Heterosis as a consequence of regulatory incompatibility

Herbst, Rebecca H.; Bar-Zvi, Dana; Reikhav, Sharon; Soifer, Ilya; Breker, Michal; Jona, Ghil; Shimoni, Eyal; Schuldiner, Maya; Levy, Avraham A.; Barkai, Naama

doi:10.1186/s12915-017-0373-7

Cited by 38 publications

(39 citation statements)

References 52 publications

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“…Though we have focused here on beneficial gene deletions, we note that other groups have used similar datasets to look at mutations that decrease fitness (Herbst et al 2017;Weiss et al 2018). We largely confirm the patterns observed in S. paradoxus x S. cerevisiae hybrids, though the different conditions utilized across studies make direct comparisons complicated.…”

Section: Discussionsupporting

confidence: 65%

Fitness Benefits of Loss of Heterozygosity in SaccharomycesHybrids

Lancaster

Payen

Heil

et al. 2018

Preprint

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With two genomes in the same organism, interspecific hybrids have unique opportunities and costs. In both plants and yeasts, wild, pathogenic, and domesticated hybrids may eliminate portions of one parental genome, a phenomenon known as loss of heterozygosity (LOH).Laboratory evolution of hybrid yeast recapitulates these results, with LOH occurring in just a few hundred generations of propagation. In this study, we systematically looked for alleles that are beneficial when lost in order to determine how prevalent this mode of adaptation may be, and to determine candidate loci that might underlie the benefits of larger-scale chromosome rearrangements. These aims were accomplished by mating Saccharomyces uvarum with the S. cerevisiae deletion collection to create hybrids, such that each nonessential S. cerevisiae allele is deleted. Competitive fitness assays of these pooled, barcoded, hemizygous strains, and accompanying controls, revealed a large number of loci for which LOH is beneficial. We found that the fitness effects of hemizygosity are dependent on the species context, the selective environment, and the species origin of the deleted allele. Further, we found that hybrids have a larger distribution of fitness consequences vs. matched S. cerevisiae hemizygous diploids. Our results suggest that LOH can be a successful strategy for adaptation of hybrids to new environments, and we identify candidate loci that drive the chromosomal rearrangements observed in evolution of yeast hybrids.

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Section: Discussionsupporting

confidence: 65%

Fitness Benefits of Loss of Heterozygosity in SaccharomycesHybrids

Lancaster

Payen

Heil

et al. 2018

Preprint

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“…RNA extraction and library preparation were performed as described above and the fastq files was then processes by a pipeline for RNAseq data was created by Gil Hornung (INCPM, Weizmann Institute of Science, Israel), as described in (Herbst et al, 2017). Total reads were normalized to the ratio between the S. cerevisiae and S. paradoxus sum-of-reads and then to number of cells as measured in the experiment as described earlier.…”

Section: Methodsmentioning

confidence: 99%

Gene transcription as a limiting factor in protein production and cell growth

Metzl-Raz

Kafri

Yaakov

et al. 2019

Preprint

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8Growth rate and cell size are principle characteristics of proliferating cells, whose values 9 depend on cellular biosynthetic processes in a way poorly understood. Protein production is 10 critical for growth, and we therefore examined for processes limiting this production. 11Burdening cells with an excess of inert protein changed endogenous gene expression similarly 12 to transcription-perturbing mutants, was epistatic to these mutants, but did not deplete 13 respective factors from gene promoters. Mathematical modeling, corroborated by 14 experiments, attributed this signature to a feedback which proportionally increases all 15 endogenous gene expression, but lags at fast initiating genes already transcribed close to the 16 maximal possible rate. As a possible benefit of maximizing transcription rates, we discuss a 17 conflict between cell growth rate and size, which emerges above a critical cell size set by 18 transcript abundance. We propose that biochemical limits on protein and mRNA production 19 define the characteristic values of cell size and division time. 20 21 22 23 Introduction: 24 Cells tightly control the rate by which different proteins are produced. Regulation of protein 25 expression can be direct, by factors that bind specific regulatory regions, or indirect, through 26 changes in global parameters such as growth rate or cell size that subsequently alter protein 27 expression. Indirect regulation may also occur through the depletion of common resources: 28 when a general machinery is limiting, inducing the expression of specific proteins reduces 29 production of other proteins that compete for the same machinery. Direct regulation of gene 30 expression is extensively studied. By contrast, little is known about indirect regulations within 31 the transcription and translation networks.32 Ribosomes present a potentially limiting resource that determines the rate of protein 33 translation and cell growth. Theory shows that in order to maximize growth rate, cells must tune 34 their proteome compositions, so that they express the maximal number of ribosomes which can 35 still be simultaneously engaged in translation. Under these conditions, in which all expressed 36 ribosomes are constantly translating, growth rate is proportional to ribosome concentration, 37 namely the ribosome:protein ratio. This predicted linear relation between ribosome 38 concentration and cell growth rate was verified experimentally in a large number of cell types Metzl-Raz et al.,major role in transcription initiation and re-initiation, we focused on the rate by which 79 transcription is initiated. We discuss why transcription cannot be initiated at rates that exceed 80 an upper bound, and review data reporting genes transcribed at rates close to this limit. We 81 provide evidence that the transcription profile of the burden cells is attributed to these rapidly 82 transcribed genes: burden initiates a feedback in cells, which proportionally increases the 83 amounts of endogenous mRNAs, but fails to do so at genes already t...

