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Mobility, microtubule nucleation and structure of microtubule-organizing centers in multinucleated hyphae of Ashbya gossypii.

Lang C, Grava S, van den Hoorn T, Trimble R, Philippsen P, Jaspersen SL - Mol. Biol. Cell (2009)

Bottom Line: This latter mode is sufficient to support wild-type-like hyphal growth speeds. cMT-dependent nuclear movements were led by a nuclear-associated microtubule-organizing center, the spindle pole body (SPB), which is the sole site of microtubule nucleation in A. gossypii.Analysis of A. gossypii SPBs by electron microscopy revealed an overall laminar structure similar to the budding yeast SPB but with distinct differences at the cytoplasmic side.Each SPB nucleates its own array of cMTs, and the lack of overlapping cMT arrays between neighboring nuclei explains the autonomous nuclear oscillations and bypassing observed in A. gossypii hyphae.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Microbiology, Biozentrum University of Basel, 4056 Basel, Switzerland.

ABSTRACT
We investigated the migration of multiple nuclei in hyphae of the filamentous fungus Ashbya gossypii. Three types of cytoplasmic microtubule (cMT)-dependent nuclear movements were characterized using live cell imaging: short-range oscillations (up to 4.5 microm/min), rotations (up to 180 degrees in 30 s), and long-range nuclear bypassing (up to 9 microm/min). These movements were superimposed on a cMT-independent mode of nuclear migration, cotransport with the cytoplasmic stream. This latter mode is sufficient to support wild-type-like hyphal growth speeds. cMT-dependent nuclear movements were led by a nuclear-associated microtubule-organizing center, the spindle pole body (SPB), which is the sole site of microtubule nucleation in A. gossypii. Analysis of A. gossypii SPBs by electron microscopy revealed an overall laminar structure similar to the budding yeast SPB but with distinct differences at the cytoplasmic side. Up to six perpendicular and tangential cMTs emanated from a more spherical outer plaque. The perpendicular and tangential cMTs most likely correspond to short, often cortex-associated cMTs and to long, hyphal growth-axis-oriented cMTs, respectively, seen by in vivo imaging. Each SPB nucleates its own array of cMTs, and the lack of overlapping cMT arrays between neighboring nuclei explains the autonomous nuclear oscillations and bypassing observed in A. gossypii hyphae.

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Comparison of A. gossypii and S. cerevisiae SPB structure based on EM analysis. (A) Schematic depicting the S. cerevisiae and A. gossypii SPB layers and distances between SPB layers. Although the CP and IL2 are similar in size and structure in A. gossypii and S. cerevisiae, the IL1 and OP of A. gossypii are considerably smaller and the spacing between those layers is increased compared with budding yeast. The A. gossypii OP appears amorphous rather than electron dense like in S. cerevisiae. (B) Quantitation of distances between A. gossypii SPB layers with SD and number of plaques used for the measurements. The data for S. cerevisiae SPB plaques were compiled from published work (Byers and Goetsch, 1974; Bullitt et al., 1997; O'Toole et al., 1999; Schaerer et al., 2001).
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Figure 7: Comparison of A. gossypii and S. cerevisiae SPB structure based on EM analysis. (A) Schematic depicting the S. cerevisiae and A. gossypii SPB layers and distances between SPB layers. Although the CP and IL2 are similar in size and structure in A. gossypii and S. cerevisiae, the IL1 and OP of A. gossypii are considerably smaller and the spacing between those layers is increased compared with budding yeast. The A. gossypii OP appears amorphous rather than electron dense like in S. cerevisiae. (B) Quantitation of distances between A. gossypii SPB layers with SD and number of plaques used for the measurements. The data for S. cerevisiae SPB plaques were compiled from published work (Byers and Goetsch, 1974; Bullitt et al., 1997; O'Toole et al., 1999; Schaerer et al., 2001).

Mentions: Even though the general structure of the A. gossypii SPB is similar to that of S. cerevisiae, careful analysis of the size and spacing between A. gossypii SPB layers revealed distinct differences compared with budding yeast SPBs. One of the most notable features of A. gossypii SPBs is the distance between the OP and IL2, which is ∼25 nm greater than it is in S. cerevisiae. There is also a slight increase in the spacing between IL2 and IL1, whereas the distance between the remaining plaques is equivalent (Figure 7). A second major distinction is the shape of the OP. In A. gossypii, the OP does not form a distinctive plaque but rather appears as an amorphous sphere with a diameter significantly reduced compared with the other layers of the SPB (Figure 7). These features result in a considerable degree of variability in the height measurement of the A. gossypii SPBs (Figure 7).


