JXB Advance Access originally published online on November 16, 2005
Journal of Experimental Botany 2006 57(2):283-290; doi:10.1093/jxb/erj015
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RESEARCH PAPER |
Photosynthetic consequences of phenotypic plasticity in response to submergence: Rumex palustris as a case study
1 Experimental Plant Ecology, Institute for Water and Wetland Research, Faculty of Science, Radboud University Nijmegen, Toernooiveld 1, 6525 ED Nijmegen, The Netherlands
2 Plant Ecophysiology, Utrecht University, Sorbonnelaan 16, 3584 CA Utrecht, The Netherlands
* To whom correspondence should be addressed. Fax: +31 24 3652409. E-mail: L.Mommer{at}science.ru.nl
Received 23 May 2005; Accepted 11 October 2005
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Abstract |
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 Top Abstract IntroductionPotential for underwater...Leaf morphology changes in...Acclimation to submergence...Acclimation to submergence...Quantification of diffusion...References |
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Survival and growth of terrestrial plants is negatively affected by complete submergence. This is mainly the result of hampered gas exchange between plants and their environment, since gas diffusion is severely reduced in water compared with air, resulting in O2 deficits which limit aerobic respiration. The continuation of photosynthesis could probably alleviate submergence-stress in terrestrial plants, but its potential under water will be limited as the availability of CO2 is hampered. Several submerged terrestrial plant species, however, express plastic responses of the shoot which may reduce gas diffusion resistance and enhance benefits from underwater photosynthesis. In particular, the plasticity of the flooding-tolerant terrestrial species Rumex palustris turned out to be remarkable, making it a model species suitable for the study of these responses. During submergence, the morphology and anatomy of newly developed leaves changed: ‘aquatic’ leaves were thinner and had thinner cuticles. As a consequence, internal O2 concentrations and underwater CO2 assimilation rates were higher at the prevailing low CO2 concentrations in water. Compared with heterophyllous amphibious plant species, underwater photosynthesis rates of terrestrial plants may be very limited, but the effects of underwater photosynthesis on underwater survival are impressive. A combination of recently published data allowed quantification of the magnitude of the acclimation response in this species. Gas diffusion resistance in terrestrial leaves underwater was about 15 000 times higher than in air. Strikingly, acclimation to submergence reduced this factor to 400, indicating that acclimated leaves of R. palustris had an approximately 40 times lower gas diffusion resistance than non-acclimated ones.
Key words: Acclimation, amphibious plants, diffusion resistance, heterophylly, photosynthetic plasticity, Rumex palustris, submergence, underwater photosynthesis
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Introduction |
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TopAbstractIntroductionPotential for underwater...Leaf morphology changes in...Acclimation to submergence...Acclimation to submergence...Quantification of diffusion...References |
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Flooding of river forelands can often be characterized as a highly dynamic, but unpredictable process (Vervuren et al., 2003
) that significantly affects plant species distribution (Silvertown et al., 1999; van Eck et al., 2004). Most flooding-sensitive species are restricted to high elevations of the floodplain where floods are rare, although a few occur at lower sites where they avoid flooding through life-history tactics and survive unfavourable conditions as dormant seeds or perennial organs (Menges and Waller, 1983; Van der Sman et al., 1993). The majority of species growing at low floodplain elevations, however, are tolerant to submergence (van Eck et al., 2004) and exhibit different suites of traits that are considered to reduce the negative effects of submergence (Armstrong et al., 1994; Vartapetian and Jackson, 1997).
The negative effects of complete submergence on plant growth and survival are mainly caused by the severely inhibited gas exchange between the plant and the environment because gas diffusion is severely limited under water compared with air (Armstrong, 1979). As a result of the limited gas exchange under water, oxygen concentrations within plants may decrease rapidly upon submergence (Stünzi and Kende, 1989; Rijnders et al., 2000). Due to oxygen deficiency aerobic respiration is inhibited (Armstrong and Gaynard, 1976) and, consequently, the carbohydrate and energy status—at least in the shoot—will drop to harmful levels for the plant (Setter et al., 1987; Ram et al., 2002).
A well-known trait of plants to avoid oxygen deficiency is elongation of the shoot (for review see Voesenek et al., 2004) leading to restoration of contact with the atmosphere, thereby restoring the gas exchange. Subsequently, gas diffusion within the plant is enhanced by increased development of longitudinal air channels (aerenchyma) in shoot and roots (Visser et al., 1996; Colmer, 2003) and by the induction of a gas-tight barrier in the roots to prevent oxygen loss into the anaerobic soil (Colmer et al., 1998; Visser et al., 2000).
