Underwater Photosynthesis Research Articles

Partial versus complete submergence: snorkelling aids root aeration in Rumex palustris but not in R. acetosa

The root and shoot tissues of flood-tolerant wetland plants are highly porous to enable internal gas phase diffusion of O2 during waterlogging or submergence. In the case of only partial submergence (snorkelling), the atmosphere can act as source of O2 . The aim of this study was to assess the effect of waterlogging, partial submergence and complete submergence in the dark as well as in light on O2 partial pressure (pO2 ) in roots of Rumex palustris (flood tolerant) and R. acetosa (flood intolerant). We used O2 microelectrodes to measure pO2 of adventitious roots during manipulations of the water level around the shoot. Root pO2 in both species declined significantly upon submergence but remained oxic also when shoots were completely submerged in the dark (0.8 and 4.6 kPa in R. acetosa and R. palustris, respectively). The snorkelling effect was substantial in R. palustris only. Submergence in light had less impact on root pO2 and the effect of snorkelling was also minor. Hence, the benefits of light (underwater photosynthesis) and air contact (snorkelling) upon growth and survival in submerged wetland plants can now be linked to enhanced internal aeration.

Physiological and transcriptomic characterization of submergence and reoxygenation responses in soybean seedlings

Complete inundation at the early seedling stage is a common environmental constraint for soybean production throughout the world. As floodwaters subside, submerged seedlings are subsequently exposed to reoxygenation stress in the natural progression of a flood event. Here, we characterized the fundamental acclimation responses to submergence and reoxygenation in soybean at the seedling establishment stage. Approximately 90% of seedlings succumbed during 3 d of inundation under constant darkness, whereas 10 d of submergence were lethal to over 90% of seedlings under 12 h light/12 h dark cycles, indicating the significance of underwater photosynthesis in seedling survival. Submergence rapidly decreased the abundance of carbohydrate reserves and ATP in aerial tissue of seedlings although chlorophyll breakdown was not observed. The carbohydrate and ATP contents were recovered upon de-submergence, but sudden exposure to oxygen also induced lipid peroxidation, confirming that reoxygenation induced oxidative stress. Whole transcriptome analysis recognized genome-scale reconfiguration of gene expression that regulates various signalling and metabolic pathways under submergence and reoxygenation. Comparative analysis of differentially regulated genes in shoots and roots of soybean and other plants defines conserved, organ-specific and species-specific adjustments which enhance adaptability to submergence and reoxygenation through different metabolic pathways.

Leaf gas films delay salt entry and enhance underwater photosynthesis and internal aeration of Melilotus siculus submerged in saline water

A combination of flooding and salinity is detrimental to most plants. We studied tolerance of complete submergence in saline water for Melilotus siculus, an annual legume with superhydrophobic leaf surfaces that retain gas films when under water. M. siculus survived complete submergence of 1 week at low salinity (up to 50 mol m(-3) NaCl), but did not recover following de-submergence from 100 mol m(-3) NaCl. The leaf gas films protected against direct salt ingress into the leaves when submerged in saline water, enabling underwater photosynthesis even after 3 d of complete submergence. By contrast, leaves with the gas films experimentally removed suffered from substantial Na(+) and Cl(-) intrusion and lost the capacity for underwater photosynthesis. Similarly, plants in saline water and without gas films lost more K(+) than those with intact gas films. This study has demonstrated that leaf gas films reduce Na(+) and Cl(-) ingress into leaves when submerged by saline water - the thin gas layer physically separates the floodwater from the leaf surface. This feature aids survival of plants exposed to short-term saline submergence, as well as the previously recognized beneficial effects of gas exchange under water.

Lowland rice: high‐end submergence tolerance

Lowland rice: high‐end submergence tolerance

Complete submergence escape with shoot elongation ability by underwater photosynthesis in African rice, Oryza glaberrima Steud.

Flooding imposes severe selection pressure on plants, principally because excess water in their surroundings deprives the plants certain basic resources such as oxygen, carbon dioxide, and light for photosynthesis. In recent years, reports of damage caused by flooding to rice plants have increased concomitantly with the expansion of rainfed lowland rice cultivation throughout the world. Strong submergence-induced elongation, a common escape mechanism, helps submerged individuals regain and retain contact with the aerobic environment. This study analyzed physiological mechanisms of escape from complete submergence by evaluating photosynthesis, photochemical reaction, and plant behavior during and after submergence in Oryza glaberrima Steud. Partially submerged plants were unaffected by excess water because their photosynthetic rate was maintained during and after submergence. Escape mechanisms, when under complete submergence, restrain shoot elongation per shoot dry weight per day during submergence (shoot elongation index). Our results demonstrate that the leaf area and shoot biomass of the submerged plants during submergence affects their post-submergence photosynthetic rate and the PSII maximum efficiency to some degree. Under deeply prolonged submergence, O. glaberrima genotypes were characterized by faster shoot elongation, anaerobic tillering, larger leaf area extension, higher photosynthetic rate, and maintenance of PSII maximum efficiency compared with Oryza sativa genotypes without an escape mechanism. O. glaberrima employs a submergence escape strategy that effectively uses stored carbohydrates for shoot elongation and leaf extension in a severely photosynthesis-limited environment under complete submergence.

