Intra- and inter-specific variations of gene expression levels in yeast are largely neutral

Yang, Jian; Maclean, Calum J.; Park, C; Zhao, Huanhuan; Zhang, J

doi:10.1101/089995

Cited by 3 publications

(4 citation statements)

References 53 publications

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“…But, it also means that failure to reject neutrality, as in the case of yeast gene expression evolution, neither proves neutrality nor refutes adaptation. Nonetheless, based on additional experiments and tests, we recently found unambiguous evidence that the vast majority of gene expression level variations within and between yeast species are not adaptive but neutral 25 . Together, these analyses of yeast morphological and gene expression data raise the intriguing possibility that some classes of phenotypic traits evolve generally adaptively while others neutrally.…”

Section: Msmentioning

confidence: 93%

Testing the neutral hypothesis of phenotypic evolution

Ohya

Zhang

2016

Preprint

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It is generally accepted that a large fraction of genomic sequence variations within and between species are neutral or nearly so 1 . Whether the same is true for phenotypic variations is a central question in biology 2-7 . On the one hand, numerous phenotypic adaptations have been documented 2,8,9 and even Kimura, the champion of the neutral theory of molecular evolution, believed in widespread adaptive phenotypic evolution 1 . On the other hand, phenotypic studies are strongly biased toward traits that are likely to be adaptive 9 , contrasting genomic studies that are typically unbiased. It is thus desirable to test the neutral hypothesis of phenotypic evolution using traits irrespective of their potential involvement in adaptation. Here we present such a test for 210 morphological traits measured in multiple strains of the yeast Saccharomyces cerevisiae and two related species. Our test is based on the premise that, under neutrality, the rate of phenotypic evolution declines as the trait becomes more important to fitness, analogous to the neutral paradigm that functional genes evolve more slowly than functionless pseudogenes 10 .Neutrality is rejected in favor of adaptation if important traits evolve faster than less important ones, parallel to the demonstration of molecular adaptation when a functional gene evolves faster than pseudogenes. After controlling for the mutational size, we find faster evolution of more important morphological traits within and between species. By contrast, an analysis of 3466 yeast gene expression traits fails to reject neutrality. Thus, yeast morphological evolution is largely adaptive, but the same may not apply to other classes of phenotypes.Analogous to the neutral hypothesis of molecular evolution 1 , the neutral hypothesis of phenotypic evolution allows the presence of purifying selection; neutrality is rejected only when positive selection is invoked. Under the neutral hypothesis, compared with traits that are 3 relatively unimportant to fitness, relatively important traits should be subject to stronger purifying selection and evolve more slowly given the same speed of mutational input (Fig. 1a).However, if relatively important traits evolve faster than relatively unimportant traits, the neutral hypothesis would no longer hold and the only reasonable explanation would be stronger positive selection acting on relatively important traits than relatively unimportant ones ( Fig. 1b). This test of phenotypic neutrality differs from previous tests 3,4,[11][12][13][14][15] , which consider only one trait at a time and effectively require the intensity of positive selection to surpass that of purifying selection to reject neutrality. Because this requirement is sufficient but not necessary for demonstrating positive selection, it is replaced with the criterion of a positive correlation between trait importance and evolutionary rate to improve the power of the test (see Methods and Discussion).We first tested the neutral hypothesis of phenotypic evolution in a set of 210 morphologic...

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Section: Msmentioning

confidence: 93%

Testing the neutral hypothesis of phenotypic evolution

Ohya

Zhang

2016

Preprint

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“…Transcriptomic analyses are broadly considered a good first approach to understanding the state of a given cell population or its response to a stimulus. In fact, its use is becoming wider in the study of the physiology of Saccharomyces from industrial or other origins, especially the species Saccharomyces cerevisiae (Carvalho-Netto et al, 2015;Sardi et al, 2016;Nielsen et al, 2017;Yang et al, 2017;Zhang et al, 2018). However different authors had demonstrated a notable lack of correlation with proteomics or metabolomics data that cannot be diminished (Gygi et al, 1999;Chen et al, 2002;Pascal et al, 2008;Ghazalpour et al, 2011;Yeung, 2011).…”

Section: Discussionmentioning

confidence: 99%

Dominance of wine Saccharomyces cerevisiae strains over S. kudriavzevii in industrial fermentation competitions is related to an acceleration of nutrient uptake and utilization

Alonso-del-Real

Pérez‐Torrado

Querol

et al. 2019

Environmental Microbiology

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Summary Grape must is a sugar‐rich habitat for a complex microbiota which is replaced by Saccharomyces cerevisiae strains during the first fermentation stages. Interest on yeast competitive interactions has recently been propelled due to the use of alternative yeasts in the wine industry to respond to new market demands. The main issue resides in the persistence of these yeasts due to the specific competitive activity of S. cerevisiae. To gather deeper knowledge of the molecular mechanisms involved, we performed a comparative transcriptomic analysis during fermentation carried out by a wine S. cerevisiae strain and a strain representative of the cryophilic S. kudriavzevii, which exhibits high genetic and physiological similarities to S. cerevisiae, but also differences of biotechnological interest. In this study, we report that transcriptomic response to the presence of a competitor is stronger in S. cerevisiae than in S. kudriavzevii. Our results demonstrate that a wine S. cerevisiae industrial strain accelerates nutrient uptake and utilization to outcompete the co‐inoculated yeast, and that this process requires cell‐to‐cell contact to occur. Finally, we propose that this competitive phenotype evolved recently, during the adaptation of S. cerevisiae to man‐manipulated fermentative environments, since a non‐wine S. cerevisiae strain, isolated from a North American oak, showed a remarkable low response to competition.

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“…We followed a previous study (2) to compute the distance between each pair of transcriptomes on the basis of expression-level differences of orthologous genes and build a neighboring-joining tree of the 10 transcriptomes. Young et al's (1) conclusion means that the transcriptomes from the 5 monogamous species should be clustered in the tree, in exclusion of those from the nonmonogamous species.…”

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confidence: 99%

“…Names of monogamous species are underlined. Following ref 2,. for each gene i of species j, we converted the raw expression level X ij to the standardized expression level Y ij = (X ij − X i )/S i , where X i and S i are respectively the mean and SD of the expression level of gene i among the 10 species.…”

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confidence: 99%