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
Pattern forming FLO11 S. cerevisiae cells out-expand flo11Δ cells during head-to-head competition.(A, B, C) Schematic showing the range expansion of mixed populations segregated into sectors with constant or gradually changing sector angles along the radius due to fitness differences between the particular sector and the adjacent sectors. (A): Neither population has advantage. (B): Unlabeled population has advantage. (C): Red-labeled population has advantage. (D, E) A small competitive advantage of unlabeled cells is observed between isogenic cells of unlabeled and mCherry-labeled flo11Δ cells. (F, G) A small competitive advantage of unlabeled cells is observed between unlabeled and mCherry labeled FLO11 cells. (H, I) Unlabeled FLO11 cells out-expanded mCherry-labeled flo11Δ cells with a conspicuous increase in the unlabeled sector angle, in comparison to minimal competition between isogenic cells (see below). (J, K) Reverse labeling of (H, I) showed that mCherry-labeled FLO11 cells overtook the mixed colonies after some time, despite of the initial lack of expansion advantage against unlabeled flo11Δ cells. Bright field (D, F, H, J) and mCherry (E, G, I, K) were shown respectively. Contrast is adjusted in Adobe Photoshop CS for mCherry images. All cells were grown on 1.0% agar, 0.5% galactose YPGal plates.
© Copyright Policy
Related In: Results  -  Collection

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

pcbi-1003979-g005: Pattern forming FLO11 S. cerevisiae cells out-expand flo11Δ cells during head-to-head competition.(A, B, C) Schematic showing the range expansion of mixed populations segregated into sectors with constant or gradually changing sector angles along the radius due to fitness differences between the particular sector and the adjacent sectors. (A): Neither population has advantage. (B): Unlabeled population has advantage. (C): Red-labeled population has advantage. (D, E) A small competitive advantage of unlabeled cells is observed between isogenic cells of unlabeled and mCherry-labeled flo11Δ cells. (F, G) A small competitive advantage of unlabeled cells is observed between unlabeled and mCherry labeled FLO11 cells. (H, I) Unlabeled FLO11 cells out-expanded mCherry-labeled flo11Δ cells with a conspicuous increase in the unlabeled sector angle, in comparison to minimal competition between isogenic cells (see below). (J, K) Reverse labeling of (H, I) showed that mCherry-labeled FLO11 cells overtook the mixed colonies after some time, despite of the initial lack of expansion advantage against unlabeled flo11Δ cells. Bright field (D, F, H, J) and mCherry (E, G, I, K) were shown respectively. Contrast is adjusted in Adobe Photoshop CS for mCherry images. All cells were grown on 1.0% agar, 0.5% galactose YPGal plates.

Mentions: Previously, Korolev and colleagues [43] showed that two differently labeled S. cerevisiae cell types should segregate into single-colored sectors as initial spatial non-homogeneities amplify through a “founder effect” during colony expansion. The boundaries of such single-colored sectors should reveal any competitive advantage between the two cell types (or lack thereof). Specifically, straight sector boundaries indicate that sectors occupy approximately the same arc-angle θ(r) around the colony's periphery over time (Fig. 5A), meaning that neither cell type has competitive advantage over the other. However, if the sector boundaries occupied by unlabeled cells curve outwards then their arc-angle θ(r) increases at the expense of the arc-angle occupied by the mCherry-labeled cells, meaning that the unlabeled cells have a competitive advantage (Fig. 5B). The opposite is true if the unlabeled sector boundaries curve inward (Fig. 5C).


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)

Pattern forming FLO11 S. cerevisiae cells out-expand flo11Δ cells during head-to-head competition.(A, B, C) Schematic showing the range expansion of mixed populations segregated into sectors with constant or gradually changing sector angles along the radius due to fitness differences between the particular sector and the adjacent sectors. (A): Neither population has advantage. (B): Unlabeled population has advantage. (C): Red-labeled population has advantage. (D, E) A small competitive advantage of unlabeled cells is observed between isogenic cells of unlabeled and mCherry-labeled flo11Δ cells. (F, G) A small competitive advantage of unlabeled cells is observed between unlabeled and mCherry labeled FLO11 cells. (H, I) Unlabeled FLO11 cells out-expanded mCherry-labeled flo11Δ cells with a conspicuous increase in the unlabeled sector angle, in comparison to minimal competition between isogenic cells (see below). (J, K) Reverse labeling of (H, I) showed that mCherry-labeled FLO11 cells overtook the mixed colonies after some time, despite of the initial lack of expansion advantage against unlabeled flo11Δ cells. Bright field (D, F, H, J) and mCherry (E, G, I, K) were shown respectively. Contrast is adjusted in Adobe Photoshop CS for mCherry images. All cells were grown on 1.0% agar, 0.5% galactose YPGal plates.
© Copyright Policy
Related In: Results  -  Collection

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

pcbi-1003979-g005: Pattern forming FLO11 S. cerevisiae cells out-expand flo11Δ cells during head-to-head competition.(A, B, C) Schematic showing the range expansion of mixed populations segregated into sectors with constant or gradually changing sector angles along the radius due to fitness differences between the particular sector and the adjacent sectors. (A): Neither population has advantage. (B): Unlabeled population has advantage. (C): Red-labeled population has advantage. (D, E) A small competitive advantage of unlabeled cells is observed between isogenic cells of unlabeled and mCherry-labeled flo11Δ cells. (F, G) A small competitive advantage of unlabeled cells is observed between unlabeled and mCherry labeled FLO11 cells. (H, I) Unlabeled FLO11 cells out-expanded mCherry-labeled flo11Δ cells with a conspicuous increase in the unlabeled sector angle, in comparison to minimal competition between isogenic cells (see below). (J, K) Reverse labeling of (H, I) showed that mCherry-labeled FLO11 cells overtook the mixed colonies after some time, despite of the initial lack of expansion advantage against unlabeled flo11Δ cells. Bright field (D, F, H, J) and mCherry (E, G, I, K) were shown respectively. Contrast is adjusted in Adobe Photoshop CS for mCherry images. All cells were grown on 1.0% agar, 0.5% galactose YPGal plates.
Mentions: Previously, Korolev and colleagues [43] showed that two differently labeled S. cerevisiae cell types should segregate into single-colored sectors as initial spatial non-homogeneities amplify through a “founder effect” during colony expansion. The boundaries of such single-colored sectors should reveal any competitive advantage between the two cell types (or lack thereof). Specifically, straight sector boundaries indicate that sectors occupy approximately the same arc-angle θ(r) around the colony's periphery over time (Fig. 5A), meaning that neither cell type has competitive advantage over the other. However, if the sector boundaries occupied by unlabeled cells curve outwards then their arc-angle θ(r) increases at the expense of the arc-angle occupied by the mCherry-labeled cells, meaning that the unlabeled cells have a competitive advantage (Fig. 5B). The opposite is true if the unlabeled sector boundaries curve inward (Fig. 5C).

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