However, flooding may often be too deep (e.g. >1 m) for a plant to reach the surface through shoot elongation. Reduced metabolic activity (Setter and Laureles, 1996) and generation of energy via anaerobic pathways (for review see Greenway and Gibbs, 2003) might then be a sufficient strategy for survival. A more preferable way to reduce the shortages of oxygen and carbohydrates under such conditions, however, would be the continuation of photosynthesis under water. As photosynthesis produces both oxygen and carbohydrates, it will alleviate considerably submergence stress in completely submerged plants.
Evidence suggesting that the availability of light is an important factor for survival of terrestrial plants during submergence has accumulated during recent years, implying an important role for photosynthesis under water (for review see Mommer and Visser, 2005). However, the severely limited gas diffusion in water also limits CO2 availability to the plant and thus the potential for underwater photosynthesis. This apparent contradiction between observation and prediction might be explained by the hypothesis that terrestrial plants are able to acclimate to the aquatic environment, thereby increasing their underwater gas exchange.
An overview is presented here of the degree of phenotypic plasticity that terrestrial plants express in the shoot in response to complete submergence, and its consequences for photosynthesis under water. The focus is specifically on the acclimation response of the shoot of the flooding-tolerant species Rumex palustris that has become a model species to investigate responses to submergence. This species shows an interestingly high plasticity in leaf morphology in response to submergence which appears to be functional for underwater photosynthesis (Fig. 1; Mommer et al., 2005b). Furthermore, this species develops aerenchymatous adventitious roots upon partial soil flooding (Visser et al., 1996) and enhanced petiole elongation during full submergence in order to restore contact with the atmosphere (Voesenek et al., 2004). These different ecophysiological traits allow R. palustris to grow and persist on frequently flooded mud flats (Blom et al., 1994) and poorly drained sites where floodwater tables remain high for a longer period of time (Voesenek et al., 2004). The strong acclimation response of the leaves of R. palustris to submergence has only recently been studied in detail and covers different aspects of morphology, anatomy, and photosynthesis (Mommer et al., 2004, 2005a, b; Fig. 2). A combination of the data from these recent publications allows quantification of the magnitude of the acclimation response, since an important functional aspect of the acclimation response can be expressed in terms of reduction of the gas diffusion resistance. This calculation is used as an example to show the importance of the development of acclimated leaves under water in a submerged terrestrial plant. These leaves have been shown to be crucial for plant performance under water (Fig. 2), and moreover, for the survival-enhancing effects of photosynthesis under submerged conditions (Mommer and Visser, 2005).
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Potential for underwater photosynthesis to alleviate submergence stress |
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TopAbstractIntroductionPotential for underwater...Leaf morphology changes in...Acclimation to submergence...Acclimation to submergence...Quantification of diffusion...References |
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Light availability under water may be relatively low, due to surface reflection and absorption by water, suspended particles, zooplankton, and algae (Holmes and Klein, 1987
). For example, light transmission levels have been shown to be below 1% at depths greater than 0.3 m during a flooding event with a sediment load of 150 mg l–1 in the River Rhine (Vervuren et al., 2003), leaving <20 µmol m–2 s–1 of photosynthetic active radiation (PAR) on an average sunny day. As a result, aquatic environments are generally described as shaded environments (Chambers and Kalff, 1987; Holmes and Klein, 1987; Sand-Jensen, 1989). This is especially true in waters with large amounts of algae which, next to severely reducing the light intensity also affect the light quality, thereby, for example, lowering the red:far-red ratio, which is a typical canopy shade signal (Monro and Poore, 2005). However, this spectral quality change may be restricted to algae-rich waters as red and far-red light are generally attenuated too quickly under water to serve as a shade signal (Smith, 1982). Furthermore, submergence of plants is certainly not always accompanied by low light intensities. In temporarily flooded oligotrophic limestone lakes (turloughs), floodwater may be exceptionally clear (S Waldren, personal communication), resulting in high light levels. Furthermore, in depressions in the floodplains of the River Rhine that contained persisting, shallow floodwater, where sediments have settled, light levels close to ambient have been observed (e.g. 600 µmol PAR m–2 s–1 at 0.3 m depth; Fig. 3). There may even be a risk of photodamage in these habitats, since the availability of electron sinks relative to photon absorption is low under water (MacKenzie et al., 2004).