Mobility, microtubule nucleation and structure of microtubule-organizing centers in multinucleated hyphae of Ashbya gossypii.

Lang C, Grava S, van den Hoorn T, Trimble R, Philippsen P, Jaspersen SL - Mol. Biol. Cell (2009)

Comparison of A. gossypii and S. cerevisiae SPB structure based on EM analysis. (A) Schematic depicting the S. cerevisiae and A. gossypii SPB layers and distances between SPB layers. Although the CP and IL2 are similar in size and structure in A. gossypii and S. cerevisiae, the IL1 and OP of A. gossypii are considerably smaller and the spacing between those layers is increased compared with budding yeast. The A. gossypii OP appears amorphous rather than electron dense like in S. cerevisiae. (B) Quantitation of distances between A. gossypii SPB layers with SD and number of plaques used for the measurements. The data for S. cerevisiae SPB plaques were compiled from published work (Byers and Goetsch, 1974; Bullitt et al., 1997; O'Toole et al., 1999; Schaerer et al., 2001).
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Related In: Results  -  Collection

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Figure 7: Comparison of A. gossypii and S. cerevisiae SPB structure based on EM analysis. (A) Schematic depicting the S. cerevisiae and A. gossypii SPB layers and distances between SPB layers. Although the CP and IL2 are similar in size and structure in A. gossypii and S. cerevisiae, the IL1 and OP of A. gossypii are considerably smaller and the spacing between those layers is increased compared with budding yeast. The A. gossypii OP appears amorphous rather than electron dense like in S. cerevisiae. (B) Quantitation of distances between A. gossypii SPB layers with SD and number of plaques used for the measurements. The data for S. cerevisiae SPB plaques were compiled from published work (Byers and Goetsch, 1974; Bullitt et al., 1997; O'Toole et al., 1999; Schaerer et al., 2001).
Mentions: Even though the general structure of the A. gossypii SPB is similar to that of S. cerevisiae, careful analysis of the size and spacing between A. gossypii SPB layers revealed distinct differences compared with budding yeast SPBs. One of the most notable features of A. gossypii SPBs is the distance between the OP and IL2, which is ∼25 nm greater than it is in S. cerevisiae. There is also a slight increase in the spacing between IL2 and IL1, whereas the distance between the remaining plaques is equivalent (Figure 7). A second major distinction is the shape of the OP. In A. gossypii, the OP does not form a distinctive plaque but rather appears as an amorphous sphere with a diameter significantly reduced compared with the other layers of the SPB (Figure 7). These features result in a considerable degree of variability in the height measurement of the A. gossypii SPBs (Figure 7).

Bottom Line: This latter mode is sufficient to support wild-type-like hyphal growth speeds. cMT-dependent nuclear movements were led by a nuclear-associated microtubule-organizing center, the spindle pole body (SPB), which is the sole site of microtubule nucleation in A. gossypii.Analysis of A. gossypii SPBs by electron microscopy revealed an overall laminar structure similar to the budding yeast SPB but with distinct differences at the cytoplasmic side.Each SPB nucleates its own array of cMTs, and the lack of overlapping cMT arrays between neighboring nuclei explains the autonomous nuclear oscillations and bypassing observed in A. gossypii hyphae.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Microbiology, Biozentrum University of Basel, 4056 Basel, Switzerland.

ABSTRACT
We investigated the migration of multiple nuclei in hyphae of the filamentous fungus Ashbya gossypii. Three types of cytoplasmic microtubule (cMT)-dependent nuclear movements were characterized using live cell imaging: short-range oscillations (up to 4.5 microm/min), rotations (up to 180 degrees in 30 s), and long-range nuclear bypassing (up to 9 microm/min). These movements were superimposed on a cMT-independent mode of nuclear migration, cotransport with the cytoplasmic stream. This latter mode is sufficient to support wild-type-like hyphal growth speeds. cMT-dependent nuclear movements were led by a nuclear-associated microtubule-organizing center, the spindle pole body (SPB), which is the sole site of microtubule nucleation in A. gossypii. Analysis of A. gossypii SPBs by electron microscopy revealed an overall laminar structure similar to the budding yeast SPB but with distinct differences at the cytoplasmic side. Up to six perpendicular and tangential cMTs emanated from a more spherical outer plaque. The perpendicular and tangential cMTs most likely correspond to short, often cortex-associated cMTs and to long, hyphal growth-axis-oriented cMTs, respectively, seen by in vivo imaging. Each SPB nucleates its own array of cMTs, and the lack of overlapping cMT arrays between neighboring nuclei explains the autonomous nuclear oscillations and bypassing observed in A. gossypii hyphae.

Show MeSH
Related in: MedlinePlus