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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

Thallus of Chara australis and charasomes in internodal cells. a Simplified schematic drawing of a Chara thallus. The apical cell (AC) gives rise to a regular series of cylindrical internodal cells (I) and groups of nodal cells (gray). Nodal cells may divide further and produce side branches (shoots of unlimited growth like that of the main axis; not shown) and branchlets (shoots of limited growth). Nodes incubated in darkness produce upward growing protonemata and downward growing rhizoids. Protonema and rhizoid internodal cells investigated in this study are marked by asterisks. Non-dividing cone-shaped cells are called stipulodes (long arrow) in nodes of the main axis or bract cells (short arrow) in nodes of branchlets. b Light micrograph of an internodal cell incubated in phenol red. Pink color indicates alkaline pH. The arrows point to the intersections of chloroplast-free neutral lines located at the upper and lower surface of the cells. c Cortex of internodal cells containing helical files of stationary chloroplasts (red autofluorescent) and FM1-43-stained charasomes (green fluorescent). Note absence of charasomes at the neutral line (NL). d Side view of charasomes (FM1-43-fluorescent) between chloroplasts (red autofluorescent). e The green fluorescent FM1-43-stained plasma membrane at the cross wall (arrow; optical cross-section) between a nodal (N) and an internodal cell (I) is smooth (compare with (d)). In the internodal cell charasomes are seen at the longitudinal wall and between the chloroplasts (empty spaces; asterisk). Plasmodesmata are out of focus. f Two intertwining basal protonema internodal cells (arrows). g Red fluorescent chloroplasts and green fluorescent, FM1-43-stained punctate charasomes in a basal protonema internodal cell. The arrow points to FM1-43-stained epiphytes. h Proximal internodal cells of rhizoids (arrows) after 2 weeks of exposure to light. i–k Charasomes in a proximal rhizoid internodal cell. CLSM image of FM1-43-stained fluorescent charasomes (i) between starch-containing chloroplasts visualized by DIC in the merged image (j). The electron micrograph (k) is a slightly tangential section showing charasomes (asterisks) along the cell wall (CW) and mitochondria (M). Bars = 1 mm (a, b, f, h), 20 μm (e, i, j), 10 μm (c, d, g), and 500 nm (k)
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Fig1: Thallus of Chara australis and charasomes in internodal cells. a Simplified schematic drawing of a Chara thallus. The apical cell (AC) gives rise to a regular series of cylindrical internodal cells (I) and groups of nodal cells (gray). Nodal cells may divide further and produce side branches (shoots of unlimited growth like that of the main axis; not shown) and branchlets (shoots of limited growth). Nodes incubated in darkness produce upward growing protonemata and downward growing rhizoids. Protonema and rhizoid internodal cells investigated in this study are marked by asterisks. Non-dividing cone-shaped cells are called stipulodes (long arrow) in nodes of the main axis or bract cells (short arrow) in nodes of branchlets. b Light micrograph of an internodal cell incubated in phenol red. Pink color indicates alkaline pH. The arrows point to the intersections of chloroplast-free neutral lines located at the upper and lower surface of the cells. c Cortex of internodal cells containing helical files of stationary chloroplasts (red autofluorescent) and FM1-43-stained charasomes (green fluorescent). Note absence of charasomes at the neutral line (NL). d Side view of charasomes (FM1-43-fluorescent) between chloroplasts (red autofluorescent). e The green fluorescent FM1-43-stained plasma membrane at the cross wall (arrow; optical cross-section) between a nodal (N) and an internodal cell (I) is smooth (compare with (d)). In the internodal cell charasomes are seen at the longitudinal wall and between the chloroplasts (empty spaces; asterisk). Plasmodesmata are out of focus. f Two intertwining basal protonema internodal cells (arrows). g Red fluorescent chloroplasts and green fluorescent, FM1-43-stained punctate charasomes in a basal protonema internodal cell. The arrow points to FM1-43-stained epiphytes. h Proximal internodal cells of rhizoids (arrows) after 2 weeks of exposure to light. i–k Charasomes in a proximal rhizoid internodal cell. CLSM image of FM1-43-stained fluorescent charasomes (i) between starch-containing chloroplasts visualized by DIC in the merged image (j). The electron micrograph (k) is a slightly tangential section showing charasomes (asterisks) along the cell wall (CW) and mitochondria (M). Bars = 1 mm (a, b, f, h), 20 μm (e, i, j), 10 μm (c, d, g), and 500 nm (k)

Mentions: The characean thallus consists of a regular series of long, cylindrical internodal cells and groups of small, isodiametric or flat nodal cells from which side branches (shoots with unlimited growth) and whorls of lateral cells (branchlets, shoots with limited growth) emerge (Fig. 1a) (Wood and Imahori 1965). Growth occurs by the ordered division of a dome-shaped apical cell, which sequentially produces the internodal and nodal cells. Sexual reproduction involves the germination of an oospore, which produces a positively gravitropic primary rhizoid and a negatively gravitropic, upward growing primary protonema from which a new thallus emerges. Secondary protonemata and secondary rhizoids arise from nodes isolated from the differentiated thallus and buried in the sediment (Braun and Limbach 2006; Hodick 1993).Fig. 1


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)

