How plants cope with complete submergence

Flooding is a widespread phenomenon that drastically reduces the growth and survival of terrestrial plants. The dramatic decrease of gas diffusion in water compared with in air is a major problem for terrestrial plants and limits the entry of CO(2) for photosynthesis and of O(2) for respiration. Responses to avoid the adverse effects of submergence are the central theme in this review. These include underwater photosynthesis, aerenchyma formation and enhanced shoot elongation. Aerenchyma facilitates gas diffusion inside plants so that shoot-derived O(2) can diffuse to O(2)-deprived plant parts, such as the roots. The underwater gas-exchange capacity of leaves can be greatly enhanced by a thinner cuticle, reorientation of the chloroplasts towards the epidermis and increased specific leaf area (i.e. thinner leaves). At the same time, plants can outgrow the water through increased shoot elongation, which in some species is preceded by an adjustment of leaf angle to a more vertical position. The molecular regulatory networks involved in these responses, including the putative signals to sense submergence, are discussed and suggestions made on how to unravel the mechanistic basis of the induced expression of various adaptations that alleviate O(2) shortage underwater.     

Submergence-induced morphological, anatomical, and biochemical responses in a terrestrial species affect gas diffusion resistance and photosynthetic performance

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.     

A functional comparison of acclimation to shade and submergence in two terrestrial plant species

Terrestrial plants experience multiple stresses when they are submerged, caused both by oxygen deficiency due to reduced gas diffusion in water, and by shade due to high turbidity of the floodwater. It has been suggested that responses to submergence are de facto responses to low light intensity. We investigated the extent to which submergence and shade induce similar acclimation responses by comparing two terrestrial Rumex species that differ in their responses to flooding. Our study confirms that there are strong similarities between acclimation responses to shade and submergence. Petiole length, specific leaf area (SLA), chlorophyll parameters and underwater light-compensation points changed at least qualitatively in the same direction. Maximum underwater photosynthesis rate, however, did discriminate between the functionality of the responses, as the acclimation to submergence appeared to be more effective than acclimation to shade at saturating light. We conclude that acclimation to submergence involves more than an increase in SLA to achieve the significant reduction of diffusion resistance for gas exchange between leaves and the water column.     

Acclimation of a terrestrial plant to submergence facilitates gas exchange under water

Flooding imposes stress upon terrestrial plants since it severely hampers gas exchange rates between the shoot and the environment. The resulting oxygen deficiency is considered to be the major problem for submerged plants. Oxygen microelectrode studies have, however, shown that aquatic plants maintain relatively high internal oxygen pressures under water, and even may release oxygen via the roots into the sediment, also in dark. Based on these results, we challenge the dogma that oxygen pressures in submerged terrestrial plants immediately drop to levels at which aerobic respiration is impaired. The present study demonstrates that the internal oxygen pressure in the petioles of Rumex palustris plants under water is indeed well above the critical oxygen pressure for aerobic respiration, provided that the air‐saturated water is not completely stagnant. The beneficial effect of shoot acclimation of this terrestrial plant species to submergence for gas exchange capacity is also shown. Shoot acclimation to submergence involved a reduction of the diffusion resistance to gases, which was not only functional by increasing diffusion of oxygen into the plant, but also by increasing influx of CO₂, which enhances underwater photosynthesis.     

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

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.     

Light acclimation, CO2 response and long-term capacity of underwater photosynthesis in three terrestrial plant species

To characterize underwater photosynthetic performance in some terrestrial plants, we determined (i) underwater light acclimation (ii) underwater photosynthetic response to dissolved CO₂, and (iii) underwater photosynthetic capacity during prolonged submergence in three species that differ in submergence tolerance: Phalaris arundinacea, Rumex crispus (both submergence-tolerant) and Arrhenatherum elatius (submergence-intolerant). None of the species had adjusted to low irradiance after 1 week of submergence. Under non-submerged (control) conditions, only R. crispus displayed shade acclimation. Submergence increased the apparent quantum yield in this species, presumably because of the enhanced CO₂ affinity of the elongated leaves. In control plants of the grass species P. arundinacea and A. elatius, CO₂ affinities were higher than for R. crispus. The underwater photosynthetic capacity of R. crispus increased during 1 month of submergence. In P. arundinacea photosynthesis remained constant during 1 month of submergence at normal irradiance; at low irradiance a reduction in photosynthetic capacity was observed after 2 weeks, although there was no tissue degeneration. In contrast, underwater photosynthesis of the submergence-intolerant species A. elatius collapsed rapidly under both irradiances, and this was accompanied by leaf decay. To describe photosynthesis versus irradiance curves, four models were evaluated. The hyperbolic tangent produced the best goodness-of-fit, whereas the rectangular hyperbola (Michaelis-Menten model) gave relatively poor results.     

