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

Holzinger A, Herburger K, Kaplan F, Lewis LA - Planta (2015)

Bottom Line: 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.Already a reduction to 73% RWC caused severe changes of the cell walls.

View Article: PubMed Central - PubMed

Affiliation: Institute of Botany, Functional Plant Biology, University of Innsbruck, Sternwartestrasse 15, 6020, Innsbruck, Austria, andreas.holzinger@uibk.ac.at.

ABSTRACT

Main conclusion: Desiccation leads to structural changes of the inner pectic cell wall layers in Ulva 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 (F v/F m) 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.

No MeSH data available.


Related in: MedlinePlus

Light micrographs of U. compressa. a Surface view of a central area of the thallus. No intercellular spaces are visible between the polygonal cells. b Corresponding CFW staining of cellulose. c RR staining of fresh samples to visualize pectins, which are abundant in the inner cell wall layer attached to the protoplast (arrows). d RR staining in a sample desiccated for 30 min. The inner pectic-rich layer increases in diameter (arrows). e Chemically fixed, TB-stained semithin cross section of a fresh sample showing an irregular arrangement of cells in both thallus layers. TB-stained cross section of a sample desiccated for 30 min. Fragments of the cell wall matrix are attached to periclinal cell walls (arrowheads). The protoplasts show undulations followed by the cell walls, while no retraction of the cytoplasm from the cell walls occurs. The thickness of the thallus segment decreases. Scale bars 10 µm
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Fig3: Light micrographs of U. compressa. a Surface view of a central area of the thallus. No intercellular spaces are visible between the polygonal cells. b Corresponding CFW staining of cellulose. c RR staining of fresh samples to visualize pectins, which are abundant in the inner cell wall layer attached to the protoplast (arrows). d RR staining in a sample desiccated for 30 min. The inner pectic-rich layer increases in diameter (arrows). e Chemically fixed, TB-stained semithin cross section of a fresh sample showing an irregular arrangement of cells in both thallus layers. TB-stained cross section of a sample desiccated for 30 min. Fragments of the cell wall matrix are attached to periclinal cell walls (arrowheads). The protoplasts show undulations followed by the cell walls, while no retraction of the cytoplasm from the cell walls occurs. The thickness of the thallus segment decreases. Scale bars 10 µm

Mentions: Ulva compressa thalli were unbranched, tubular and showed typical conduplicated margins (Fig. 2a). Their diameter was between 4 and 10 mm, while mid-sized thalli were chosen to punch out discs for microscopic and physiological investigations (Fig. 2b–e). Control discs were covered with a thin water layer after removing most water with a paper towel (Fig. 2b). In contrast, after 30 min (73 % RWC) of desiccation at a relative humidity (RH) of ~62 %, no surface water was visible (Fig. 2b–e). Formation of salt crystals was scarce and the discs stayed visibly green (Fig. 2b–d). In top view, cells were irregularly arranged and had a diameter of 6–12 µm (Fig. 3a, b). Usually they were polygonal with rounded corners (Fig. 3a). However, cells were spherical when they became separated from the cell complex, as seen in some areas of the thallus (Fig. 3c, Fig. S2). The chloroplasts were hood-shaped or appeared to fill the cells (Fig. 3c). The thick multilayered cell wall contained cellulose (Fig. 3b) and pectic substances, which were particularly abundant in the innermost cell wall layer as shown by staining with RR and TB (Fig. 3c–f). This pectic layer increased in diameter after desiccation (Fig. 3d, f). Furthermore, cellular water loss led to shrinkage and undulations of the cell walls (Fig. 3f). In cross-sectional view, desiccated thalli appeared flatter compared to hydrated control groups (Fig. 3e, f).Fig. 2


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

Holzinger A, Herburger K, Kaplan F, Lewis LA - Planta (2015)

Light micrographs of U. compressa. a Surface view of a central area of the thallus. No intercellular spaces are visible between the polygonal cells. b Corresponding CFW staining of cellulose. c RR staining of fresh samples to visualize pectins, which are abundant in the inner cell wall layer attached to the protoplast (arrows). d RR staining in a sample desiccated for 30 min. The inner pectic-rich layer increases in diameter (arrows). e Chemically fixed, TB-stained semithin cross section of a fresh sample showing an irregular arrangement of cells in both thallus layers. TB-stained cross section of a sample desiccated for 30 min. Fragments of the cell wall matrix are attached to periclinal cell walls (arrowheads). The protoplasts show undulations followed by the cell walls, while no retraction of the cytoplasm from the cell walls occurs. The thickness of the thallus segment decreases. Scale bars 10 µm
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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Fig3: Light micrographs of U. compressa. a Surface view of a central area of the thallus. No intercellular spaces are visible between the polygonal cells. b Corresponding CFW staining of cellulose. c RR staining of fresh samples to visualize pectins, which are abundant in the inner cell wall layer attached to the protoplast (arrows). d RR staining in a sample desiccated for 30 min. The inner pectic-rich layer increases in diameter (arrows). e Chemically fixed, TB-stained semithin cross section of a fresh sample showing an irregular arrangement of cells in both thallus layers. TB-stained cross section of a sample desiccated for 30 min. Fragments of the cell wall matrix are attached to periclinal cell walls (arrowheads). The protoplasts show undulations followed by the cell walls, while no retraction of the cytoplasm from the cell walls occurs. The thickness of the thallus segment decreases. Scale bars 10 µm
Mentions: Ulva compressa thalli were unbranched, tubular and showed typical conduplicated margins (Fig. 2a). Their diameter was between 4 and 10 mm, while mid-sized thalli were chosen to punch out discs for microscopic and physiological investigations (Fig. 2b–e). Control discs were covered with a thin water layer after removing most water with a paper towel (Fig. 2b). In contrast, after 30 min (73 % RWC) of desiccation at a relative humidity (RH) of ~62 %, no surface water was visible (Fig. 2b–e). Formation of salt crystals was scarce and the discs stayed visibly green (Fig. 2b–d). In top view, cells were irregularly arranged and had a diameter of 6–12 µm (Fig. 3a, b). Usually they were polygonal with rounded corners (Fig. 3a). However, cells were spherical when they became separated from the cell complex, as seen in some areas of the thallus (Fig. 3c, Fig. S2). The chloroplasts were hood-shaped or appeared to fill the cells (Fig. 3c). The thick multilayered cell wall contained cellulose (Fig. 3b) and pectic substances, which were particularly abundant in the innermost cell wall layer as shown by staining with RR and TB (Fig. 3c–f). This pectic layer increased in diameter after desiccation (Fig. 3d, f). Furthermore, cellular water loss led to shrinkage and undulations of the cell walls (Fig. 3f). In cross-sectional view, desiccated thalli appeared flatter compared to hydrated control groups (Fig. 3e, f).Fig. 2

Bottom Line: 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.Already a reduction to 73% RWC caused severe changes of the cell walls.

View Article: PubMed Central - PubMed

Affiliation: Institute of Botany, Functional Plant Biology, University of Innsbruck, Sternwartestrasse 15, 6020, Innsbruck, Austria, andreas.holzinger@uibk.ac.at.

ABSTRACT

Main conclusion: Desiccation leads to structural changes of the inner pectic cell wall layers in Ulva 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 (F v/F m) 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.

No MeSH data available.


Related in: MedlinePlus