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Single-cell phenomics reveals intra-species variation of phenotypic noise in yeast.

ABSTRACT: Most quantitative measures of phenotypic traits represent macroscopic contributions of large numbers of cells. Yet, cells of a tissue do not behave similarly, and molecular studies on several organisms have shown that regulations can be highly stochastic, sometimes generating diversified cellular phenotypes within tissues. Phenotypic noise, defined here as trait variability among isogenic cells of the same type and sharing a common environment, has therefore received a lot of attention. Given the potential fitness advantage provided by phenotypic noise in fluctuating environments, the possibility that it is directly subjected to evolutionary selection is being considered. For selection to act, phenotypic noise must differ between contemporary genotypes. Whether this is the case or not remains, however, unclear because phenotypic noise has very rarely been quantified in natural populations.Using automated image analysis, we describe here the phenotypic diversity of S. cerevisiae morphology at single-cell resolution. We profiled hundreds of quantitative traits in more than 1,000 cells of 37 natural strains, which represent various geographical and ecological origins of the species. We observed abundant trait variation between strains, with no correlation with their ecological origin or population history. Phenotypic noise strongly depended on the strain background. Noise variation was largely trait-specific (specific strains showing elevated noise for subset of traits) but also global (a few strains displaying elevated noise for many unrelated traits).Our results demonstrate that phenotypic noise does differ quantitatively between natural populations. This supports the possibility that, if noise is adaptive, microevolution may tune it in the wild. This tuning may happen on specific traits or by varying the degree of global phenotypic buffering.

SUBMITTER: Yvert G

PROVIDER: S-EPMC3711934 | biostudies-literature | 2013 Jul

REPOSITORIES: biostudies-literature

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Single-cell phenomics reveals intra-species variation of phenotypic noise in yeast.

Yvert Gaël G Ohnuki Shinsuke S Nogami Satoru S Imanaga Yasutaka Y Fehrmann Steffen S Schacherer Joseph J Ohya Yoshikazu Y

BMC systems biology 20130703

<h4>Background</h4>Most quantitative measures of phenotypic traits represent macroscopic contributions of large numbers of cells. Yet, cells of a tissue do not behave similarly, and molecular studies on several organisms have shown that regulations can be highly stochastic, sometimes generating diversified cellular phenotypes within tissues. Phenotypic noise, defined here as trait variability among isogenic cells of the same type and sharing a common environment, has therefore received a lot of ...[more]

PMID: 23822767

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Project description:Abundant genomic heterozygosity can be found in wild strains of the budding yeast Saccharomyces cerevisiae isolated from industrial and clinical environments. The extent to which heterozygosity influences the phenotypes of these isolates is not fully understood. One such case is the PE-2/JAY270 strain, a natural hybrid widely adopted by sugarcane bioethanol distilleries for its ability to thrive under harsh biotic and abiotic stresses during industrial scale fermentation, however, it is not known whether or how the heterozygous configuration of the JAY270 genome contributes to its many desirable traits. In this study, we took a step toward exploring this question by conducting an initial functional characterization of JAY270's heteroalleles. We manipulated the abundance and distribution of heterozygous alleles through inbreeding and targeted uniparental disomy (UPD). Unique combinations of homozygous alleles in each inbred strain revealed wide phenotypic variation for at least two important industrial traits: Heat stress tolerance and competitive growth. Quantitative trait loci analyses allowed the identification of broad genomic regions where genetic polymorphisms potentially impacted these traits, and there was no overlap between the loci associated with each. In addition, we adapted an approach to induce bidirectional UPD of three targeted pairs of chromosomes (IV, XIV, and XV), while heterozygosity was maintained elsewhere in the genome. In most cases UPD led to detectable phenotypic alterations, often in opposite directions between the two homozygous haplotypes in each UPD pair. Our results showed that both widespread and regional homozygosity could uncover cryptic phenotypic variation supported by the heteroalleles residing in the JAY270 genome. Interestingly, we characterized multiple examples of inbred and UPD strains that displayed heat tolerance or competitive growth phenotypes that were superior to their heterozygous parent. However, we propose that homozygosity for those regions may be associated with a decrease in overall fitness in the complex and dynamic distillery environment, and that may have contributed to slowing down the erosion of heterozygosity from the JAY270 genome. This study also laid a foundation for approaches that can be expanded to the identification of specific alleles of interest for industrial applications in this and other hybrid yeast strains.

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Single-cell phenomics reveals intra-species variation of phenotypic noise in yeast.

Publications

Single-cell phenomics reveals intra-species variation of phenotypic noise in yeast.

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