Submergence-induced leaf acclimation in terrestrial species varying in flooding tolerance

Earlier work on the submergence-tolerant species Rumex palustris revealed that leaf anatomical and morphological changes induced by submergence enhance underwater gas exchange considerably. Here, the hypothesis is tested that these plastic responses are typical properties of submergence-tolerant species. Submergence-induced plasticity in leaf mass area (LMA) and leaf, cell wall and cuticle thickness was investigated in nine plant species differing considerably in tolerance to complete submergence. The functionality of the responses for underwater gas exchange was evaluated by recording oxygen partial pressures inside the petioles when plants were submerged. Acclimation to submergence resulted in a decrease in all leaf parameters, including cuticle thickness, in all species irrespective of flooding tolerance. Consequently, internal oxygen partial pressures (pO(2)) increased significantly in all species until values were close to air saturation. Only in nonacclimated leaves in darkness did intolerant species have a significantly lower pO(2) than tolerant species. These results suggest that submergence-induced leaf plasticity, albeit a prerequisite for underwater survival, does not discriminate tolerant from intolerant species. It is hypothesized that these plastic leaf responses may be induced in all species by several signals present during submergence; for example, low LMA may be a response to low photosynthate concentrations and a thin cuticle may be a response to high relative humidity.     

Underwater photosynthesis and respiration in leaves of submerged wetland plants: gas films improve CO2 and O2 exchange.

Many wetland plants have gas films on submerged leaf surfaces. We tested the hypotheses that leaf gas films enhance CO(2) uptake for net photosynthesis (P(N)) during light periods, and enhance O(2) uptake for respiration during dark periods. Leaves of four wetland species that form gas films, and two species that do not, were used. Gas films were also experimentally removed by brushing with 0.05% (v/v) Triton X. Net O(2) production in light, or O(2) consumption in darkness, was measured at various CO(2) and O(2) concentrations. When gas films were removed, O(2) uptake in darkness was already diffusion-limited at 20.6 kPa (critical O(2) pressure for respiration, COP(R)>/= 284 mmol O(2) m(-3)), whereas for some leaves with gas films, O(2) uptake declined only at approx. 4 kPa (COP(R) 54 mmol O(2) m(-3)). Gas films also improved CO(2) uptake so that, during light periods, underwater P(N) was enhanced up to sixfold. Gas films on submerged leaves enable continued gas exchange via stomata and thus bypassing of cuticle resistance, enhancing exchange of O(2) and CO(2) with the surrounding water, and therefore underwater P(N) and respiration.     

Crassulacean acid metabolism enhances underwater photosynthesis and diminishes photorespiration in the aquatic plant Isoetes australis

? Underwater photosynthesis by aquatic plants is often limited by low availability of CO(2), and photorespiration can be high. Some aquatic plants utilize crassulacean acid metabolism (CAM) photosynthesis. The benefits of CAM for increased underwater photosynthesis and suppression of photorespiration were evaluated for Isoetes australis, a submerged plant that inhabits shallow temporary rock pools. ? Leaves high or low in malate were evaluated for underwater net photosynthesis and apparent photorespiration at a range of CO(2) and O(2) concentrations. ? CAM activity was indicated by 9.7-fold higher leaf malate at dawn, compared with at dusk, and also by changes in the titratable acidity (μmol H(+) equivalents) of leaves. Leaves high in malate showed not only higher underwater net photosynthesis at low external CO(2) concentrations but also lower apparent photorespiration. Suppression by CAM of apparent photorespiration was evident at a range of O(2) concentrations, including values below air equilibrium. At a high O(2) concentration of 2.2-fold the atmospheric equilibrium concentration, net photosynthesis was reduced substantially and, although it remained positive in leaves containing high malate concentrations, it became negative in those low in malate. ? CAM in aquatic plants enables higher rates of underwater net photosynthesis over large O(2) and CO(2) concentration ranges in floodwaters, via increased CO(2) fixation and suppression of photorespiration.     

