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Photosynthesis-dependent formation of convoluted plasma membrane domains in Chara internodal cells is independent of chloroplast position.

Foissner I, Sommer A, Hoeftberger M - Protoplasma (2014)

Bottom Line: In contrast, charasomes were rarely found at uneven, bulged wound walls which protrude into the streaming endoplasm and which were induced by ligation or puncturing.The results of this study show that charasome formation, although dependent on photosynthesis, does not require intimate contact with chloroplasts.Finally, we hypothesize that the absence of charasomes at bulged wound walls is due to the disturbance of uniform laminar mass streaming.

View Article: PubMed Central - PubMed

Affiliation: Plant Physiology/Cell Biology, University of Salzburg, Hellbrunnerstrasse 34, 5020, Salzburg, Austria, Ilse.Foissner@sbg.ac.at.

ABSTRACT
The characean green alga Chara australis forms complex plasma membrane convolutions called charasomes when exposed to light. Charasomes are involved in local acidification of the surrounding medium which facilitates carbon uptake required for photosynthesis. They have hitherto been only described in the internodal cells and in close contact with the stationary chloroplasts. Here, we show that charasomes are not only present in the internodal cells of the main axis, side branches, and branchlets but that the plasma membranes of chloroplast-containing nodal cells, protonemata, and rhizoids are also able to invaginate into complex domains. Removal of chloroplasts by local irradiation with intense light revealed that charasomes can develop at chloroplast-free "windows" and that the resulting pH banding pattern is independent of chloroplast or window position. Charasomes were not detected along cell walls containing functional plasmodesmata. However, charasomes formed next to a smooth wound wall which was deposited onto the plasmodesmata-containing wall when the neighboring cell was damaged. In contrast, charasomes were rarely found at uneven, bulged wound walls which protrude into the streaming endoplasm and which were induced by ligation or puncturing. The results of this study show that charasome formation, although dependent on photosynthesis, does not require intimate contact with chloroplasts. Our data suggest further that the presence of plasmodesmata inhibits charasome formation and/or that exposure to the outer medium is a prerequisite for charasome formation. Finally, we hypothesize that the absence of charasomes at bulged wound walls is due to the disturbance of uniform laminar mass streaming.

No MeSH data available.


Related in: MedlinePlus

Schematic summary. In intact internodal cells (I) charasomes (black dots) are present between chloroplasts (C) at the longitudinal cell walls but absent from the chloroplast-free cross walls (arrows) which are perforated by plasmodesmata-containing channels (short black lines within the light gray cell wall). Charasomes may form at chloroplast-free windows (W) but they are absent from uneven wound walls (WW) which protrude into the endoplasm (not drawn). In nodes charasomes are present along the outer cell walls of peripheral, roundish nodal cells (rN), and of peripheral, cone-shaped nodal cells (cN; bract cells or stipulodes). No charasomes are found beneath the plasmodesmata-containing cell walls. Following damage of internodal cell (dI), a plasmodesmata-free wound wall (dark gray line) is deposited by the adjacent nodal cells (N) and charasomes may form along its smooth surface. Only approximately drawn to scale and with reduced number of nodal cells
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Fig5: Schematic summary. In intact internodal cells (I) charasomes (black dots) are present between chloroplasts (C) at the longitudinal cell walls but absent from the chloroplast-free cross walls (arrows) which are perforated by plasmodesmata-containing channels (short black lines within the light gray cell wall). Charasomes may form at chloroplast-free windows (W) but they are absent from uneven wound walls (WW) which protrude into the endoplasm (not drawn). In nodes charasomes are present along the outer cell walls of peripheral, roundish nodal cells (rN), and of peripheral, cone-shaped nodal cells (cN; bract cells or stipulodes). No charasomes are found beneath the plasmodesmata-containing cell walls. Following damage of internodal cell (dI), a plasmodesmata-free wound wall (dark gray line) is deposited by the adjacent nodal cells (N) and charasomes may form along its smooth surface. Only approximately drawn to scale and with reduced number of nodal cells

