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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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Analysis of the wavelengths of the colony surface patterns.(A) The wavelength of spokes (2) measured manually and by Fast Fourier Transformation (FFT) decreased with increasing agar density, while the wavelength of primary wrinkles (1) from manual measurements were less sensitive to the change of agar density. Since the automated FFT measurement was sensitive to noise in the image, FFT did not detect the small-wavelength primary wrinkles as significant. The wavelength of the wrinkles was shorter than that of the spokes at all agar levels tested. The experimentally measured geometric mean wavelength of spokes matched best the ESVS thick substrate model, while the geometric mean wavelength of primary wrinkles matched the ESVS thin substrate model. The inserted image shows the primary and secondary wrinkles measured at the outer radii, indicated by red and green lines, respectively. (B) The Fourier wavelengths plotted as a function of section radius, independent of time for FLO11 colony at 0.5% glucose and 0.9% agar. (C) Same as (B), but for a flo11Δ colony at 0.5% glucose and 0.9% agar. Each dot (C, D) represented a colony from a replicate and a time point. (D) The percent of significant points (Fourier spectral peak height>1.5) plotted as a function of agar. The cell type (FLO11 or flo11Δ) is indicated in white font inside the circles.
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pcbi-1003979-g004: Analysis of the wavelengths of the colony surface patterns.(A) The wavelength of spokes (2) measured manually and by Fast Fourier Transformation (FFT) decreased with increasing agar density, while the wavelength of primary wrinkles (1) from manual measurements were less sensitive to the change of agar density. Since the automated FFT measurement was sensitive to noise in the image, FFT did not detect the small-wavelength primary wrinkles as significant. The wavelength of the wrinkles was shorter than that of the spokes at all agar levels tested. The experimentally measured geometric mean wavelength of spokes matched best the ESVS thick substrate model, while the geometric mean wavelength of primary wrinkles matched the ESVS thin substrate model. The inserted image shows the primary and secondary wrinkles measured at the outer radii, indicated by red and green lines, respectively. (B) The Fourier wavelengths plotted as a function of section radius, independent of time for FLO11 colony at 0.5% glucose and 0.9% agar. (C) Same as (B), but for a flo11Δ colony at 0.5% glucose and 0.9% agar. Each dot (C, D) represented a colony from a replicate and a time point. (D) The percent of significant points (Fourier spectral peak height>1.5) plotted as a function of agar. The cell type (FLO11 or flo11Δ) is indicated in white font inside the circles.

Mentions: To determine whether the distances between wrinkles and spokes were regular, and had a dependence on agar and glucose concentrations, we investigated the surface patterns of individual colonies by manual measurements of inter-wrinkle distances. The narrow distributions of inter-wrinkle and inter-spoke distances suggested regular spacing of these structures (Fig. 4, S8 Figure). Moreover, the number of wrinkles and spokes increased towards the colony edge, indicating that pattern formation tended to preserve inter-wrinkle and inter-spoke arc-lengths rather than arc-angles (S3 Movie). Therefore, the quasi-regular spacing between these structures suggested preference of specific inter-wrinkle and inter-spoke distances. The preferred distance between consecutive spokes decreased with the agar concentration (Fig. 4, S8 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)

Analysis of the wavelengths of the colony surface patterns.(A) The wavelength of spokes (2) measured manually and by Fast Fourier Transformation (FFT) decreased with increasing agar density, while the wavelength of primary wrinkles (1) from manual measurements were less sensitive to the change of agar density. Since the automated FFT measurement was sensitive to noise in the image, FFT did not detect the small-wavelength primary wrinkles as significant. The wavelength of the wrinkles was shorter than that of the spokes at all agar levels tested. The experimentally measured geometric mean wavelength of spokes matched best the ESVS thick substrate model, while the geometric mean wavelength of primary wrinkles matched the ESVS thin substrate model. The inserted image shows the primary and secondary wrinkles measured at the outer radii, indicated by red and green lines, respectively. (B) The Fourier wavelengths plotted as a function of section radius, independent of time for FLO11 colony at 0.5% glucose and 0.9% agar. (C) Same as (B), but for a flo11Δ colony at 0.5% glucose and 0.9% agar. Each dot (C, D) represented a colony from a replicate and a time point. (D) The percent of significant points (Fourier spectral peak height>1.5) plotted as a function of agar. The cell type (FLO11 or flo11Δ) is indicated in white font inside the circles.
© Copyright Policy
Related In: Results  -  Collection

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

pcbi-1003979-g004: Analysis of the wavelengths of the colony surface patterns.(A) The wavelength of spokes (2) measured manually and by Fast Fourier Transformation (FFT) decreased with increasing agar density, while the wavelength of primary wrinkles (1) from manual measurements were less sensitive to the change of agar density. Since the automated FFT measurement was sensitive to noise in the image, FFT did not detect the small-wavelength primary wrinkles as significant. The wavelength of the wrinkles was shorter than that of the spokes at all agar levels tested. The experimentally measured geometric mean wavelength of spokes matched best the ESVS thick substrate model, while the geometric mean wavelength of primary wrinkles matched the ESVS thin substrate model. The inserted image shows the primary and secondary wrinkles measured at the outer radii, indicated by red and green lines, respectively. (B) The Fourier wavelengths plotted as a function of section radius, independent of time for FLO11 colony at 0.5% glucose and 0.9% agar. (C) Same as (B), but for a flo11Δ colony at 0.5% glucose and 0.9% agar. Each dot (C, D) represented a colony from a replicate and a time point. (D) The percent of significant points (Fourier spectral peak height>1.5) plotted as a function of agar. The cell type (FLO11 or flo11Δ) is indicated in white font inside the circles.
Mentions: To determine whether the distances between wrinkles and spokes were regular, and had a dependence on agar and glucose concentrations, we investigated the surface patterns of individual colonies by manual measurements of inter-wrinkle distances. The narrow distributions of inter-wrinkle and inter-spoke distances suggested regular spacing of these structures (Fig. 4, S8 Figure). Moreover, the number of wrinkles and spokes increased towards the colony edge, indicating that pattern formation tended to preserve inter-wrinkle and inter-spoke arc-lengths rather than arc-angles (S3 Movie). Therefore, the quasi-regular spacing between these structures suggested preference of specific inter-wrinkle and inter-spoke distances. The preferred distance between consecutive spokes decreased with the agar concentration (Fig. 4, S8 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
Related in: MedlinePlus