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Apart from potential changes in the light climate when plants are submerged, the availability of inorganic carbon supply for photosynthesis will be severely limited due to slow diffusion rates of gases in water and the development of boundary layers (Bowes, 1987
; Madsen and Sand-Jensen, 1994). Many true aquatic plants have developed several carbon-concentrating mechanisms to overcome this carbon limitation (Prins and Elzenga, 1989; Keeley and Rundel, 2003), but these have not been observed yet in terrestrial plants. Underwater photosynthesis in terrestrial plants is characterized by extremely low photosynthesis rates immediately after submergence (He et al., 1999; Vervuren et al., 1999), and even strong acclimation responses will not lead to underwater photosynthesis rates comparable with these of true aquatic plants (Sand-Jensen and Krause-Jensen, 1997; Sand-Jensen and Frost-Christensen, 1999). It should, however, be noted that terrestrial plants do not generally grow and reproduce under water like aquatic species do, but rather need to survive the period of complete submergence. Not withstanding the low rates, both CO2 assimilation and O2 production seem important, since survival of terrestrial plants under water is much higher in the light than in the dark and also biomass loss during submergence is strongly reduced in the presence of light (Nabben et al., 1999; Mommer, 2005). |
Leaf morphology changes in response to submergence |
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TopAbstractIntroductionPotential for underwater...Leaf morphology changes in...Acclimation to submergence...Acclimation to submergence...Quantification of diffusion...References |
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Amphibious species, which grow in shallow water, develop both specialized terrestrial and aquatic leaves. Aquatic leaves of these species can sometimes be filamentous and dissected with few or no stomata, and differ strongly in morphology from their terrestrial leaves (Sculthorpe, 1967
). Clear examples of this phenomenon are shown by amphibious Ranunculus species, showing heterophylly in its most extreme form (Bruni et al., 1996). Some of these Ranunculus species, such as R. peltatus, even use 
as an additional carbon source (Nielsen and Sand-Jensen, 1993). Most aquatic leaves of amphibious plants, however, are simply more elongated and thinner and have a higher specific leaf area (SLA) than the terrestrial, emergent (Nielsen, 1993; Sand-Jensen and Frost-Christensen, 1999) or floating leaves (e.g. in the case of several Potamogeton species; Frost-Christensen and Sand-Jensen, 1995). The aquatic leaves of most of these heterophyllous species have reduced cuticle thickness and resistance compared with their terrestrial leaves (Frost-Christensen et al., 2003). Sometimes the chloroplasts of the aquatic leaves are located in the epidermal layer rather than in the mesophyll (Bruni et al., 1996), positioned as close to the entry of CO2 as possible.
Leaf morphology measurements on aquatic leaves of the terrestrial plant Rumex palustris showed that these were, to a large extent, comparable with those of amphibious species. Submergence-acclimated leaves which had developed during complete submergence (so called ‘aquatic’ leaves were elongated; Fig. 1), had a more than doubled SLA and a 20% decrease in leaf thickness (Mommer et al., 2005b). Aquatic leaves of other terrestrial species that had developed under water also had thinner leaves with a higher SLA (Mommer, 2005). Furthermore, chloroplasts were orientated towards the epidermis in the submergence-acclimated leaves of R. palustris, instead of being present adjacent to the intercellular gas spaces as in terrestrial leaves in air (Mommer et al., 2005b). This differential orientation of the chloroplasts under water keeps diffusion pathways short and thus gas diffusion resistance low.
Leaves of R. palustris did not develop gas envelopes when submerged, contrasting with observations in rice, where these gas films were suggested to function as ‘gills’ by increasing the gas exchange surface of the leaves and enabling convective gas flow (Raskin and Kende, 1983).
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Acclimation to submergence increases underwater photosynthesis |
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TopAbstractIntroductionPotential for underwater...Leaf morphology changes in...Acclimation to submergence...Acclimation to submergence...Quantification of diffusion...References |
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Evidence for an important functional aspect of the shoot response to submergence was achieved from oxygen micro-electrode studies on R. palustris (Mommer et al., 2004
). The internal oxygen pressures in leaves of plants submerged in air-saturated water were almost a factor of 2 higher in submergence-acclimated plants compared with non-acclimated plants in the dark, when only diffusion of oxygen from the water column into the plant takes place. In the presence of light (PAR = 450 µmol m–2 s–1), when photosynthesis occurs, internal oxygen pressures increased in both acclimated and non-acclimated plants, but still remained 20% higher in the acclimated plants, which is attributed to a reduction in the diffusion resistance for gas exchange between water and the acclimated leaves (Mommer et al., 2004).