Underwater photosynthesis of submerged plants - recent advances and methods.

We describe the general background and the recent advances in research on underwater photosynthesis of leaf segments, whole communities, and plant dominated aquatic ecosystems and present contemporary methods tailor made to quantify photosynthesis and carbon fixation under water. The majority of studies of aquatic photosynthesis have been carried out with detached leaves or thalli and this selectiveness influences the perception of the regulation of aquatic photosynthesis. We thus recommend assessing the influence of inorganic carbon and temperature on natural aquatic communities of variable density in addition to studying detached leaves in the scenarios of rising CO2 and temperature. Moreover, a growing number of researchers are interested in tolerance of terrestrial plants during flooding as torrential rains sometimes result in overland floods that inundate terrestrial plants. We propose to undertake studies to elucidate the importance of leaf acclimation of terrestrial plants to facilitate gas exchange and light utilization under water as these acclimations influence underwater photosynthesis as well as internal aeration of plant tissues during submergence.

Internal aeration of paddy field rice (Oryza sativa) during complete submergence – importance of light and floodwater O2

Flash floods can submerge paddy field rice (Oryza sativa), with adverse effects on internal aeration, sugar status and survival. Here, we investigated the in situ aeration of roots of rice during complete submergence, and elucidated how underwater photosynthesis and floodwater pO(2) influence root aeration in anoxic soil. In the field, root pO(2) was measured using microelectrodes during 2 d of complete submergence. Leaf gas films that formed on the superhydrophobic leaves were left intact, or experimentally removed, to elucidate their effect on internal aeration. In darkness, root pO(2) declined to very low concentrations (0.24 kPa) and was strongly correlated with floodwater pO(2). In light, root pO(2) was high (14 kPa) and primarily a function of the incident light determining the rates of underwater net photosynthesis. Plants with intact leaf gas films maintained higher underwater net photosynthesis relative to plants without gas films when the submerged shoots were in light. During complete submergence, internal aeration of rice in the field relies on underwater photosynthesis during the day and entry of O(2) from the floodwater during the night. Leaf gas films enhance photosynthesis during submergence leading to improved O(2) production and sugar status, and therefore contribute to the submergence tolerance of rice.

Early responses of Bassia diffusa (Thunb.) Kuntze to submergence for different salinity treatments

Early responses of the salt marsh succulent Bassia diffusa (Thunb.) Kuntze to combined salinity and submergence were studied in a laboratory experiment aimed at determining the pattern of the response of photosynthetic pigments, membrane stability, oxalic acid and water relations to these stressors. Three key stages in the response were identified. A drop in chlorophyll a+b within 6h (4.2±0.2 to 2.4±0.3mgg−1 DM) with a corresponding increase in carotenoid concentration (0.6±0.1mgg−1 DM) indicated an immediate response to submergence. Oxalic acid concentration was highest on Day 4 (1.7gg−1 DM) as opposed to control levels, indicative of its role in submergence tolerance, thus Day 4 may be the peak of positive acclimation. The third phase was marked by a sharp increase in electrolyte leakage to 47.5±2.6% on Day 10, from 9.4±1.4% on Day 7, with a corresponding decrease in total dissolved solutes between Days 7 and 10. Results suggest that oxalic acid accumulates under submergence possibly as a stabilising osmolyte. The threshold for tolerance of the species under submergence is 7days with membrane damage thereafter. B. diffusa would not survive prolonged submergence (>7days) but could survive submergence of short duration (<7days) through continuous underwater photosynthesis, accumulation of osmolytes such as oxalic acid and carotenoid, and maintenance of relative water content and succulence within control levels. These data show that this upper intertidal salt marsh plant would be sensitive to prolonged inundation as a result of sea level rise or due to estuary mouth closure and a subsequent rise in water level.

