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The dynamics of the actin cytoskeleton during sporogenesis in Psilotum nudum L.

Tchórzewska D, Bednara J - Protoplasma (2010)

Bottom Line: Moreover, in telophase I F-actin filaments formed short-lived phragmoplast, which was adjacent to the plasma membrane, exactly at the site of future cell wall formation.Changes were observed that occurred in the cytochalasin-treated cells: the daughter nuclei were located abnormally close to each other, there was no formation of the equatorial plate of organelles and, consequently, meiosis did not occur normally.It seems possible that, if the actin cytoskeleton only is damaged, regular cytokinesis will not occur and, hence, no viable spores will be produced.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Anatomy and Cytology, Maria Curie-Skłodowska University, Akademicka 19, 20-033, Lublin, Poland. dorota.tchorzewska@poczta.umcs.lublin.pl

ABSTRACT
The actin cytoskeleton (microfilaments, MFs) accompanies the tubulin cytoskeleton (microtubules) during the meiotic division of the cell, but knowledge about the scope of their physiological competence and cooperation is insufficient. To cast more light on this issue, we analysed the F-actin distribution during the meiotic division of the Psilotum nudum sporocytes. Unfixed sporangia of P. nudum were stained with rhodamine-phalloidin and 4',6-diamidino-2-phenylindole dihydrochloride, and we monitored the changes in the actin cytoskeleton and nuclear chromatin throughout sporogenesis. We observed that the actin cytoskeleton in meiotically dividing cells is not only part of the kariokinetic spindle and phragmoplast but it also forms a well-developed network in the cytoplasm present in all phases of meiosis. Moreover, in telophase I F-actin filaments formed short-lived phragmoplast, which was adjacent to the plasma membrane, exactly at the site of future cell wall formation. Additionally, the meiocytes were pre-treated with cytochalasin-B at a concentration that causes damage to the MFs. This facilitated observation of the effect of selective MFs damage on the course of meiosis and sporogenesis of P. nudum. Changes were observed that occurred in the cytochalasin-treated cells: the daughter nuclei were located abnormally close to each other, there was no formation of the equatorial plate of organelles and, consequently, meiosis did not occur normally. It seems possible that, if the actin cytoskeleton only is damaged, regular cytokinesis will not occur and, hence, no viable spores will be produced.

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17 Sporocytes of P. nudum treated with cytochalasin-B. MFs stained with rhodamine-phalloidin. Nuclear and organellar DNA stained with DAPI. a, b Prophase I. a F-actin has a form of only short fragments dispersed in the cytoplasm. b The nuclear chromatin is highly condensed. 18 Sporocytes of P. nudum treated with cytochalasin-B. MFs stained with rhodamine-phalloidin. Nuclear and organellar DNA stained with DAPI. a, b telophase I. a MFs as short bundles; slightly longer fragments are visible only at the borders of the nuclei. b Two lens-shaped nuclei are visible at the two cell poles. 19 Sporocytes of P. nudum treated with cytochalasin-B. MFs stained with rhodamine-phalloidin. Nuclear and organellar DNA stained with DAPI. a, b Early telophase II. a Short branching fragments of MFs arranged in a non-directional mode can be seen in the cytoplasm. b Three out of the four daughter nuclei and cell organelles are dispersed in the cytoplasm. 20 Sporocytes of P. nudum treated with cytochalasin-B. MFs stained with rhodamine-phalloidin. Nuclear and organellar DNA stained with DAPI. a, b Telophase II. a Shorter and less regularly arranged MFs form a phragmoplast-like network. b Four nuclei and nucleoids of the cell organelles dispersed in the cytoplasm are visible
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Fig4: 17 Sporocytes of P. nudum treated with cytochalasin-B. MFs stained with rhodamine-phalloidin. Nuclear and organellar DNA stained with DAPI. a, b Prophase I. a F-actin has a form of only short fragments dispersed in the cytoplasm. b The nuclear chromatin is highly condensed. 18 Sporocytes of P. nudum treated with cytochalasin-B. MFs stained with rhodamine-phalloidin. Nuclear and organellar DNA stained with DAPI. a, b telophase I. a MFs as short bundles; slightly longer fragments are visible only at the borders of the nuclei. b Two lens-shaped nuclei are visible at the two cell poles. 19 Sporocytes of P. nudum treated with cytochalasin-B. MFs stained with rhodamine-phalloidin. Nuclear and organellar DNA stained with DAPI. a, b Early telophase II. a Short branching fragments of MFs arranged in a non-directional mode can be seen in the cytoplasm. b Three out of the four daughter nuclei and cell organelles are dispersed in the cytoplasm. 20 Sporocytes of P. nudum treated with cytochalasin-B. MFs stained with rhodamine-phalloidin. Nuclear and organellar DNA stained with DAPI. a, b Telophase II. a Shorter and less regularly arranged MFs form a phragmoplast-like network. b Four nuclei and nucleoids of the cell organelles dispersed in the cytoplasm are visible

