Limits...
Two-dimensionality of yeast colony expansion accompanied by pattern formation.

Chen L, Noorbakhsh J, Adams RM, Samaniego-Evans J, Agollah G, Nevozhay D, Kuzdzal-Fick J, Mehta P, Balázsi G - PLoS Comput. Biol. (2014)

Bottom Line: Although the biochemical and molecular requirements for such patterns have been examined, the mechanisms underlying their formation are not entirely clear.Here we develop quantitative methods to accurately characterize the size, shape, and surface patterns of yeast colonies for various combinations of agar and sugar concentrations.We combine these measurements with mathematical and physical models and find that FLO11 gene constrains cells to grow near the agar surface, causing the formation of larger and more irregular colonies that undergo hierarchical wrinkling.

View Article: PubMed Central - PubMed

Affiliation: Department of Systems Biology, The University of Texas MD Anderson Cancer Center, Houston, Texas, United States of America.

ABSTRACT
Yeasts can form multicellular patterns as they expand on agar plates, a phenotype that requires a functional copy of the FLO11 gene. Although the biochemical and molecular requirements for such patterns have been examined, the mechanisms underlying their formation are not entirely clear. Here we develop quantitative methods to accurately characterize the size, shape, and surface patterns of yeast colonies for various combinations of agar and sugar concentrations. We combine these measurements with mathematical and physical models and find that FLO11 gene constrains cells to grow near the agar surface, causing the formation of larger and more irregular colonies that undergo hierarchical wrinkling. Head-to-head competition assays on agar plates indicate that two-dimensional constraint on the expansion of FLO11 wild type (FLO11) cells confers a fitness advantage over FLO11 knockout (flo11Δ) cells on the agar surface.

Show MeSH
FLO11-induced wrinkles on the colony surface.(A, D) Frozen blocks oriented across-spokes (blue box indicating estimated location) and radially (yellow box indicating estimated location) were cut from the FLO11 (A) or flo11Δ (D) S. cerevisiae colonies on 1.5% agar and 1.0% glucose YPD plates. The scale bar was 7500 µm. (B) Montage of the cryosections oriented across-spokes of a FLO11 colony (A) indicating wrinkles (red box) and spokes (green box). (C) Radial cryosectioning of the FLO11 colony (A). (E, F) Montage of the cryosections oriented across-spokes (E) or radially (F) for a flo11Δ colony (D). The scale bar (B, C, E, F) was 500 µm. (G) A schematic showing primary wrinkle formation (red dashed line), the saturation of which upon increasing stress leads to secondary wrinkle formation (green dashed line). The agar substrate on which the colony expands is shown in blue.
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4263361&req=5

pcbi-1003979-g003: FLO11-induced wrinkles on the colony surface.(A, D) Frozen blocks oriented across-spokes (blue box indicating estimated location) and radially (yellow box indicating estimated location) were cut from the FLO11 (A) or flo11Δ (D) S. cerevisiae colonies on 1.5% agar and 1.0% glucose YPD plates. The scale bar was 7500 µm. (B) Montage of the cryosections oriented across-spokes of a FLO11 colony (A) indicating wrinkles (red box) and spokes (green box). (C) Radial cryosectioning of the FLO11 colony (A). (E, F) Montage of the cryosections oriented across-spokes (E) or radially (F) for a flo11Δ colony (D). The scale bar (B, C, E, F) was 500 µm. (G) A schematic showing primary wrinkle formation (red dashed line), the saturation of which upon increasing stress leads to secondary wrinkle formation (green dashed line). The agar substrate on which the colony expands is shown in blue.

Mentions: The third characteristic we investigated was pattern formation on colony surfaces during expansion. Initial patterns on FLO11 colonies typically appeared as irregular wrinkles developing into a “hub”, a thickening mass of cells in the colony center. After a few days, as the colony expanded beyond the wrinkled hub, and radial wrinkles emerged, some bundled into thicker spoke-like structures. As the colony area increased, radial spokes appeared de novo between two existing spokes or by branching (S3 Movie), with apparently quasi-regular spacing (S3 Movie). In contrast, flo11Δ colonies appeared smooth, without any obvious surface patterns (Fig. 1B). Wrinkling was also observable on the vertical cross-sections of FLO11 (but not flo11Δ) colonies obtained by cryosectioning (Fig. 3A–F, S7 Figure).


