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      Effectiveness of cuticular transpiration barriers in a desert plant at controlling water loss at high temperatures

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          Abstract

          Maintaining the integrity of the cuticular transpiration barrier even at elevated temperatures is of vital importance especially for hot-desert plants. Currently, the temperature dependence of the leaf cuticular water permeability and its relationship with the chemistry of the cuticles are not known for a single desert plant. This study investigates whether (i) the cuticular permeability of a desert plant is lower than that of species from non-desert habitats, (ii) the temperature-dependent increase of permeability is less pronounced than in those species and (iii) whether the susceptibility of the cuticular permeability barrier to high temperatures is related to the amounts or properties of the cutin or the cuticular waxes. We test these questions with Rhazya stricta using the minimum leaf water vapour conductance ( g min) as a proxy for cuticular water permeability. g min of R. stricta (5.41 × 10 −5 m s −1 at 25 °C) is in the upper range of all existing data for woody species from various non-desert habitats. At the same time, in R. stricta, the effect of temperature (15–50 °C) on g min (2.4-fold) is lower than in all other species (up to 12-fold). Rhazya stricta is also special since the temperature dependence of g min does not become steeper above a certain transition temperature. For identifying the chemical and physical foundation of this phenomenon, the amounts and the compositions of cuticular waxes and cutin were determined. The leaf cuticular wax (251.4 μg cm −2) is mainly composed of pentacyclic triterpenoids (85.2% of total wax) while long-chain aliphatics contribute only 3.4%. In comparison with many other species, the triterpenoid-to-cutin ratio of R. stricta (0.63) is high. We propose that the triterpenoids deposited within the cutin matrix restrict the thermal expansion of the polymer and, thus, prevent thermal damage to the highly ordered aliphatic wax barrier even at high temperatures.

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          Most cited references24

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          Building lipid barriers: biosynthesis of cutin and suberin.

          Cutin and suberin are the polymer matrices for lipophilic cell wall barriers. These barriers control the fluxes of gases, water and solutes, and also play roles in protecting plants from biotic and abiotic stresses and in controlling plant morphology. Although they are ubiquitous, cutin and suberin are the least understood of the major plant extracellular polymers. The use of forward and reverse genetic approaches in Arabidopsis has led to the identification of oxidoreductase and acyltransferase genes involved in the biosynthesis of these polymers. However, major questions about the underlying polymer structure, biochemistry, and intracellular versus extracellular assembly remain to be resolved. The analysis of plant lines with modified cutins and suberins has begun to reveal the inter-relationships between the composition and function of these polymers.
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            Protecting against water loss: analysis of the barrier properties of plant cuticles.

            The cuticle is the major barrier against uncontrolled water loss from leaves, fruits and other primary parts of higher plants. More than 100 mean values for water permeabilities determined with isolated leaf and fruit cuticles from 61 plant species are compiled and discussed in relation to plant organ, natural habitat and morphology. The maximum barrier properties of plant cuticles exceed that of synthetic polymeric films of equal thickness. Cuticular water permeability is not correlated to the thickness of the cuticle or to wax coverage. Relationships between cuticular permeability, wax composition and physical properties of the cuticle are evaluated. Cuticular permeability to water increases on the average by a factor of 2 when leaf surface temperature is raised from 15 degrees C to 35 degrees C. Organic compounds of anthropogenic and biogenic origin may enhance cuticular permeability. The pathway taken by water across the cuticular transport barrier is reviewed. The conclusion from this discussion is that the bulk of water diffuses as single molecules across a lipophilic barrier while a minor fraction travels along polar pores. Open questions concerning the mechanistic understanding of the plant cuticular transport barrier and the role the plant cuticle plays in ensuring the survival and reproductive success of an individual plant are indicated.
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              Tomato fruit cuticular waxes and their effects on transpiration barrier properties: functional characterization of a mutant deficient in a very-long-chain fatty acid beta-ketoacyl-CoA synthase.

              Cuticular waxes play a pivotal role in limiting transpirational water loss across the plant surface. The correlation between the chemical composition of the cuticular waxes and their function as a transpiration barrier is still unclear. In the present study, intact tomato fruits (Lycopersicon esculentum) are used, due to their astomatous surface, as a novel integrative approach to investigate this composition- function relationship: wax amounts and compositions of tomato were manipulated before measuring unbiased cuticular transpiration. First, successive mechanical and extractive wax-removal steps allowed the selective modification of epi- and intracuticular wax layers. The epicuticular film consisted exclusively of very-long-chain aliphatics, while the intracuticular compartment contained large quantities of pentacyclic triterpenoids as well. Second, applying reverse genetic techniques, a loss-of-function mutation with a transposon insertion in a very-long-chain fatty acid elongase beta-ketoacyl-CoA synthase was isolated and characterized. Mutant leaf and fruit waxes were deficient in n-alkanes and aldehydes with chain lengths beyond C30, while shorter chains and branched hydrocarbons were not affected. The mutant fruit wax also showed a significant increase in intracuticular triterpenoids. Removal of the epicuticular wax layer, accounting for one-third of the total wax coverage on wild-type fruits, had only moderate effects on transpiration. By contrast, reduction of the intracuticular aliphatics in the mutant to approximately 50% caused a 4-fold increase in permeability. Hence, the main portion of the transpiration barrier is located in the intracuticular wax layer, largely determined by the aliphatic constituents, but modified by the presence of triterpenoids, whereas epicuticular aliphatics play a minor role.
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                Author and article information

                Journal
                AoB Plants
                AoB Plants
                aobpla
                aobpla
                AoB Plants
                Oxford University Press
                2041-2851
                2016
                06 May 2016
                : 8
                : plw027
                Affiliations
                1Chair of Botany II - Ecophysiology and Vegetation Ecology, University of Würzburg, Julius-von-Sachs-Pl. 3, Würzburg D-97082, Germany
                2Department of Botany and Microbiology, College of Science, King Saud University, PO Box 2455, Riyadh 11451, Saudi Arabia
                3Chair of Botany I - Plant Physiology and Biophysics, University of Würzburg, Julius-von-Sachs-Pl. 2, Würzburg D-97082, Germany
                Author notes

                Associate Editor: Rafael S. Oliveira

                Citation: Schuster A, Burghardt M, Alfarhan A, Bueno A, Hedrich R, Leide J, Thomas J, Riederer M. 2016. Effectiveness of cuticular transpiration barriers in a desert plant at controlling water loss at high temperatures. AoB PLANTS 8: plw027; doi:10.1093/aobpla/plw027

                *Corresponding author’s e-mail address: riederer@ 123456uni-wuerzburg.de
                Article
                plw027
                10.1093/aobpla/plw027
                4925923
                27154622
                7a9d0064-1a76-448a-979b-d9b4a0dbf4cc
                Published by Oxford University Press on behalf of the Annals of Botany Company.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 29 September 2015
                : 13 April 2016
                Page count
                Pages: 14
                Categories
                Research Article

                Plant science & Botany
                aliphatic compounds,cuticular transpiration,cuticular wax,cutin,desert,minimum conductance,plant cuticle,temperature,transition temperature,triterpenoids

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