Mentions: Nodal cells differ from the internodal cells in their shape, size, and in the presence of only one nucleus (Beilby and Casanova 2014; Wood and Imahori 1965). Apart from this very general definition, nodal cells vary considerably in localization, shape, and cytoplasmic organization (Figs. 1a and 2a, b). The nodes of Chara australis consist of a group of flat central cells squeezed between the upper and lower internodal cell. The flat central nodal cells are surrounded by peripheral, roundish cells intercalating with cone-shaped cells called stipulodes or bract cells dependent on whether they are located at the nodes of the main axis or the nodes of the branchlets (Figs. 1a and 2a, b). No charasomes were found in nodes of freshly collected, growing thalli, which were cultivated at rather low light intensities (about 5 μEinstein m−2 s−1 at the surface of culture vessels). In fully grown thalli and in thallus fragments exposed to stronger light, FM1-43 fluorescent immobile punctae were detected in the cortical cytoplasm of stipulodes and bract cells (Figs. 2c, d and 5) and the electron microscopy confirmed their identity as charasomes (not shown). The cytoarchitecture of these cells mostly resembled that of the internodes and consisted of a stationary layer of well-developed chloroplasts and a streaming endoplasm. Charasomes were also present in the peripheral roundish nodal cells (Figs. 2e, f and 5) irrespective whether their cytoplasm was stagnant or separated into a stationary cortical layer and a streaming endoplasm. Occasionally, we observed nodal cells in which chloroplasts participated in rotational mass streaming and even in these cell charasomes, although very delicate ones, could be detected (Suppl. Video 1). A prerequisite for charasome formation appeared to be the presence of chloroplasts because charasomes were never detected in those peripheral nodal cells, which were likely to give rise to a side branch and contained only proplastids embedded in a dense, non-streaming cytoplasm.Fig. 2


Photosynthesis-dependent formation of convoluted plasma membrane domains in Chara internodal cells is independent of chloroplast position.

Foissner I, Sommer A, Hoeftberger M - Protoplasma (2014)

