Desiccation tolerance in the chlorophyte green alga Ulva compressa: does cell wall architecture contribute to ecological success?

Abstract

Main conclusionDesiccation leads to structural changes of the inner pectic cell wall layers inUlva compressa. This contributes to protection against mechanical damage due to desiccation–rehydration cycles.Ulva compressa, characterized by rbcL phylogeny, is a common species in the Mediterranean Sea. Ulva as an intertidal species tolerates repeated desiccation–rehydration cycles in nature; the physiological and structural basis were investigated under experimental conditions here. Desiccation to 73 % relative water content (RWC) led to a significant decrease of the maximum quantum yield of photosystem II (Fv/Fm) to about half of the initial value. A reduction to 48 or 27 % RWC caused a more drastic effect and thalli were only able to recover fully from desiccation to 73 % RWC. Relative electron transport rates were stimulated at 73 % RWC, but decreased significantly at 48 and 27 % RWC, respectively. Imaging-PAM analysis demonstrated a homogenous desiccation process within individual thallus discs. The different cell wall layers of U. compressa were characterized by standard staining procedures, i.e. calcofluor white and aniline blue for structural components (cellulose, callose), ruthenium red for pectins and toluidine blue for acidic polysaccharides. Already a reduction to 73 % RWC caused severe changes of the cell walls. The inner pectin-rich layers followed the shrinkage process of the cytoplasm, while the outer denser fibrillar layers maintained their shape. In this way, the thalli were not plasmolyzed during water loss, and upon recovery not negatively influenced by any mechanical damage. Transmission electron microscopy corroborated the arrangement of the different layers clearly distinguishable by their texture and electron density. We suggest the flexibility of the pectin-rich cell wall layers as a major contribution to desiccation tolerance in Ulva.Electronic supplementary materialThe online version of this article (doi:10.1007/s00425-015-2292-6) contains supplementary material, which is available to authorized users.

Interaction of Photoprotective and Acclimation Mechanisms in Ulva rigida (Chlorophyta) in Response to Diurnal Changes in Solar Radiation in Southern Chile

“…, Holzinger et al. ). These structures appear to be similar to vesicles containing phenolic compounds in brown algae called physodes (Gomez and Huovinen ).…”

“…In this respect, the chemical structures of flavonoids are derived from the acetate/malonate pathway and phenylalanine through the shikimate pathway (Merken andBeecher 2000, Ignat et al 2011). Another strategy that has been observed in some filamentous algae is the accumulation of phenolic compounds in large vacuoles surrounding the central parts of the cells or the thickening and rigidification of the cell wall, which allows them an efficient protection against both high PAR and UV radiation to the lower cell layers by shading (Aigner et al 2013, Holzinger et al 2015. These structures appear to be similar to vesicles containing phenolic compounds in brown algae called physodes (Gomez and Huovinen 2010).…”

“…The acclimation of the photosynthetic apparatus to diurnal changes of light in Ulva are related to the efficiency of a series of mechanisms such as: (i) the dissipation of energy as heat via the xanthophyll cycle (Franklin et al 2003, Mou et al 2013), (ii) a reduction in the efficiency of energy transfer to PSII reaction centers (i.e., photoinhibition; Pescheck et al 2016), and (iii) changes in the size of the light-harvesting antennae through the reduction of photosynthetic and accessory pigments (Melis 2009). Likewise, in the genus Ulva, the carbon-assimilation pathways also could play an important role in its acclimation to different light conditions (Cruces et al 2012b, G omez and Huovinen 2012, Holzinger et al 2015, Zhao et al 2016. For example, studies have shown that the exposure of U. prolifera to light intensities >1,000 lmol photons Á m À2 Á s À1 triggered a decrease in the gene expression of key enzymes of C 4 metabolism and RuBisCO's large subunit (Xu et al 2012).…”

Cell structure and microtubule organisation during gametogenesis of Ulva mutabilis Føyn (Chlorophyta)

“…Gardner (Leonardi et al 1997). A more detailed description of the cell wall of Ulva compressa L. has been reported by Holzinger et al (2015). According to this study, the wall is multilayered, consisting of cellulose, callose and acidic polysaccharides.…”

Introduction to desiccation biology: from old borders to new frontiers

“…Avoidance of mechanical stress both at the macroscopic level (e.g., leaf folding in resurrection plants, coiling of midge and dauer larvae) and the molecular level (composition and bending of phospholipid membranes, plasticity of cell walls). An example of cell wall adaptation to drying is provided by Holzinger et al (2015) on Ulva compressa, a Mediterranean macroalga that survives severe desiccation (-23 MPa) and salinity. These authors present evidence that the flexibility of the cell wall due to pectins contributes to desiccation tolerance.…”