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“…Although hybridization can have many negative impacts on the long-term genetic integrity of some taxa (Lowe et al 2015;Todesco et al 2016) , it can also create favorable conditions for rapid adaptive evolution. The adaptive role of hybridization has been shown in the colonization of new niches (Lewontin & Birch 1966;Heil et al 2017;Herbst et al 2017) , during speciation (Schumer et al 2014) , and during adaptive radiation (Ballerini 2012) . Prime examples include Darwin finches, which benefited from hybridization during adaptation to the adverse climatic conditions (drought, flooding, etc.)…”

Section: Introductionmentioning

confidence: 99%

“…Certain models and experiments show that increase in mutation rates may accelerate adaptation (Taddei et al 1997;Schaaff et al 2002;Labat et al 2005;Le Bars et al 2014;Bui et al 2015;Couce et al 2017) . Genomic instability includes higher rate of DNA damage (Wang et al 2014;Herbst et al 2017) , chromosomal rearrangements (Baack & Rieseberg 2007;Mwathi et al 2019) , gene and chromosome copy number variation (Morales & Dujon 2012;Dion-Côté & Barbash 2017) and the multiplication of repetitive and transposable elements (Fontdevila 2005;Guerreiro 2014) . These changes often lead to aneuploidy, which has also been shown to be a mechanism of adaptation in stressful conditions (Mulla et al 2014;Sunshine et al 2015) and hybrids may be particularly prone to producing aneuploid progeny (Gilchrist & Stelkens 2019) .…”

Section: Introductionmentioning

confidence: 99%

Interspecific Hybrids Show a Reduced Adaptive Potential Under DNA Damaging Conditions

Bautista

Marsit

Landry

2020

Preprint

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AbstractHybridization may increase the probability of adaptation to extreme stresses. This advantage could be caused by an increased genome plasticity in hybrids, which could accelerate the search for adaptive mutations. High ultraviolet (UV) radiation is a particular challenge in terms of adaptation because it affects the viability of organisms by directly damaging DNA, while also challenging future generations by increasing mutation rate. Here we test if hybridization accelerates adaptive evolution in response to DNA damage, using yeast as a model. We exposed 180 populations of hybrids between species (Saccharomyces cerevisiae and Saccharomyces paradoxus) and their parental strains to UV mimetic and control conditions for approximately 100 generations. Although we found that adaptation occurs in both hybrids and parents, hybrids achieved a lower rate of adaptation, contrary to our expectations. Adaptation to DNA damage conditions comes with a large and similar cost for parents and hybrids, suggesting that this cost is not responsible for the lower adaptability of hybrids. We suggest that the lower adaptive potential of hybrids in this condition may result from the interaction between DNA damage and the inherent genetic instability of hybrids.

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Heterosis as a consequence of regulatory incompatibility

Cited by 38 publications

References 52 publications

Fitness Benefits of Loss of Heterozygosity in SaccharomycesHybrids

Fitness Benefits of Loss of Heterozygosity in SaccharomycesHybrids

Gene transcription as a limiting factor in protein production and cell growth

Interspecific Hybrids Show a Reduced Adaptive Potential Under DNA Damaging Conditions

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