Oxygen dynamics during submergence in the halophytic stem succulent Halosarcia pergranulata

This study elucidated O2 dynamics in shoots and roots of submerged Halosarcia pergranulata (Salicornioideae), a perennial halophytic stem succulent that grows on floodprone mudflats of salt lakes. Oxygen within shoots and roots was measured using microelectrodes, for plants when waterlogged or completely submerged, with shoots in light or in darkness, in a controlled environment. Net photosynthesis (PN) when underwater, at a range of dissolved CO2 concentrations, was measured by monitoring O2 production rates by excised stems. The bulky nature and apparently low volume of gas-filled spaces of the succulent stems resulted in relatively high radial resistance to gas diffusion. At ambient CO2, quasi-steady state rates of PN by excised succulent stems were estimated to be close to zero; nevertheless, in intact plants, underwater photosynthesis provided O2 to tissues and led to radial O2 loss (ROL) from the roots, at least during the first several hours (the time period measured) after submergence or when light periods followed darkness. The influence of light on tissue O2 dynamics was confirmed in an experiment on a submerged plant in a salt lake in south-western Australia. In the late afternoon, partial pressure of O2 (pO2) in the succulent stem was 23.2 kPa (i.e. approximately 10% above that in the air), while in the roots, it was 6.2-9.8 kPa. Upon sunset, the pO2 in the succulent stems declined within 1 h to below detection, but then showed some fluctuations with the pO2 increasing to at most 2.5 kPa during the night. At night, pO2 in the roots remained higher than in the succulent stems, especially for a root with the basal portion in the floodwater. At sunrise, the pO2 increased in the succulent stems within minutes. In the roots, changes in the pO2 lagged behind those in the succulent stems. In summary, photosynthesis in stems of submerged plants increased the pO2 in the shoots and roots so that tissues experience diurnal changes in the pO2, but O2 from the H2O column also entered submerged plants.     

Leaf gas films of Spartina anglica enhance rhizome and root oxygen during tidal submergence

Gas films on hydrophobic surfaces of leaves of some wetland plants can improve O₂ and CO₂ exchange when completely submerged during floods. Here we investigated the in situ aeration of rhizomes of cordgrass (Spartina anglica) during natural tidal submergence, with focus on the role of leaf gas films on underwater gas exchange. Underwater net photosynthesis was also studied in controlled laboratory experiments. In field experiments, O₂ microelectrodes were inserted into rhizomes and pO₂ measured throughout two tidal submergence events; one during daylight and one during night‐time. Plants had leaf gas films intact or removed. Rhizome pO₂ dropped significantly during complete submergence and most severely during night. Leaf gas films: (1) enhanced underwater photosynthesis and pO₂ in rhizomes remained above 10 kPa during submergence in light; and (2) facilitated O₂ entry from the water into leaves so that rhizome pO₂ was about 5 kPa during darkness. This study is the first in situ demonstration of the beneficial effects of leaf gas films on internal aeration in a submerged wetland plant. Leaf gas films likely contribute to submergence tolerance of S. anglica and this feature is expected to also benefit other wetland plant species when submerged.     

Ethylene Sensitivity and Response Sensor Expression in Petioles of Rumex Species at Low O2 and High CO2 Concentrations

Rumex palustris, a flooding-tolerant plant, elongates its petioles in response to complete submergence. This response can be partly mimicked by enhanced ethylene levels and low O2 concentrations. High levels of CO2 do not markedly affect petiole elongation in R. palustris. Experiments with ethylene synthesis and action inhibitors demonstrate that treatment with low O2 concentrations enhances petiole extension by shifting sensitivity to ethylene without changing the rate of ethylene production. The expression level of the R. palustris gene coding for the putative ethylene receptor (RP-ERS1) is up-regulated by 3% O2 and increases after 20 min of exposure to a low concentration of O2, thus preceding the first significant increase in elongation observable after 40 to 50 min. In the flooding-sensitive species Rumex acetosa, submergence results in a different response pattern: petiole growth of the submerged plants is the same as for control plants. Exposure of R. acetosa to enhanced ethylene levels strongly inhibits petiole growth. This inhibitory effect of ethylene on R. acetosa can be reduced by both low levels of O2 and/or high concentrations of CO2.     

Surviving floods: leaf gas films improve O2 and CO2 exchange, root aeration, and growth of completely submerged rice

When completely submerged, the leaves of some species retain a surface gas film. Leaf gas films on submerged plants have recently been termed 'plant plastrons', analogous with the plastrons of aquatic insects. In aquatic insects, surface gas layers (i.e. plastrons) enlarge the gas–water interface to promote O₂ uptake when under water; however, the function of leaf gas films has rarely been considered. The present study demonstrates that gas films on leaves of completely submerged rice facilitate entry of O₂ from floodwaters when in darkness and CO₂ entry when in light. O₂ microprofiles showed that the improved gas exchange was not caused by differences in diffusive boundary layers adjacent to submerged leaves with or without gas films; instead, reduced resistance to gas exchange was probably due to the enlarged water–gas interface (cf. aquatic insects). When gas films were removed artificially, underwater net photosynthesis declined to only 20% of the rate with gas films present, such that, after 7 days of complete submergence, tissue sugar levels declined, and both shoot and root growth were reduced. Internal aeration of roots in anoxic medium, when shoots were in aerobic floodwater in darkness or when in light, was improved considerably when leaf gas films were present. Thus, leaf gas films contribute to the submergence tolerance of rice, in addition to those traits already recognized, such as the shoot-elongation response, aerenchyma and metabolic adjustments to O₂ deficiency and oxidative stress.     

