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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.

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Colony size and irregularity for various glucose and agar concentrations.(A, B) Images of FLO11 (A) and flo11Δ (B) on YPD plates containing different glucose (0.5%, 1.0%, 2.0%) and agar (1.5%, 3.0%, 6.0%) concentrations around day 20. (C, D) The expansion of colony area (C) and the irregularity (D) of FLO11 (red curves) and flo11Δ (green curves) colonies over the 60-day time course. FLO11 colonies (red curves) demonstrated higher maximum colony size (C) with higher irregularity (D) at the colony rim than the flo11Δ colonies (green curves) in all conditions tested. The maximum colony size (C) of both FLO11 (red curves) and flo11Δ (green curves) colonies increased with glucose and inversely depended on agar concentrations. The irregularity of FLO11 (D) (red curves) inversely depended on both the agar and the glucose concentrations, compared to the minimal irregularity of flo11Δ (D) (green curves) colonies throughout the time course at all conditions tested. Thinner curves represent different replicates while thicker curves represent their average up until all the replicates were present.
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pcbi-1003979-g001: Colony size and irregularity for various glucose and agar concentrations.(A, B) Images of FLO11 (A) and flo11Δ (B) on YPD plates containing different glucose (0.5%, 1.0%, 2.0%) and agar (1.5%, 3.0%, 6.0%) concentrations around day 20. (C, D) The expansion of colony area (C) and the irregularity (D) of FLO11 (red curves) and flo11Δ (green curves) colonies over the 60-day time course. FLO11 colonies (red curves) demonstrated higher maximum colony size (C) with higher irregularity (D) at the colony rim than the flo11Δ colonies (green curves) in all conditions tested. The maximum colony size (C) of both FLO11 (red curves) and flo11Δ (green curves) colonies increased with glucose and inversely depended on agar concentrations. The irregularity of FLO11 (D) (red curves) inversely depended on both the agar and the glucose concentrations, compared to the minimal irregularity of flo11Δ (D) (green curves) colonies throughout the time course at all conditions tested. Thinner curves represent different replicates while thicker curves represent their average up until all the replicates were present.

Mentions: We first asked how the presence of a functional FLO11 gene influenced colony expansion under various nutrient conditions, as previously done in bacteria [31]. To address this question, we applied automated image segmentation followed by pixel counting [32] to obtain the area of FLO11 and flo11Δ colonies that expanded under nine different combinations of agar (1.5%, 3.0%, 6.0%) and glucose (0.5%, 1.0%, 2.0%) concentrations on Yeast Extract-Peptone-Dextrose (YPD) agar plates. We found that FLO11 colonies (Fig. 1A, C) expanded faster than flo11Δ colonies (Fig. 1B, C) and reached larger maximum size in all of these conditions, in agreement with previous observations in soft agar [18]. The maximum colony area increased with glucose concentration, but had an inverse dependence on agar density, regardless of FLO11 status (Fig. 1C, S1A, B Figure). The time that colonies took to reach their maximum area increased with agar density, with no obvious dependence on glucose concentration, regardless of FLO11 status (S1E, F Figure). Time derivative of the experimentally measured FLO11 colony area indicated that the colony expansion curve convexity increased with glucose concentration (S2 Figure). These trends of colony expansion were independent of the sugar type, as suggested by similar trends obtained for agar with galactose (S3 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)

Colony size and irregularity for various glucose and agar concentrations.(A, B) Images of FLO11 (A) and flo11Δ (B) on YPD plates containing different glucose (0.5%, 1.0%, 2.0%) and agar (1.5%, 3.0%, 6.0%) concentrations around day 20. (C, D) The expansion of colony area (C) and the irregularity (D) of FLO11 (red curves) and flo11Δ (green curves) colonies over the 60-day time course. FLO11 colonies (red curves) demonstrated higher maximum colony size (C) with higher irregularity (D) at the colony rim than the flo11Δ colonies (green curves) in all conditions tested. The maximum colony size (C) of both FLO11 (red curves) and flo11Δ (green curves) colonies increased with glucose and inversely depended on agar concentrations. The irregularity of FLO11 (D) (red curves) inversely depended on both the agar and the glucose concentrations, compared to the minimal irregularity of flo11Δ (D) (green curves) colonies throughout the time course at all conditions tested. Thinner curves represent different replicates while thicker curves represent their average up until all the replicates were present.
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Related In: Results  -  Collection

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pcbi-1003979-g001: Colony size and irregularity for various glucose and agar concentrations.(A, B) Images of FLO11 (A) and flo11Δ (B) on YPD plates containing different glucose (0.5%, 1.0%, 2.0%) and agar (1.5%, 3.0%, 6.0%) concentrations around day 20. (C, D) The expansion of colony area (C) and the irregularity (D) of FLO11 (red curves) and flo11Δ (green curves) colonies over the 60-day time course. FLO11 colonies (red curves) demonstrated higher maximum colony size (C) with higher irregularity (D) at the colony rim than the flo11Δ colonies (green curves) in all conditions tested. The maximum colony size (C) of both FLO11 (red curves) and flo11Δ (green curves) colonies increased with glucose and inversely depended on agar concentrations. The irregularity of FLO11 (D) (red curves) inversely depended on both the agar and the glucose concentrations, compared to the minimal irregularity of flo11Δ (D) (green curves) colonies throughout the time course at all conditions tested. Thinner curves represent different replicates while thicker curves represent their average up until all the replicates were present.
Mentions: We first asked how the presence of a functional FLO11 gene influenced colony expansion under various nutrient conditions, as previously done in bacteria [31]. To address this question, we applied automated image segmentation followed by pixel counting [32] to obtain the area of FLO11 and flo11Δ colonies that expanded under nine different combinations of agar (1.5%, 3.0%, 6.0%) and glucose (0.5%, 1.0%, 2.0%) concentrations on Yeast Extract-Peptone-Dextrose (YPD) agar plates. We found that FLO11 colonies (Fig. 1A, C) expanded faster than flo11Δ colonies (Fig. 1B, C) and reached larger maximum size in all of these conditions, in agreement with previous observations in soft agar [18]. The maximum colony area increased with glucose concentration, but had an inverse dependence on agar density, regardless of FLO11 status (Fig. 1C, S1A, B Figure). The time that colonies took to reach their maximum area increased with agar density, with no obvious dependence on glucose concentration, regardless of FLO11 status (S1E, F Figure). Time derivative of the experimentally measured FLO11 colony area indicated that the colony expansion curve convexity increased with glucose concentration (S2 Figure). These trends of colony expansion were independent of the sugar type, as suggested by similar trends obtained for agar with galactose (S3 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.

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