Schematic summary. In intact internodal cells (I) charasomes (black dots) are present between chloroplasts (C) at the longitudinal cell walls but absent from the chloroplast-free cross walls (arrows) which are perforated by plasmodesmata-containing channels (short black lines within the light gray cell wall). Charasomes may form at chloroplast-free windows (W) but they are absent from uneven wound walls (WW) which protrude into the endoplasm (not drawn). In nodes charasomes are present along the outer cell walls of peripheral, roundish nodal cells (rN), and of peripheral, cone-shaped nodal cells (cN; bract cells or stipulodes). No charasomes are found beneath the plasmodesmata-containing cell walls. Following damage of internodal cell (dI), a plasmodesmata-free wound wall (dark gray line) is deposited by the adjacent nodal cells (N) and charasomes may form along its smooth surface. Only approximately drawn to scale and with reduced number of nodal cells
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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Fig5: Schematic summary. In intact internodal cells (I) charasomes (black dots) are present between chloroplasts (C) at the longitudinal cell walls but absent from the chloroplast-free cross walls (arrows) which are perforated by plasmodesmata-containing channels (short black lines within the light gray cell wall). Charasomes may form at chloroplast-free windows (W) but they are absent from uneven wound walls (WW) which protrude into the endoplasm (not drawn). In nodes charasomes are present along the outer cell walls of peripheral, roundish nodal cells (rN), and of peripheral, cone-shaped nodal cells (cN; bract cells or stipulodes). No charasomes are found beneath the plasmodesmata-containing cell walls. Following damage of internodal cell (dI), a plasmodesmata-free wound wall (dark gray line) is deposited by the adjacent nodal cells (N) and charasomes may form along its smooth surface. Only approximately drawn to scale and with reduced number of nodal cells
Mentions: Nodal cells differ from the internodal cells in their shape, size, and in the presence of only one nucleus (Beilby and Casanova 2014; Wood and Imahori 1965). Apart from this very general definition, nodal cells vary considerably in localization, shape, and cytoplasmic organization (Figs. 1a and 2a, b). The nodes of Chara australis consist of a group of flat central cells squeezed between the upper and lower internodal cell. The flat central nodal cells are surrounded by peripheral, roundish cells intercalating with cone-shaped cells called stipulodes or bract cells dependent on whether they are located at the nodes of the main axis or the nodes of the branchlets (Figs. 1a and 2a, b). No charasomes were found in nodes of freshly collected, growing thalli, which were cultivated at rather low light intensities (about 5 μEinstein m−2 s−1 at the surface of culture vessels). In fully grown thalli and in thallus fragments exposed to stronger light, FM1-43 fluorescent immobile punctae were detected in the cortical cytoplasm of stipulodes and bract cells (Figs. 2c, d and 5) and the electron microscopy confirmed their identity as charasomes (not shown). The cytoarchitecture of these cells mostly resembled that of the internodes and consisted of a stationary layer of well-developed chloroplasts and a streaming endoplasm. Charasomes were also present in the peripheral roundish nodal cells (Figs. 2e, f and 5) irrespective whether their cytoplasm was stagnant or separated into a stationary cortical layer and a streaming endoplasm. Occasionally, we observed nodal cells in which chloroplasts participated in rotational mass streaming and even in these cell charasomes, although very delicate ones, could be detected (Suppl. Video 1). A prerequisite for charasome formation appeared to be the presence of chloroplasts because charasomes were never detected in those peripheral nodal cells, which were likely to give rise to a side branch and contained only proplastids embedded in a dense, non-streaming cytoplasm.Fig. 2

Bottom Line: In contrast, charasomes were rarely found at uneven, bulged wound walls which protrude into the streaming endoplasm and which were induced by ligation or puncturing.The results of this study show that charasome formation, although dependent on photosynthesis, does not require intimate contact with chloroplasts.Finally, we hypothesize that the absence of charasomes at bulged wound walls is due to the disturbance of uniform laminar mass streaming.

View Article: PubMed Central - PubMed

Affiliation: Plant Physiology/Cell Biology, University of Salzburg, Hellbrunnerstrasse 34, 5020, Salzburg, Austria, Ilse.Foissner@sbg.ac.at.

ABSTRACT
The characean green alga Chara australis forms complex plasma membrane convolutions called charasomes when exposed to light. Charasomes are involved in local acidification of the surrounding medium which facilitates carbon uptake required for photosynthesis. They have hitherto been only described in the internodal cells and in close contact with the stationary chloroplasts. Here, we show that charasomes are not only present in the internodal cells of the main axis, side branches, and branchlets but that the plasma membranes of chloroplast-containing nodal cells, protonemata, and rhizoids are also able to invaginate into complex domains. Removal of chloroplasts by local irradiation with intense light revealed that charasomes can develop at chloroplast-free "windows" and that the resulting pH banding pattern is independent of chloroplast or window position. Charasomes were not detected along cell walls containing functional plasmodesmata. However, charasomes formed next to a smooth wound wall which was deposited onto the plasmodesmata-containing wall when the neighboring cell was damaged. In contrast, charasomes were rarely found at uneven, bulged wound walls which protrude into the streaming endoplasm and which were induced by ligation or puncturing. The results of this study show that charasome formation, although dependent on photosynthesis, does not require intimate contact with chloroplasts. Our data suggest further that the presence of plasmodesmata inhibits charasome formation and/or that exposure to the outer medium is a prerequisite for charasome formation. Finally, we hypothesize that the absence of charasomes at bulged wound walls is due to the disturbance of uniform laminar mass streaming.

No MeSH data available.


Related in: MedlinePlus