Thallus of Chara australis and charasomes in internodal cells. a Simplified schematic drawing of a Chara thallus. The apical cell (AC) gives rise to a regular series of cylindrical internodal cells (I) and groups of nodal cells (gray). Nodal cells may divide further and produce side branches (shoots of unlimited growth like that of the main axis; not shown) and branchlets (shoots of limited growth). Nodes incubated in darkness produce upward growing protonemata and downward growing rhizoids. Protonema and rhizoid internodal cells investigated in this study are marked by asterisks. Non-dividing cone-shaped cells are called stipulodes (long arrow) in nodes of the main axis or bract cells (short arrow) in nodes of branchlets. b Light micrograph of an internodal cell incubated in phenol red. Pink color indicates alkaline pH. The arrows point to the intersections of chloroplast-free neutral lines located at the upper and lower surface of the cells. c Cortex of internodal cells containing helical files of stationary chloroplasts (red autofluorescent) and FM1-43-stained charasomes (green fluorescent). Note absence of charasomes at the neutral line (NL). d Side view of charasomes (FM1-43-fluorescent) between chloroplasts (red autofluorescent). e The green fluorescent FM1-43-stained plasma membrane at the cross wall (arrow; optical cross-section) between a nodal (N) and an internodal cell (I) is smooth (compare with (d)). In the internodal cell charasomes are seen at the longitudinal wall and between the chloroplasts (empty spaces; asterisk). Plasmodesmata are out of focus. f Two intertwining basal protonema internodal cells (arrows). g Red fluorescent chloroplasts and green fluorescent, FM1-43-stained punctate charasomes in a basal protonema internodal cell. The arrow points to FM1-43-stained epiphytes. h Proximal internodal cells of rhizoids (arrows) after 2 weeks of exposure to light. i–k Charasomes in a proximal rhizoid internodal cell. CLSM image of FM1-43-stained fluorescent charasomes (i) between starch-containing chloroplasts visualized by DIC in the merged image (j). The electron micrograph (k) is a slightly tangential section showing charasomes (asterisks) along the cell wall (CW) and mitochondria (M). Bars = 1 mm (a, b, f, h), 20 μm (e, i, j), 10 μm (c, d, g), and 500 nm (k)
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Related In: Results  -  Collection

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Fig1: Thallus of Chara australis and charasomes in internodal cells. a Simplified schematic drawing of a Chara thallus. The apical cell (AC) gives rise to a regular series of cylindrical internodal cells (I) and groups of nodal cells (gray). Nodal cells may divide further and produce side branches (shoots of unlimited growth like that of the main axis; not shown) and branchlets (shoots of limited growth). Nodes incubated in darkness produce upward growing protonemata and downward growing rhizoids. Protonema and rhizoid internodal cells investigated in this study are marked by asterisks. Non-dividing cone-shaped cells are called stipulodes (long arrow) in nodes of the main axis or bract cells (short arrow) in nodes of branchlets. b Light micrograph of an internodal cell incubated in phenol red. Pink color indicates alkaline pH. The arrows point to the intersections of chloroplast-free neutral lines located at the upper and lower surface of the cells. c Cortex of internodal cells containing helical files of stationary chloroplasts (red autofluorescent) and FM1-43-stained charasomes (green fluorescent). Note absence of charasomes at the neutral line (NL). d Side view of charasomes (FM1-43-fluorescent) between chloroplasts (red autofluorescent). e The green fluorescent FM1-43-stained plasma membrane at the cross wall (arrow; optical cross-section) between a nodal (N) and an internodal cell (I) is smooth (compare with (d)). In the internodal cell charasomes are seen at the longitudinal wall and between the chloroplasts (empty spaces; asterisk). Plasmodesmata are out of focus. f Two intertwining basal protonema internodal cells (arrows). g Red fluorescent chloroplasts and green fluorescent, FM1-43-stained punctate charasomes in a basal protonema internodal cell. The arrow points to FM1-43-stained epiphytes. h Proximal internodal cells of rhizoids (arrows) after 2 weeks of exposure to light. i–k Charasomes in a proximal rhizoid internodal cell. CLSM image of FM1-43-stained fluorescent charasomes (i) between starch-containing chloroplasts visualized by DIC in the merged image (j). The electron micrograph (k) is a slightly tangential section showing charasomes (asterisks) along the cell wall (CW) and mitochondria (M). Bars = 1 mm (a, b, f, h), 20 μm (e, i, j), 10 μm (c, d, g), and 500 nm (k)
Mentions: The characean thallus consists of a regular series of long, cylindrical internodal cells and groups of small, isodiametric or flat nodal cells from which side branches (shoots with unlimited growth) and whorls of lateral cells (branchlets, shoots with limited growth) emerge (Fig. 1a) (Wood and Imahori 1965). Growth occurs by the ordered division of a dome-shaped apical cell, which sequentially produces the internodal and nodal cells. Sexual reproduction involves the germination of an oospore, which produces a positively gravitropic primary rhizoid and a negatively gravitropic, upward growing primary protonema from which a new thallus emerges. Secondary protonemata and secondary rhizoids arise from nodes isolated from the differentiated thallus and buried in the sediment (Braun and Limbach 2006; Hodick 1993).Fig. 1

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