Underwater photosynthesis measurements revealed more evidence for such a decreased gas diffusion resistance resulting from acclimation to submergence. Maximum underwater CO2 assimilation rates at high CO2 concentrations (>1000 µM) were 80% higher in submergence-acclimated leaves in R. palustris (Mommer et al., 2005b). Such benefits from acclimation have been found before in other submergence-tolerant terrestrial species, including Rumex crispus, Phalaris arundinacea (Vervuren et al., 1999), Ranunculus repens (He et al., 1999), and Veronica anagallis-aquatica (Boeger and Poulson, 2003). Decreased gas diffusion resistance also resulted in increased underwater photosynthetic performance at ecologically relevant CO2 concentrations (15–90 µM; van den Brink et al., 1993).
The photosynthetic consequences of acclimation to submergence as expressed by these terrestrial species are comparable with the responses observed in amphibious species. Aquatic leaves of these species also have increased underwater CO2 assimilation rates (Sand-Jensen et al., 1992; Frost-Christensen and Sand-Jensen, 1995) and higher CO2 affinity (Sand-Jensen and Frost-Christensen, 1999) compared with their terrestrial counterparts.
The reduction in gas diffusion resistance had a profound depressing effect on photorespiration rates in submergence-acclimated R. palustris plants (Mommer et al., 2005b), which is favourable for plant performance, as photorespiration is potentially damaging at high rates, and reduced photorespiration also limits the associated carbon losses (Keys, 1999). Furthermore, the excitation pressure on the photosynthetic machinery was lower in acclimated leaves, because the ratio between the availability of electron acceptors (mainly CO2 and O2) and the absorbed photons had increased due to the reduced diffusion resistance (Mommer et al., 2005b). The photosynthetic machinery itself was also affected, as a higher investment in electron transport capacity relative to carboxylation capacity was observed in acclimated leaves compared with non-acclimated leaves (Mommer et al., 2005b). It is not known yet if this novel phenomenon has functional significance for submerged plants, but it might further prevent photodamage of the photosystems.
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Acclimation to submergence increases performance even at low light intensity |
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TopAbstractIntroductionPotential for underwater...Leaf morphology changes in...Acclimation to submergence...Acclimation to submergence...Quantification of diffusion...References |
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Relative investment in light-harvesting capacity, indicated by the reduced chlorophyll a/b ratio increased in R. palustris under water (Mommer et al., 2005a
). This change in submerged plants mimics classic shade acclimation, even though control and submergence treatments did not differ in light intensity in this experiment. A shift in the chlorophyll a/b ratio in response to submergence was also observed in the related, but flooding-intolerant species, R. thyrsiflorus (Mommer et al., 2005a), and the two grass species Phalaris arundinacea and Arrhenatherum elatius (Vervuren et al., 1999), but not in Ranunculus repens (Lynn and Waldren, 2002). It is tempting to interpret submergence responses as responses to shade, i.e. low light conditions, as both stimuli induce similar responses in SLA, chlorophyll parameters, and light compensation points (Mommer et al., 2005a). However, underwater photosynthesis measurements clearly showed a functional difference between plants acclimated to either shade or submergence, as gas diffusion resistances were much more reduced in the submerged plants than in shade plants. Interestingly, no additional acclimation to low light conditions could be observed when terrestrial plants were shaded under water (Vervuren et al., 1999; Mommer et al., 2005a), contrasting with the responses of true submerged aquatic macrophytes (Goldsborough and Kemp, 1988; Wolff and Senger, 1991; Pilon and Santamaria, 2002).
The observation that light compensation points of R. palustris decreased under water, from 14 to 4 µmol photons m–2 s–1 (Mommer et al., 2005a) indicates that lower assimilation rates and thus lower light intensities were sufficient to compensate respiratory demand. The reduction in the light compensation point might be the result of increased underwater assimilation rates and decreased photorespiratory losses, both resulting from decreased gas diffusion resistance (Mommer et al., 2005b) and reduced dark respiration rate (Mommer et al., 2005a). Decreased light compensation points in the aquatic leaves compared with the terrestrial ones are also observed in heterophyllous aquatic species (reviewed in Maberly and Spence, 1989). Summarizing the data above, it is concluded that acclimation to submergence leads to more efficient use of the low light intensities that might occur during submergence events.
