1991a, Winter and Smith, 1996). In the daytime malate is decarboxylated and the released CO2 enters the C-3 cycle via fixation by ribulose-bisphosphate carboxylase/oxygenase (rubisco). Opposed to many terrestrial CAM plants the daytime uptake of exogenous CO2 is not suppressed during malate decarboxylation, allowing the isoetids to assimilate exogenous CO2 24 h a day (Winter and Smith, 1996, Maden, 1985). For plants grown under laboratory conditions the contribution to the carbon budget of inorganic carbon uptake by CAM may be as high as 95% (Madsen, 1987a), and CAM is therefore expected to be of high importance for the carbon balance in the isoetids.

In addition to increased carbon conservation, CAM may, by increasing the internal CO2 concentration in lacunae and cells during malate decarboxylation, have physiological impact on the plants resembling the effects of carbon concentrating mechanisms operating in other aquatic macrophytes (Bowes and Salvucci, 1989, Maberly and Madsen, 2002). Since decarboxylation does not confer an additional resistance to diffusion of gasses, the higher internal CO2 concentrations may inhibit or reduce the competitive effect of oxygen on CO2 fixation and may reduce the inorganic carbon loss through photorespiration (Bowes, 1991). As a result of higher internal CO2 concentration the efficiency of rubisco is enhanced, which may diminish the need for rubisco and hence nitrogen (Ehleringer and Monson, 1993, Lüttge, 2002). For L. uniflora however, no coupling between CAM and photosynthetic nitrogen use efficiency has been found (Baatrup-Pedersen and Madsen, 1999). A reason could be that the nitrogen supply is not a limiting resource for growth for these plants (Christiansen et al., 1985).

The expression of CAM in both terrestrial and aquatic isoetids is affected by a range of environmental parameters, e.g. irradiance, water cover, nutrient availability and CO2 availability (Aulio, 1985, Madsen, 1987b, Hostrup and Wiegleb, 1991b, Robe and Griffith, 1990). The activity of CAM may also be dependent on leaf age and in many terrestrial species CAM is expressed fully in mature leaves only (Ting et al., 1996, Wen et al., 1997, Taybi et al., 2002). Whether comparable ontogenetic drift occurs in aquatic CAM plants is not known. However, a high extent of CAM in young leaves of CAM-isoetids would influence the carbon budget of the plants positively.

The aim of this study was to test whether CAM activity is dependent on leaf age in L. uniflora, and thus address the importance of ontogenetic drift for the efficiency of CAM as a carbon-conserving strategy in aquatic CAM species. To ensure generality correlation between leaf age and CAM was tested for three spatially separated populations of L. uniflora.

Section snippets

Plant material

Littorella uniflora (L.) Aschers was collected in three Danish softwater lakes, Lake Almind (56° 9′03N, 9° 32′30E), Lake Hampen (56° 1′05N, 9° 23′27E) and Lake Kalgaard (56° 0′47N, 9° 27′10E). The alkalinity of the lakes vary from 0.1 to 0.6 equiv. m−3 and the pH from 6.8 to 7.6. The total nitrogen and phosphorous concentrations in the lakes are similar and around 0.4 g m−3 and 15 mg m−3 for TN and TP. After collection the plants were brought from the three lakes to the laboratory and carefully

Results

The leaves tested in this study all had a capacity for CAM irrespectively of age (45–183 μequiv. g−1 FW) (Fig. 1), although the capacity was higher for young than for older leaves (ANOVA, P < 0.05) (Fig. 1). For plants collected in Lake Almind the capacity declined by 75% with increasing leaf age (P < 0.01, r2 = 0.83), which was significantly more than observed for plants from Lake Hampen and Lake Kalgaard, where CAM capacity declined by 67 and 47% (P < 0.01, r2 = 0.79 and 0.68, respectively).

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Discussion

CAM in aquatic macrophytes is considered to be a carbon-conserving mechanism that enhances the net inorganic carbon uptake of the plant; a hypothesis that is supported by our finding of a capacity for CAM in all leaves irrespectively of age in L. uniflora. Presence of CAM in all leaves has positive effects on the contribution of CAM to the carbon balance of the plants by allowing CO2 assimilation throughout the light/dark cycle for all leaves. Furthermore, the fact that all leaves possess CAM

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