Shoot atmospheric contact is of little importance to aeration of deeper portions of the wetland plant Meionectes brownii; submerged organs mainly acquire O2 from the water column or produce it endogenously in underwater photosynthesis

Partial shoot submergence is considered less stressful than complete submergence of plants, as aerial contact allows gas exchange with the atmosphere. In situ microelectrode studies of the wetland plant Meionectes brownii showed that O(2) dynamics in the submerged stems and aquatic roots of partially submerged plants were similar to those of completely submerged plants, with internal O(2) concentrations in both organs dropping to less than 5 kPa by dawn regardless of submergence level. The anatomy at the nodes and the relationship between tissue porosity and rates of O(2) diffusion through stems were studied. Stem internodes contained aerenchyma and had mean gas space area of 17.7% per cross section, whereas nodes had 8.2%, but nodal porosity was highly variable, some nodes had very low porosity or were completely occluded (ca. 23% of nodes sampled). The cumulative effect of these low porosity nodes would have impeded internal O(2) movement down stems. Therefore, regardless of the presence of an aerial connection, the deeper portions of submerged organs sourced most of their O(2) via inwards diffusion from the water column during the night, and endogenous production in underwater photosynthesis during the daytime.

Oxygen dynamics in a salt-marsh soil and in Suaeda maritima during tidal submergence

Habitats occupied by many halophytes are not only saline, but are also prone to flooding and yet surprisingly few studies have evaluated submergence tolerance in halophytes. Sediment, floodwater, and intra-plant O2 dynamics were evaluated during tidal submergence for the leaf-succulent halophyte Suaeda maritima (L.) Dum. For S. maritima growing in soil just above the mud flat in a UK salt marsh, the soil was only moderately hypoxic just prior to tidal inundation, presumably owing to drainage and O2 entry facilitated by frequent, large cracks. O2 declined to very low levels following high tide. By contrast, mud flat sediment remained waterlogged, lacked cracks, and was anoxic. Plant O2 dynamics were investigated using field-collected plants in sediment blocks transported to a controlled-submergence system in a glasshouse. Submergence during night-time resulted in anoxia within leaves, whereas during day-time O2 was produced by underwater photosynthesis. The thin lateral roots of S. maritima presumably access some O2 from hypoxic sediments, but could also experience transient episodes of severe hypoxia/anoxia, especially as any internal O2 movement from shoots would be small owing to the low gas-filled porosity in roots. Fermentative metabolism to lactate, producing some ATP in the absence of O2, might contribute to tolerance of transient O2 deficits. Lactate was high in root tissues, whereas ethanol production (tissue and incubation medium contents) was low, both in comparison with values reported for other species. Our findings demonstrate the importance of tolerance to transient waterlogging and submergence for the halophyte S. maritima growing in a tidal salt marsh.

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 O(2) and CO(2) 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, O(2) microelectrodes were inserted into rhizomes and pO(2) measured throughout two tidal submergence events; one during daylight and one during night-time. Plants had leaf gas films intact or removed. Rhizome pO(2) dropped significantly during complete submergence and most severely during night. Leaf gas films: (1) enhanced underwater photosynthesis and pO(2) in rhizomes remained above 10 kPa during submergence in light; and (2) facilitated O(2) entry from the water into leaves so that rhizome pO(2) 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.

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 O2 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 (PN) and radial O2 loss to sediments is highlighted. O2 microelectrodes were used in situ to monitor pO2 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 PN, loss of tissue water, radial O2 loss, and light microscopy. Tissue and sediment pO2 showed large diurnal amplitudes and internal O2 was more similar to sediment pO2 than water pO2. In early afternoon, sediment pO2 was often higher than tissue pO2 and although sediment O2 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 PN by the green portions, presumably by increasing the surface area for CO2 entry. In addition, these leaf bases would contribute to loss of O2 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 CO2, or exit for O2, with the surrounding sediment.

A perspective on underwater photosynthesis in submerged terrestrial wetland plants.

Wetland plants inhabit flood-prone areas and therefore can experience episodes of complete submergence. Submergence impedes exchange of O(2) and CO(2) between leaves and the environment, and light availability is also reduced. The present review examines limitations to underwater net photosynthesis (P(N)) by terrestrial (i.e. usually emergent) wetland plants, as compared with submerged aquatic plants, with focus on leaf traits for enhanced CO(2) acquisition. Floodwaters are variable in dissolved O(2), CO(2), light and temperature, and these parameters influence underwater P(N) and the growth and survival of submerged plants. Aquatic species possess morphological and anatomical leaf traits that reduce diffusion limitations to CO(2) uptake and thus aid P(N) under water. Many aquatic plants also have carbon-concentrating mechanisms to increase CO(2) at Rubisco. Terrestrial wetland plants generally lack the numerous beneficial leaf traits possessed by aquatic plants, so submergence markedly reduces P(N). Some terrestrial species, however, produce new leaves with a thinner cuticle and higher specific leaf area, whereas others have leaves with hydrophobic surfaces so that gas films are retained when submerged; both improve CO(2) entry. Submergence inhibits P(N) by terrestrial wetland plants, but less so in species that produce new leaves under water or in those with leaf gas films. Leaves with a thinner cuticle, or those with gas films, have improved gas diffusion with floodwaters, so that underwater P(N) is enhanced. Underwater P(N) provides sugars and O(2) to submerged plants. Floodwaters often contain dissolved CO(2) above levels in equilibrium with air, enabling at least some P(N) by terrestrial species when submerged, although rates remain well below those in air.