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Quantification of diffusion resistance in both leaf types of R. palustris |
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TopAbstractIntroductionPotential for underwater...Leaf morphology changes in...Acclimation to submergence...Acclimation to submergence...Quantification of diffusion...References |
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It has been shown above that the submerged leaf morphology of R. palustris facilitates gas exchange under water, which has implications for underwater performance in the presence of light (Fig. 2). All experimental data point to a decreased gas diffusion resistance to the exchange of gases between leaf and floodwater, but the magnitude of this decrease remained to be quantified. Here, the magnitude of the effect of acclimation on gas diffusion resistance is calculated in the flooding-tolerant species R. palustris, combining several well-accepted photosynthesis equations, which have, as far as is known, not been used earlier to determine the diffusion resistance of leaves under water. The experimental data needed for this calculation were obtained from the oxygen micro-electrode experiments of Mommer et al. (2004)
and gas exchange measurements in both air and water as described in Mommer et al. (2005b), but see the footnote to Table 1 for a short explanation of the experimental conditions.
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Explanation of calculations for total leaf resistance
Gas diffusion resistance for the total leaf is the inverse of total leaf conductance (gleaf). Total leaf conductance of CO2 is, in its turn, proportionally related to the rate of assimilation and is expressed, according to Fick's law (Harley et al., 1992
; Long and Bernacchi, 2003) as:
 | (1) |
653 Pa); Table 1], and Cc the internal CO2 pressure at the site of the chloroplasts. The internal CO2 concentration at the site of the chloroplast (Cc) was calculated for both leaf types from the model of von Caemmerer (2000):
 | (2) |
*) were estimated to be 4.05 Pa in ambient air (21 kPa O2, 20 °C; von Caemmerer et al., 1994). Estimates of * under water are based on both this reported value and the oxygen micro-electrode measurements in the petiole (Mommer et al., 2004), since the CO2 compensation point is proportional to the internal oxygen concentration, due to competition for binding sites at the Rubisco enzyme between O2 and CO2. Since submergence-acclimated leaves have higher internal O2 pressures than non-acclimated leaves, they also have higher CO2 compensation points (Table 1).
Interpretation of results
In air, CO2 enters the leaf via the stomata, diffuses through the stomata into intercellular spaces and finally reaches the chloroplasts. Calculation of the total leaf resistance (1/gleaf) is, therefore, the combined result of diffusional resistances over the boundary layer, stomata, and mesophyll (Harley et al., 1992; Long and Bernacchi, 2003). An additional resistance under water is the cuticle resistance (Mommer et al., 2005b), as CO2 has to cross the cuticle and epidermis cells to reach the chloroplasts in the palisade parenchyma and the mesophyll (Frost-Christensen et al., 2003).
The calculations of total leaf resistance, based on measurements of terrestrial R. palustris leaves show that the diffusion path under water has a 15000 times higher resistance to CO2 than when these leaves were in air (Table 1), illustrating the tremendous difficulties for underwater gas exchange in terrestrial plants.
Acclimation of R. palustris to submergence leads to a 38-fold decrease in diffusion resistance to CO2 under water, as represented by the ratio between the terrestrial and aquatic leaves under water (Table 1). As a result, the 15000 times higher diffusion resistance under water than in air in non-acclimated plants is reduced by a factor of 400 in submergence-acclimated leaves. Thus, acclimation to submergence strongly increases underwater gas exchange in R. palustris, and its consequences have been shown in Mommer et al. (2005b).
In air, terrestrial leaves have a 25 times lower diffusion resistance than aquatic leaves, which is probably due to increased stomatal resistance in the aquatic leaves in response to de-submergence.
These calculations show that the enhanced gas exchange upon acclimation to submergence is a clear example of adaptive phenotypic plasticity, as the phenotypic response is beneficial in one environment (under water), but disadvantageous in the other (air; Dudley and Schmitt, 1996). This had been recognized previously for heterophylly in aquatic species (Winn, 1999; Wells and Pigliucci, 2000), and can now be extended to submergence acclimation of at least one terrestrial species, R. palustris, but probably also to others. Compared with true aquatic species, R. palustris was still a relatively poor performer under water with respect to photosynthesis but, clearly, acclimation improved its gas exchange to such levels that survival is significantly prolonged. Also other terrestrial plant species, even when rather intolerant to submergence, appear to show prolonged survival when flooded in the light (Mommer, 2005) and it remains to be proven if similar morphological and anatomical acclimation occurs in these species as well.
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Acknowledgements |
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The authors are grateful Hans de Kroon (Radboud University, Nijmegen, The Netherlands), Danny Tholen and Ronald Pierik (both Utrecht University, The Netherlands) for interesting discussions and/or useful suggestions on an earlier draft of this manuscript. Comments by Steve Waldren (Trinity College, Ireland) and an anonymous referee improved the manuscript further.
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TopAbstractIntroductionPotential for underwater...Leaf morphology changes in...Acclimation to submergence...Acclimation to submergence...Quantification of diffusion...References |
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