Leaf gas films,underwater photosynthesis and plant species distributions in a flood gradient

Traits for survival during flooding of terrestrial plants include stimulation or inhibition of shoot elongation, aerenchyma formation and efficient gas exchange. Leaf gas films form on superhydrophobic cuticles during submergence and enhance underwater gas exchange. The main hypothesis tested was that the presence of leaf gas films influences the distribution of plant species along a natural flood gradient. We conducted laboratory experiments and field observations on species distributed along a natural flood gradient. We measured presence or absence of leaf gas films and specific leaf area of 95 species. We also measured, gas film retention time during submergence and underwater net photosynthesis and dark respiration of 25 target species. The presence of a leaf gas film was inversely correlated to flood frequency and duration and reached a maximum value of 80% of the species in the rarely flooded locations. This relationship was primarily driven by grasses that all, independently of their field location along the flood gradient, possess gas films when submerged. Although the present study and earlier experiments have shown that leaf gas films enhance gas exchange of submerged plants, the ability of species to form leaf gas films did not show the hypothesized relationship with species composition along the flood gradient.     

Resistance to complete submergence in Rumex species with different life histories: the influence of plant size and light

Resistance to complete submergence was tested in three Rumex species that occur in the Dutch river forelands. The species differ in both habitat and life history characteristics. The annual or biennial R. maritimus and the biennial or short lived perennial R. palustris grow on frequently flooded mud flats of low elevation, while the perennial R. thyrsiflorus can be found on dykes and river dunes that are seldom flooded. The flooding characteristics of the habitats of the three species were determined. These data were used to design experiments to determine the survival and biomass development of the three species during submergence and the influence of plant size and light level on these parameters. It was shown in all three species that plants submerged during daytime were much more resistant to flooding than those submerged at night. This is most probably due to the generation of oxygen or carbohydrates by underwater photosynthesis. Mature plants of the three species showed higher survival after submergence than juvenile plants, which might be caused by higher carbohydrate levels in the taproots of mature plants. In addition, the three species clearly differed in survival and biomass development during submergence. Rumex thyrsiflorus , the species least subjected to flooding, is least tolerant to complete submergence. Rumex maritimus , which can avoid the floods by having a short life cycle, is less tolerant to submergence than R. palustris , which has to survive the floods as a vegetative plant. It was noted that some plants that survived the flooding period itself, still died in the following period of drained conditions, possibly due to post-anoxic injury.     

Ethylene-promoted elongation: an adaptation to submergence stress

BACKGROUND: A sizeable minority of taxa is successful in areas prone to submergence. Many such plants elongate with increased vigour when underwater. This helps to restore contact with the aerial environment by shortening the duration of inundation. Poorly adapted species are usually incapable of this underwater escape. SCOPE: Evidence implicating ethylene as the principal factor initiating fast underwater elongation by leaves or stems is evaluated comprehensively along with its interactions with other hormones and gases. These interactions make up a sequence of events that link the perception of submergence to a prompt acceleration of extension. The review encompasses whole plant physiology, cell biology and molecular genetics. It includes assessments of how submergence threatens plant life and of the extent to which the submergence escape demonstrably improves the likelihood of survival. CONCLUSIONS: Experimental testing over many years establishes ethylene-promoted underwater extension as one of the most convincing examples of hormone-mediated stress adaptation by plants. The research has utilized a wide range of species that includes numerous angiosperms, a fern and a liverwort. It has also benefited from detailed physiological and molecular studies of underwater elongation by rice (Oryza sativa) and the marsh dock (Rumex palustris). Despite complexities and interactions, the work reveals that the signal transduction pathway is initiated by the simple expediency of physical entrapment of ethylene within growing cells by a covering of water.     