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.

Submergence tolerance in Hordeum marinum: dissolved CO2 determines underwater photosynthesis and growth

Floodwaters differ markedly in dissolved CO2, yet the effects of CO2 on submergence responses of terrestrial plants have rarely been examined. The influence of dissolved CO2 on underwater photosynthesis and growth was evaluated for three accessions of the wetland plant Hordeum marinum Huds. All three accessions tolerated complete submergence, but only when in CO2 enriched floodwater. Plants submerged for 7 days in water at air equilibrium (18 µM CO2) suffered loss of biomass, whereas those with 200 µM CO2 continued to grow. Higher underwater net photosynthesis at 200 µM CO2 increased by 2.7- to 3.2-fold sugar concentrations in roots of submerged plants, compared with at air equilibrium CO2. Leaf gas films enhancing gas exchange with floodwater, lack of a shoot elongation response conserving tissue sugars and high tissue porosity (24–31% in roots) facilitating internal O2 movement, would all contribute to submergence tolerance in H. marinum. The present study demonstrates that dissolved CO2 levels can determine submergence tolerance of terrestrial plants. So, submergence experiments should be conducted with defined CO2 concentrations and enrichment might be needed to simulate natural environments and, thus, provide relevant plant responses.

Flooding tolerance: suites of plant traits in variable environments.

Flooding regimes of different depths and durations impose selection pressures for various traits in terrestrial wetland plants. Suites of adaptive traits for different flooding stresses, such as soil waterlogging (short or long duration) and full submergence (short or long duration - shallow or deep), are reviewed. Synergies occur amongst traits for improved internal aeration, and those for anoxia tolerance and recovery, both for roots during soil waterlogging and shoots during submergence. Submergence tolerance of terrestrial species has recently been classified as either the Low Oxygen Quiescence Syndrome (LOQS) or the Low Oxygen Escape Syndrome (LOES), with advantages, respectively, in short duration or long duration (shallow) flood-prone environments. A major feature of species with the LOQS is that shoots do not elongate upon submergence, whereas those with the LOES show rapid shoot extension. In addition, plants faced with long duration deep submergence can demonstrate aspects of both syndromes; shoots do not elongate, but these are not quiescent, as new aquatic-type leaves are formed. Enhanced entries of O2 and CO2 from floodwaters into acclimated leaves, minimises O2 deprivation and improves underwater photosynthesis, respectively. Evolution of 'suites of traits' are evident in wild wetland species and in rice, adapted to particular flooding regimes.

Oxygen dynamics in submerged rice (Oryza sativa)

Complete submergence of plants prevents direct O(2) and CO(2) exchange with air. Underwater photosynthesis can result in marked diurnal changes in O(2) supply to submerged plants. Dynamics in pO(2) had not been measured directly for submerged rice (Oryza sativa), but in an earlier study, radial O(2) loss from roots showed an initial peak following shoot illumination. O(2) dynamics in shoots and roots of submerged rice were monitored during light and dark periods, using O(2) microelectrodes. Tissue sugar concentrations were also measured. On illumination of shoots of submerged rice, pO(2) increased rapidly and then declined slightly to a new quasi-steady state. An initial peak was evident first in the shoots and then in the roots, and was still observed when 20 mol m(-3) glucose was added to the medium to ensure substrate supply in roots. At the new quasi-steady state following illumination, sheath pO(2) was one order of magnitude higher than in darkness, enhancing also pO(2) in roots. The initial peak in pO(2) following illumination of submerged rice was likely to result from high initial rates of net photosynthesis, fuelled by CO(2) accumulated during the dark period. Nevertheless, since sugars decline with time in submerged rice, substrate limitation of respiration could also contribute to morning peaks in pO(2) after longer periods of submergence.

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.

Oxygen dynamics during submergence in the halophytic stem succulentHalosarcia 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.

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.