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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

Chloroplasts and charasomes in nodal cells. a Side view of nodal complex and adjacent internodal cell (I) visualized by fluorescent chloroplasts (projection of 109 optical sections with a thickness of 1.4 μm). Peripheral roundish nodal cells (N) alternate with bract cells (B). b Autofluorescent chloroplasts in a nodal complex viewed from above and after removal of internodes (projection of 134 optical sections with a thickness of 1.4 μm). The central, flat nodal cells (several cells died during preparation) are surrounded by peripheral, roundish nodal cells which intercalate with cone-shaped bract cells (B). The inset corresponds to Fig. 2g. c, d Optical sections through the periphery of an FM1-43-stained bract cell. Arrows indicate fluorescent epiphytes at the cell wall, V is the central vacuole. Arrows in the higher magnification (d) show immobile charasomes near the cell wall. Mobile endosomes are seen near the vacuole. e, f Charasomes and chloroplasts at the outer cell wall of peripheral nodal cells. The fluorescence image (e) shows autofluorescent chloroplasts (red) and FM1-43-stained charasomes (green). The electron micrograph (f) shows a charasome (asterisk) beneath the cell wall (CW) and close to a chloroplast (C) and to a mitochondrion (M). g, h Plasma membrane and plasmodesmata along the inner cell walls of nodal cells. The arrow in the fluorescence image (g) points to a cell wall pervaded by plasmodesmata which were stained with green fluorescent FM1-43. Note absence of charasomes; several chloroplasts (red autofluorescent) are present in the cortical cytoplasm. The arrow in the electron micrograph (h) points to a plasmodesmal channel in the cell wall (CW). The plasma membrane is wrinkled due to chemical fixation but charasomes are absent. i–k Charasomes at the inner cell wall of nodal cells formed after removal of internodal cells. In the fluorescence image (i) the green FM1-43 fluorescent structures in the cell wall (CW) correspond to channels containing the damaged plasmodesmata. In the cytoplasm (encircled) FM1-43 stained charasomes (green) are seen between autofluorescent chloroplasts (red). The electron micrographs (j) and (k) show that a thick wound wall (WW) had been deposited over the cell wall (CW) which is pervaded by plasmodesmata-containing channels (arrows in (j), C represents chloroplast, the inset corresponds to Fig. 2k). The higher magnification (k) shows a charasome (asterisk) beneath the wound wall (WW) and close to a mitochondrion (M). Bars = 100 μm (a, b), 20 μm (c, g, i), 10 μm (d, e), 2 μm (j), 500 nm (f, h, k)
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Fig2: Chloroplasts and charasomes in nodal cells. a Side view of nodal complex and adjacent internodal cell (I) visualized by fluorescent chloroplasts (projection of 109 optical sections with a thickness of 1.4 μm). Peripheral roundish nodal cells (N) alternate with bract cells (B). b Autofluorescent chloroplasts in a nodal complex viewed from above and after removal of internodes (projection of 134 optical sections with a thickness of 1.4 μm). The central, flat nodal cells (several cells died during preparation) are surrounded by peripheral, roundish nodal cells which intercalate with cone-shaped bract cells (B). The inset corresponds to Fig. 2g. c, d Optical sections through the periphery of an FM1-43-stained bract cell. Arrows indicate fluorescent epiphytes at the cell wall, V is the central vacuole. Arrows in the higher magnification (d) show immobile charasomes near the cell wall. Mobile endosomes are seen near the vacuole. e, f Charasomes and chloroplasts at the outer cell wall of peripheral nodal cells. The fluorescence image (e) shows autofluorescent chloroplasts (red) and FM1-43-stained charasomes (green). The electron micrograph (f) shows a charasome (asterisk) beneath the cell wall (CW) and close to a chloroplast (C) and to a mitochondrion (M). g, h Plasma membrane and plasmodesmata along the inner cell walls of nodal cells. The arrow in the fluorescence image (g) points to a cell wall pervaded by plasmodesmata which were stained with green fluorescent FM1-43. Note absence of charasomes; several chloroplasts (red autofluorescent) are present in the cortical cytoplasm. The arrow in the electron micrograph (h) points to a plasmodesmal channel in the cell wall (CW). The plasma membrane is wrinkled due to chemical fixation but charasomes are absent. i–k Charasomes at the inner cell wall of nodal cells formed after removal of internodal cells. In the fluorescence image (i) the green FM1-43 fluorescent structures in the cell wall (CW) correspond to channels containing the damaged plasmodesmata. In the cytoplasm (encircled) FM1-43 stained charasomes (green) are seen between autofluorescent chloroplasts (red). The electron micrographs (j) and (k) show that a thick wound wall (WW) had been deposited over the cell wall (CW) which is pervaded by plasmodesmata-containing channels (arrows in (j), C represents chloroplast, the inset corresponds to Fig. 2k). The higher magnification (k) shows a charasome (asterisk) beneath the wound wall (WW) and close to a mitochondrion (M). Bars = 100 μm (a, b), 20 μm (c, g, i), 10 μm (d, e), 2 μm (j), 500 nm (f, h, k)

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)