植物水淹适应与碳水化合物的相关性

水淹会对陆生植物存活造成本质影响, 特别是完全水淹对陆生植物的影响更为明显。水淹对陆生植物最为主要的影响是氧气不足, 这主要是由氧气在水中的扩散速率较低引起的。同时, 在水淹胁迫下植物对光和CO₂的获取都会受到限制。所有这些因素都将引起植物生物量减少, 最终导致受淹植物死亡。碳水化合物是植物的能量来源, 与植物在水淹胁迫下存活与否有着密切联系。植物水淹适应性与碳水化合物的相关性主要体现在两大方面: 在生理形态层面, 植物通过伸长生长或抑制伸长生长、地上和地下部分碳水化合物的分配比例不同来应对水淹胁迫; 在另一个层面, 植物通过改变激素、酶和基因的表达, 调整碳水化合物的代谢方式, 从而适应水淹环境。该文结合国内外研究现状, 通过对植物在水淹胁迫下生理形态、激素、酶及基因表达诸方面的变化来认识水淹耐受性与碳水化合物的关系, 并就今后的研究方向提出几点建议。     

Bimodal respiration and ventilatory behavior in two species of central American turtles: effects of forced submergence

Respiratory gas exchange in both air and water was measured at rest and during recovery from forced submergence in the giant Mexican musk turtle (Staurotypus triporcatus) and the white-lipped mud turtle (Kinosternon leucostomum). Diving and ventilatory behavior were also measured in unrestrained animals of each species. Despite large differences in cutaneous surface area, both species exhibited an aquatic V(O(2)) and V(CO(2)) of approximately 16 and 45%, respectively, with the remainder explained by aerial gas exchange. Aquatic V(O(2)) and V(CO(2)) did not significantly change during forced submergence or during the recovery period. Aerial V(O(2)) and V(CO(2)), however, profoundly increased after forced submergence in both species and were not significantly different from resting values until approximately 60 min following the treatment. At rest, K. leucostomum took significantly more breaths per breathing bout than S. triporcatus. This inherent ventilation pattern in each species remained unaltered following forced submergence. Cutaneous surface area, therefore, remains a minor component for these two species which rely heavily on pulmonary gas exchange to recover from forced submergence.     

Resistance to CO2 diffusion in cuticular membranes of amphibious plants and the implication for CO2 acquisition

Cuticular membranes (CMs) were isolated from leaves of amphibious and submerged plants and their CO2 resistances were determined as a contribution to establish quantitatively the series of resistances met by CO2 diffusing from bulk water to the chloroplasts of submerged leaves. The isolation was performed enzymatically; permeabilities were determined and converted to resistances. The range of permeance values was 3 to 43 x 10(-6) m s(-1) corresponding to resistance values of 23 to 295 x 10(3) s m(-1), i.e. of the same order of magnitude as boundary layer resistances. The sum of boundary layer, CM, leaf cell and carboxylation resistances could be contained within the total diffusion resistance as determined from the photosynthetic CO2 affinity of the leaf. From the same species, the aerial leaf CM resistance was always higher than the aquatic leaf CM resistance. In a terrestrial plant, the CM resistance to CO2 diffusion was found lower in leaves developed submerged.     

In situ O2 dynamics in submerged Isoetes australis: varied leaf gas permeability influences underwater photosynthesis and internal O2

A unique type of vernal pool are those formed on granite outcrops, as the substrate prevents percolation so that water accumulates in depressions when precipitation exceeds evaporation. The O(2) dynamics of small, shallow vernal pools with dense populations of Isoetes australis were studied in situ, and the potential importance of the achlorophyllous leaf bases to underwater net photosynthesis (P(N)) and radial O(2) loss to sediments is highlighted. O(2) microelectrodes were used in situ to monitor pO(2) in leaves, shallow sediments, and water in four vernal pools. The role of the achlorophyllous leaf bases in gas exchange was evaluated in laboratory studies of underwater P(N), loss of tissue water, radial O(2) loss, and light microscopy. Tissue and sediment pO(2) showed large diurnal amplitudes and internal O(2) was more similar to sediment pO(2) than water pO(2). In early afternoon, sediment pO(2) was often higher than tissue pO(2) and although sediment O(2) declined substantially during the night, it did not become anoxic. The achlorophyllous leaf bases were 34% of the surface area of the shoots, and enhanced by 2.5-fold rates of underwater P(N) by the green portions, presumably by increasing the surface area for CO(2) entry. In addition, these leaf bases would contribute to loss of O(2) to the surrounding sediments. Numerous species of isoetids, seagrasses, and rosette-forming wetland plants have a large proportion of the leaf buried in sediments and this study indicates that the white achlorophyllous leaf bases may act as an important area of entry for CO(2), or exit for O(2), with the surrounding sediment.