Mentions: Treatment of P. nudum meiocytes with cytochalasin-B during sporogenesis resulted in damage to the actin cytoskeleton which involved both inhibition of polymerisation and partial degradation of the existing microfilaments. In prophase meiocytes treated with cytochalasin-B, F-actin was present in the form of short fragments arrayed in a characteristic network in the cytoplasm (17a of Fig. 4). The actin cytoskeleton had this configuration, for instance, in the late prophase I, where chromatin in the cell nuclei was strongly condensed and formed bivalents (17b of Fig. 4). The meiotic cells treated with cytochalasin at the initial stage of telophase I displayed a bundle-shaped actin cytoskeleton; however, the short bundles did not form a typical phragmoplast. Slightly longer microfilament fragments were only visible at the border of the nuclei (18a of Fig. 4). In the DAPI-stained cells at this stage, two kidney-shaped nuclei located at the two cell poles were seen (18b of Fig. 4). Meiocytes treated with cytochalasin-B at a later stage, e.g. at the beginning of telophase II, had short, crossed microfilaments that were non-directionally distributed in the cytoplasm and did not resemble a phragmoplast (19a of Fig. 4). After DAPI staining, newly formed cell nuclei and nucleoids of the organelles were evenly dispersed both in the proximal and peripheral cytoplasm (19b of Fig. 4). In some telophase cells, the microfilaments formed a network that was slightly similar to a phragmoplast, but the filament bundles were distinctly shorter and less regularly arrayed than in the control, i.e. they did not display the typical parallel filament arrangement (20a of Fig. 4). In such cells, DAPI staining showed four nuclei and cell organelles which were chaotically dispersed in the cytoplasm and did not form equatorial plates (20b of Fig. 4).Fig. 4


The dynamics of the actin cytoskeleton during sporogenesis in Psilotum nudum L.

Tchórzewska D, Bednara J - Protoplasma (2010)