Two-dimensionality of yeast colony expansion accompanied by pattern formation.

Chen L, Noorbakhsh J, Adams RM, Samaniego-Evans J, Agollah G, Nevozhay D, Kuzdzal-Fick J, Mehta P, Balázsi G - PLoS Comput. Biol. (2014)

FLO11-induced wrinkles on the colony surface.(A, D) Frozen blocks oriented across-spokes (blue box indicating estimated location) and radially (yellow box indicating estimated location) were cut from the FLO11 (A) or flo11Δ (D) S. cerevisiae colonies on 1.5% agar and 1.0% glucose YPD plates. The scale bar was 7500 µm. (B) Montage of the cryosections oriented across-spokes of a FLO11 colony (A) indicating wrinkles (red box) and spokes (green box). (C) Radial cryosectioning of the FLO11 colony (A). (E, F) Montage of the cryosections oriented across-spokes (E) or radially (F) for a flo11Δ colony (D). The scale bar (B, C, E, F) was 500 µm. (G) A schematic showing primary wrinkle formation (red dashed line), the saturation of which upon increasing stress leads to secondary wrinkle formation (green dashed line). The agar substrate on which the colony expands is shown in blue.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4263361&req=5

pcbi-1003979-g003: FLO11-induced wrinkles on the colony surface.(A, D) Frozen blocks oriented across-spokes (blue box indicating estimated location) and radially (yellow box indicating estimated location) were cut from the FLO11 (A) or flo11Δ (D) S. cerevisiae colonies on 1.5% agar and 1.0% glucose YPD plates. The scale bar was 7500 µm. (B) Montage of the cryosections oriented across-spokes of a FLO11 colony (A) indicating wrinkles (red box) and spokes (green box). (C) Radial cryosectioning of the FLO11 colony (A). (E, F) Montage of the cryosections oriented across-spokes (E) or radially (F) for a flo11Δ colony (D). The scale bar (B, C, E, F) was 500 µm. (G) A schematic showing primary wrinkle formation (red dashed line), the saturation of which upon increasing stress leads to secondary wrinkle formation (green dashed line). The agar substrate on which the colony expands is shown in blue.
Mentions: The third characteristic we investigated was pattern formation on colony surfaces during expansion. Initial patterns on FLO11 colonies typically appeared as irregular wrinkles developing into a “hub”, a thickening mass of cells in the colony center. After a few days, as the colony expanded beyond the wrinkled hub, and radial wrinkles emerged, some bundled into thicker spoke-like structures. As the colony area increased, radial spokes appeared de novo between two existing spokes or by branching (S3 Movie), with apparently quasi-regular spacing (S3 Movie). In contrast, flo11Δ colonies appeared smooth, without any obvious surface patterns (Fig. 1B). Wrinkling was also observable on the vertical cross-sections of FLO11 (but not flo11Δ) colonies obtained by cryosectioning (Fig. 3A–F, S7 Figure).

Bottom Line: Although the biochemical and molecular requirements for such patterns have been examined, the mechanisms underlying their formation are not entirely clear.Here we develop quantitative methods to accurately characterize the size, shape, and surface patterns of yeast colonies for various combinations of agar and sugar concentrations.We combine these measurements with mathematical and physical models and find that FLO11 gene constrains cells to grow near the agar surface, causing the formation of larger and more irregular colonies that undergo hierarchical wrinkling.

View Article: PubMed Central - PubMed

Affiliation: Department of Systems Biology, The University of Texas MD Anderson Cancer Center, Houston, Texas, United States of America.

ABSTRACT
Yeasts can form multicellular patterns as they expand on agar plates, a phenotype that requires a functional copy of the FLO11 gene. Although the biochemical and molecular requirements for such patterns have been examined, the mechanisms underlying their formation are not entirely clear. Here we develop quantitative methods to accurately characterize the size, shape, and surface patterns of yeast colonies for various combinations of agar and sugar concentrations. We combine these measurements with mathematical and physical models and find that FLO11 gene constrains cells to grow near the agar surface, causing the formation of larger and more irregular colonies that undergo hierarchical wrinkling. Head-to-head competition assays on agar plates indicate that two-dimensional constraint on the expansion of FLO11 wild type (FLO11) cells confers a fitness advantage over FLO11 knockout (flo11Δ) cells on the agar surface.

Show MeSH