Leaf gas film: the ecological and eco-physiological effect of leaf gas films on completely submerged plants

Anders Winkel

    Research output: ThesisDoctoral Thesis

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    Abstract

    Super hydrophobic leaf surfaces are a relatively common trait in terrestrial plants which produce a self-cleansing surface that keeps leaves free of surface water, dirt and pathogens. Super hydrophobic leaves have also been shown to retain a film of gas surrounding the leaves when completely submerged. These gas films increase gas exchange between the leaves and floodwater and result in increased O2 and CO2 uptake. Enhanced gas exchange with the floodwater alleviates some of the constraints for submerged plants of the slow diffusion in water resulting in more available O2 for respiration (RD) during night and more CO2 for photosynthesis during day. This thesis contains a series of experiments investigating the effect of leaf gas films on completely submerged plants both in the field and in the laboratory.

    Underwater net photosynthesis (PN) was measured on 27 species of plants, 16 of which had leaf gas films when submerged. Underwater PN was 3.8 fold higher in species with leaf gas films at 100 μM CO2, compared with species lacking this feature, which shows that leaf gas films significantly increase photosynthesis under water. The benefits of improved underwater PN include endogenous O2 production which is crucial with regards to internal aeration and likely improved carbohydrate status of submerged plants. Of the 4 genotypes of rice investigated in Chapter 4, the flooding tolerant FR13A retained leaf gas films modestly longer than the intolerant IR42, but Swarna-Sub1 and Swarna did not differ in this feature. Underwater photosynthesis in submerged rice was markedly enhanced by gas film presence as was the internal aeration of roots.

    Internal aeration is the process of supplying O2 to plant tissues without a direct source, i.e. movement of O2 from shoots to roots. Tissues without O2 would suffer with inhibition of aerobic metabolism (RD) which can lead to low-energy stress, cessation of growth and ultimately death. I found that leaf gas films were an important component of internal aeration under field conditions of submerged rice and Spartina anglica, but also that light was a key factor in determining the O2 concentration status of belowground organs and tissues. During daytime, floodwater O2 concentration accounted for only 14% of the variation in root pO2 in rice whereas light accounted for 70% indicating that endogenously produced O2 was the primary source for roots in anoxic soil when these plants were submerged and when light was available. During the night, variation in floodwater pO2accounted for more than 70% of the variation in root pO2 and was the main source of O2for internal aeration when no light was available for underwater PN. At night, rice plants with leaf gas films had root pO2 values of 0.24-0.42 kPa (severely hypoxic) but roots of plants without leaf gas films went anoxic (O2 was below detection and presumably zero).During day, rice plants with leaf gas films had 1.2 fold higher root pO2 than plants without leaf gas films. A similar response was found for Spartina anglica even though theCO2 concentration in the water was significantly lower (15 μM CO2) which indicates that leaf gas films increase underwater PN and thus internal O2 even at low floodwater CO2concentrations.

    Leaf gas films were retained for 4 to 6 days on leaves of rice depending on genotype and gas film retention time was positively correlated to underwater PN; when leaf gas films were lost underwater PN declined sharply and subsequently there was degradation of leaf chlorophyll. Based on these data for rice I expected to find an overrepresentation of species with leaf gas films in a natural flooding regime where the floods did not last significantly longer than the gas films. To evaluate this idea, a screening study of leaf gas films presence/absence as well as leaf gas film retention time in terrestrial plants was conducted for species along a natural flood gradient in the Netherlands in the floodplains of the river Rhine. This hypothesis was rejected as abundance of species with leaf gas films did not ‘peak’ at a specific flooding regime, but rather increased in frequency from below 20% from the most flood prone areas with extended floods toward the drier areas with less frequent floods where up to 80% of species had leaf gas films. However, this finding does not necessarily rule out that leaf gas films can act as a crucial feature regarding flood tolerance of terrestrial plants, but further research is needed. The study did confirm findings that high SLA is correlated to species in areas with flooding risk, likely due to the benefit of thin leaves on gas exchange with floodwaters.Leaf gas films enhance underwater gas exchange and increase flood tolerance of species with super hydrophobic leaves. By increasing underwater gas exchange, underwater PN and RD were increased – long-distance internal diffusion of O2 also resulted in improved plant body aeration both during day and night. Increased internal aeration of plants while completely submerged as a result of leaf gas films, means this feature has characteristics resembling a flood tolerance trait and could be classified as such. Improved tissue O2status could result in less stress on completely submerged plants as metabolism can remain aerobic allowing plants to sustain their energy metabolism and possible conserve carbohydrates and through underwater PN produce carbohydrates to replenish, or at least partially supply sugar demand, alleviating some of the stress of being under water.
    Original languageEnglish
    QualificationDoctor of Philosophy
    Publication statusUnpublished - 2015

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