Chloroplasts and charasomes in nodal cells. a Side view of nodal complex and adjacent internodal cell (I) visualized by fluorescent chloroplasts (projection of 109 optical sections with a thickness of 1.4 μm). Peripheral roundish nodal cells (N) alternate with bract cells (B). b Autofluorescent chloroplasts in a nodal complex viewed from above and after removal of internodes (projection of 134 optical sections with a thickness of 1.4 μm). The central, flat nodal cells (several cells died during preparation) are surrounded by peripheral, roundish nodal cells which intercalate with cone-shaped bract cells (B). The inset corresponds to Fig. 2g. c, d Optical sections through the periphery of an FM1-43-stained bract cell. Arrows indicate fluorescent epiphytes at the cell wall, V is the central vacuole. Arrows in the higher magnification (d) show immobile charasomes near the cell wall. Mobile endosomes are seen near the vacuole. e, f Charasomes and chloroplasts at the outer cell wall of peripheral nodal cells. The fluorescence image (e) shows autofluorescent chloroplasts (red) and FM1-43-stained charasomes (green). The electron micrograph (f) shows a charasome (asterisk) beneath the cell wall (CW) and close to a chloroplast (C) and to a mitochondrion (M). g, h Plasma membrane and plasmodesmata along the inner cell walls of nodal cells. The arrow in the fluorescence image (g) points to a cell wall pervaded by plasmodesmata which were stained with green fluorescent FM1-43. Note absence of charasomes; several chloroplasts (red autofluorescent) are present in the cortical cytoplasm. The arrow in the electron micrograph (h) points to a plasmodesmal channel in the cell wall (CW). The plasma membrane is wrinkled due to chemical fixation but charasomes are absent. i–k Charasomes at the inner cell wall of nodal cells formed after removal of internodal cells. In the fluorescence image (i) the green FM1-43 fluorescent structures in the cell wall (CW) correspond to channels containing the damaged plasmodesmata. In the cytoplasm (encircled) FM1-43 stained charasomes (green) are seen between autofluorescent chloroplasts (red). The electron micrographs (j) and (k) show that a thick wound wall (WW) had been deposited over the cell wall (CW) which is pervaded by plasmodesmata-containing channels (arrows in (j), C represents chloroplast, the inset corresponds to Fig. 2k). The higher magnification (k) shows a charasome (asterisk) beneath the wound wall (WW) and close to a mitochondrion (M). Bars = 100 μm (a, b), 20 μm (c, g, i), 10 μm (d, e), 2 μm (j), 500 nm (f, h, k)
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Related In: Results  -  Collection

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Fig2: Chloroplasts and charasomes in nodal cells. a Side view of nodal complex and adjacent internodal cell (I) visualized by fluorescent chloroplasts (projection of 109 optical sections with a thickness of 1.4 μm). Peripheral roundish nodal cells (N) alternate with bract cells (B). b Autofluorescent chloroplasts in a nodal complex viewed from above and after removal of internodes (projection of 134 optical sections with a thickness of 1.4 μm). The central, flat nodal cells (several cells died during preparation) are surrounded by peripheral, roundish nodal cells which intercalate with cone-shaped bract cells (B). The inset corresponds to Fig. 2g. c, d Optical sections through the periphery of an FM1-43-stained bract cell. Arrows indicate fluorescent epiphytes at the cell wall, V is the central vacuole. Arrows in the higher magnification (d) show immobile charasomes near the cell wall. Mobile endosomes are seen near the vacuole. e, f Charasomes and chloroplasts at the outer cell wall of peripheral nodal cells. The fluorescence image (e) shows autofluorescent chloroplasts (red) and FM1-43-stained charasomes (green). The electron micrograph (f) shows a charasome (asterisk) beneath the cell wall (CW) and close to a chloroplast (C) and to a mitochondrion (M). g, h Plasma membrane and plasmodesmata along the inner cell walls of nodal cells. The arrow in the fluorescence image (g) points to a cell wall pervaded by plasmodesmata which were stained with green fluorescent FM1-43. Note absence of charasomes; several chloroplasts (red autofluorescent) are present in the cortical cytoplasm. The arrow in the electron micrograph (h) points to a plasmodesmal channel in the cell wall (CW). The plasma membrane is wrinkled due to chemical fixation but charasomes are absent. i–k Charasomes at the inner cell wall of nodal cells formed after removal of internodal cells. In the fluorescence image (i) the green FM1-43 fluorescent structures in the cell wall (CW) correspond to channels containing the damaged plasmodesmata. In the cytoplasm (encircled) FM1-43 stained charasomes (green) are seen between autofluorescent chloroplasts (red). The electron micrographs (j) and (k) show that a thick wound wall (WW) had been deposited over the cell wall (CW) which is pervaded by plasmodesmata-containing channels (arrows in (j), C represents chloroplast, the inset corresponds to Fig. 2k). The higher magnification (k) shows a charasome (asterisk) beneath the wound wall (WW) and close to a mitochondrion (M). Bars = 100 μm (a, b), 20 μm (c, g, i), 10 μm (d, e), 2 μm (j), 500 nm (f, h, k)
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