Spatiotemporal patterns of gene expression during development of a complex colony morphology.

Clonal communities of single celled organisms, such as bacterial or fungal colonies and biofilms, are spatially structured, with subdomains of cells experiencing differing environmental conditions. In the development of such communities, cell specialization is not only important to respond and adapt...

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Main Authors: Gareth A Cromie, Zhihao Tan, Michelle Hays, Amy Sirr, Aimée M Dudley
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2024-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0311061
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author Gareth A Cromie
Zhihao Tan
Michelle Hays
Amy Sirr
Aimée M Dudley
author_facet Gareth A Cromie
Zhihao Tan
Michelle Hays
Amy Sirr
Aimée M Dudley
author_sort Gareth A Cromie
collection DOAJ
description Clonal communities of single celled organisms, such as bacterial or fungal colonies and biofilms, are spatially structured, with subdomains of cells experiencing differing environmental conditions. In the development of such communities, cell specialization is not only important to respond and adapt to the local environment but has the potential to increase the fitness of the clonal community through division of labor. Here, we examine colony development in a yeast strain (F13) that produces colonies with a highly structured "ruffled" phenotype in the colony periphery and an unstructured "smooth" phenotype in the colony center. We demonstrate that in the F13 genetic background deletions of transcription factors can either increase (dig1D, sfl1D) or decrease (tec1D) the degree of colony structure. To investigate the development of colony structure, we carried out gene expression analysis on F13 and the three deletion strains using RNA-seq. Samples were taken early in colony growth (day2), which precedes ruffled phenotype development in F13, and from the peripheral and central regions of colonies later in development (day5), at which time these regions are structured and unstructured (respectively) in F13. We identify genes responding additively and non-additively to the genotype and spatiotemporal factors and cluster these genes into a number of different expression patterns. We identify clusters whose expression correlates closely with the degree of colony structure in each sample and include genes with known roles in the development of colony structure. Individual deletion of 26 genes sampled from different clusters identified 5 with strong effects on colony morphology (BUD8, CIS3, FLO11, MSB2 and SFG1), all of which eliminated or greatly reduced the structure of the F13 outer region.
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spelling doaj-art-7610f87834024a12892337f9a25f874b2025-01-08T05:33:29ZengPublic Library of Science (PLoS)PLoS ONE1932-62032024-01-011912e031106110.1371/journal.pone.0311061Spatiotemporal patterns of gene expression during development of a complex colony morphology.Gareth A CromieZhihao TanMichelle HaysAmy SirrAimée M DudleyClonal communities of single celled organisms, such as bacterial or fungal colonies and biofilms, are spatially structured, with subdomains of cells experiencing differing environmental conditions. In the development of such communities, cell specialization is not only important to respond and adapt to the local environment but has the potential to increase the fitness of the clonal community through division of labor. Here, we examine colony development in a yeast strain (F13) that produces colonies with a highly structured "ruffled" phenotype in the colony periphery and an unstructured "smooth" phenotype in the colony center. We demonstrate that in the F13 genetic background deletions of transcription factors can either increase (dig1D, sfl1D) or decrease (tec1D) the degree of colony structure. To investigate the development of colony structure, we carried out gene expression analysis on F13 and the three deletion strains using RNA-seq. Samples were taken early in colony growth (day2), which precedes ruffled phenotype development in F13, and from the peripheral and central regions of colonies later in development (day5), at which time these regions are structured and unstructured (respectively) in F13. We identify genes responding additively and non-additively to the genotype and spatiotemporal factors and cluster these genes into a number of different expression patterns. We identify clusters whose expression correlates closely with the degree of colony structure in each sample and include genes with known roles in the development of colony structure. Individual deletion of 26 genes sampled from different clusters identified 5 with strong effects on colony morphology (BUD8, CIS3, FLO11, MSB2 and SFG1), all of which eliminated or greatly reduced the structure of the F13 outer region.https://doi.org/10.1371/journal.pone.0311061
spellingShingle Gareth A Cromie
Zhihao Tan
Michelle Hays
Amy Sirr
Aimée M Dudley
Spatiotemporal patterns of gene expression during development of a complex colony morphology.
PLoS ONE
title Spatiotemporal patterns of gene expression during development of a complex colony morphology.
title_full Spatiotemporal patterns of gene expression during development of a complex colony morphology.
title_fullStr Spatiotemporal patterns of gene expression during development of a complex colony morphology.
title_full_unstemmed Spatiotemporal patterns of gene expression during development of a complex colony morphology.
title_short Spatiotemporal patterns of gene expression during development of a complex colony morphology.
title_sort spatiotemporal patterns of gene expression during development of a complex colony morphology
url https://doi.org/10.1371/journal.pone.0311061
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