17 Sporocytes of P. nudum treated with cytochalasin-B. MFs stained with rhodamine-phalloidin. Nuclear and organellar DNA stained with DAPI. a, b Prophase I. a F-actin has a form of only short fragments dispersed in the cytoplasm. b The nuclear chromatin is highly condensed. 18 Sporocytes of P. nudum treated with cytochalasin-B. MFs stained with rhodamine-phalloidin. Nuclear and organellar DNA stained with DAPI. a, b telophase I. a MFs as short bundles; slightly longer fragments are visible only at the borders of the nuclei. b Two lens-shaped nuclei are visible at the two cell poles. 19 Sporocytes of P. nudum treated with cytochalasin-B. MFs stained with rhodamine-phalloidin. Nuclear and organellar DNA stained with DAPI. a, b Early telophase II. a Short branching fragments of MFs arranged in a non-directional mode can be seen in the cytoplasm. b Three out of the four daughter nuclei and cell organelles are dispersed in the cytoplasm. 20 Sporocytes of P. nudum treated with cytochalasin-B. MFs stained with rhodamine-phalloidin. Nuclear and organellar DNA stained with DAPI. a, b Telophase II. a Shorter and less regularly arranged MFs form a phragmoplast-like network. b Four nuclei and nucleoids of the cell organelles dispersed in the cytoplasm are visible
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Fig4: 17 Sporocytes of P. nudum treated with cytochalasin-B. MFs stained with rhodamine-phalloidin. Nuclear and organellar DNA stained with DAPI. a, b Prophase I. a F-actin has a form of only short fragments dispersed in the cytoplasm. b The nuclear chromatin is highly condensed. 18 Sporocytes of P. nudum treated with cytochalasin-B. MFs stained with rhodamine-phalloidin. Nuclear and organellar DNA stained with DAPI. a, b telophase I. a MFs as short bundles; slightly longer fragments are visible only at the borders of the nuclei. b Two lens-shaped nuclei are visible at the two cell poles. 19 Sporocytes of P. nudum treated with cytochalasin-B. MFs stained with rhodamine-phalloidin. Nuclear and organellar DNA stained with DAPI. a, b Early telophase II. a Short branching fragments of MFs arranged in a non-directional mode can be seen in the cytoplasm. b Three out of the four daughter nuclei and cell organelles are dispersed in the cytoplasm. 20 Sporocytes of P. nudum treated with cytochalasin-B. MFs stained with rhodamine-phalloidin. Nuclear and organellar DNA stained with DAPI. a, b Telophase II. a Shorter and less regularly arranged MFs form a phragmoplast-like network. b Four nuclei and nucleoids of the cell organelles dispersed in the cytoplasm are visible
Mentions: Treatment of P. nudum meiocytes with cytochalasin-B during sporogenesis resulted in damage to the actin cytoskeleton which involved both inhibition of polymerisation and partial degradation of the existing microfilaments. In prophase meiocytes treated with cytochalasin-B, F-actin was present in the form of short fragments arrayed in a characteristic network in the cytoplasm (17a of Fig. 4). The actin cytoskeleton had this configuration, for instance, in the late prophase I, where chromatin in the cell nuclei was strongly condensed and formed bivalents (17b of Fig. 4). The meiotic cells treated with cytochalasin at the initial stage of telophase I displayed a bundle-shaped actin cytoskeleton; however, the short bundles did not form a typical phragmoplast. Slightly longer microfilament fragments were only visible at the border of the nuclei (18a of Fig. 4). In the DAPI-stained cells at this stage, two kidney-shaped nuclei located at the two cell poles were seen (18b of Fig. 4). Meiocytes treated with cytochalasin-B at a later stage, e.g. at the beginning of telophase II, had short, crossed microfilaments that were non-directionally distributed in the cytoplasm and did not resemble a phragmoplast (19a of Fig. 4). After DAPI staining, newly formed cell nuclei and nucleoids of the organelles were evenly dispersed both in the proximal and peripheral cytoplasm (19b of Fig. 4). In some telophase cells, the microfilaments formed a network that was slightly similar to a phragmoplast, but the filament bundles were distinctly shorter and less regularly arrayed than in the control, i.e. they did not display the typical parallel filament arrangement (20a of Fig. 4). In such cells, DAPI staining showed four nuclei and cell organelles which were chaotically dispersed in the cytoplasm and did not form equatorial plates (20b of Fig. 4).Fig. 4

Bottom Line: Moreover, in telophase I F-actin filaments formed short-lived phragmoplast, which was adjacent to the plasma membrane, exactly at the site of future cell wall formation.Changes were observed that occurred in the cytochalasin-treated cells: the daughter nuclei were located abnormally close to each other, there was no formation of the equatorial plate of organelles and, consequently, meiosis did not occur normally.It seems possible that, if the actin cytoskeleton only is damaged, regular cytokinesis will not occur and, hence, no viable spores will be produced.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Anatomy and Cytology, Maria Curie-Skłodowska University, Akademicka 19, 20-033, Lublin, Poland. dorota.tchorzewska@poczta.umcs.lublin.pl

ABSTRACT
The actin cytoskeleton (microfilaments, MFs) accompanies the tubulin cytoskeleton (microtubules) during the meiotic division of the cell, but knowledge about the scope of their physiological competence and cooperation is insufficient. To cast more light on this issue, we analysed the F-actin distribution during the meiotic division of the Psilotum nudum sporocytes. Unfixed sporangia of P. nudum were stained with rhodamine-phalloidin and 4',6-diamidino-2-phenylindole dihydrochloride, and we monitored the changes in the actin cytoskeleton and nuclear chromatin throughout sporogenesis. We observed that the actin cytoskeleton in meiotically dividing cells is not only part of the kariokinetic spindle and phragmoplast but it also forms a well-developed network in the cytoplasm present in all phases of meiosis. Moreover, in telophase I F-actin filaments formed short-lived phragmoplast, which was adjacent to the plasma membrane, exactly at the site of future cell wall formation. Additionally, the meiocytes were pre-treated with cytochalasin-B at a concentration that causes damage to the MFs. This facilitated observation of the effect of selective MFs damage on the course of meiosis and sporogenesis of P. nudum. Changes were observed that occurred in the cytochalasin-treated cells: the daughter nuclei were located abnormally close to each other, there was no formation of the equatorial plate of organelles and, consequently, meiosis did not occur normally. It seems possible that, if the actin cytoskeleton only is damaged, regular cytokinesis will not occur and, hence, no viable spores will be produced.

Show MeSH
Related in: MedlinePlus