Coding repeat instability in the <i>FLO11</i> gene of <i>Saccharomyces</i> yeasts

Fidalgo, Manuel; Barrales, Ramón R.; Jiménez, Juan

doi:10.1002/yea.1642

Cited by 52 publications

(57 citation statements)

References 36 publications

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“…In these transformants, as the gene length increased, so did the weight of the biofilm. The same results were obtained by Fidalgo et al (2008), who showed the phenotypic effects of different alleles of FLO11 in flor/laboratory hybrids of S. cerevisiae. However, to conclude that the expansion and contraction of repeated sequences allow natural populations to rapidly adapt to a fluctuating environment, it is necessary to study the phenotypic effects of the different FLO11 alleles in their specific genetic backgrounds.…”

Section: Discussionsupporting

confidence: 73%

“…It has been reported that in the same genetic background, differences in the lengths of repeated sequences in the FLO11 gene correlate with variations in the intensities of some FLO11-associated phenotypes (Fidalgo et al, 2008 The same analysis regarding FLO11 alleles and FLO11-dependent phenotypes was carried out considering different genetic backgrounds. To this end, Spearman's correlation coefficients (r) were calculated by considering the length of FLO11 repeated sequences and mat formation, adherence to plastic, biofilm-forming ability and hydrophobicity of the 14 flor wild strains that were homozygous at the FLO11 locus.…”

Section: Flo11 Is Highly Polymorphicmentioning

confidence: 99%

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FLO11 gene length and transcriptional level affect biofilm-forming ability of wild flor strains of Saccharomyces cerevisiae

Zara

Pinna

et al. 2009

Microbiology

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In Saccharomyces cerevisiae, FLO11 encodes an adhesin that is associated with different phenotypes, such as adherence to solid surfaces, hydrophobicity, mat and air-liquid biofilm formation. In the present study, we analysed FLO11 allelic polymorphisms and FLO11-associated phenotypes of 20 flor strains. We identified 13 alleles of different lengths, varying from 3.0 to 6.1 kb, thus demonstrating that FLO11 is highly polymorphic. Two alleles of 3.1 and 5.0 kb were cloned into strain BY4742 to compare the FLO11-associated phenotypes in the same genetic background. We show that there is a significant correlation between biofilm-forming ability and FLO11 length both in different and in the same genetic backgrounds. Moreover, we propose a multiple regression model that allows prediction of air-liquid biofilm-forming ability on the basis of transcription levels and lengths of FLO11 alleles in a population of S. cerevisiae flor strains. Considering that transcriptional differences are only partially explained by the differences in the promoter sequences, our results are consistent with the hypothesis that FLO11 transcription levels are strongly influenced by genetic background and affect biofilm-forming ability.

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Section: Discussionsupporting

confidence: 73%

Section: Flo11 Is Highly Polymorphicmentioning

confidence: 99%

FLO11 gene length and transcriptional level affect biofilm-forming ability of wild flor strains of Saccharomyces cerevisiae

Zara

Pinna

et al. 2009

Microbiology

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“…Among these individuals (n = 30), we identified a single locus that was nearly fixed for the YJM allele ( Figure 3A, top), which was located on chromosome IX and overlapped FLO11. FLO11 is known to harbor extensive functional variation across yeast isolates in both its coding and noncoding regions (Fidalgo et al 2006(Fidalgo et al , 2008. To test for functional variation at FLO11 in the BYxYJM cross, we separately replaced the coding and noncoding regions of FLO11 in Segregant 2 with the BY alleles ( Figure S1; see also Materials and Methods).…”

Section: Multiple Architectures Of Flo8-independent Invasion In Ethanmentioning

confidence: 99%

Regulatory Rewiring in a Cross Causes Extensive Genetic Heterogeneity

et al. 2015

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Genetic heterogeneity occurs when individuals express similar phenotypes as a result of different underlying mechanisms. Although such heterogeneity is known to be a potential source of unexplained heritability in genetic mapping studies, its prevalence and molecular basis are not fully understood. Here we show that substantial genetic heterogeneity underlies a model phenotype-the ability to grow invasively-in a cross of two Saccharomyces cerevisiae strains. The heterogeneous basis of this trait across genotypes and environments makes it difficult to detect causal loci with standard genetic mapping techniques. However, using selective genotyping in the original cross, as well as in targeted backcrosses, we detected four loci that contribute to differences in the ability to grow invasively. Identification of causal genes at these loci suggests that they act by changing the underlying regulatory architecture of invasion. We verified this point by deleting many of the known transcriptional activators of invasion, as well as the gene encoding the cell surface protein Flo11 from five relevant segregants and showing that these individuals differ in the genes they require for invasion. Our work illustrates the extensive genetic heterogeneity that can underlie a trait and suggests that regulatory rewiring is a basic mechanism that gives rise to this heterogeneity.KEYWORDS complex traits; genetic mapping; invasive growth; regulatory networks; yeast G ENETIC studies in humans and model organisms have reported unexplained heritability for many traits (Manolio et al. 2009). A possible contributor to this "missing" heritability is genetic heterogeneity-individuals exhibiting similar phenotypes owing to different genetic and molecular mechanisms (Risch 2000;McClellan and King 2010;Wray and Maier 2014). Genetic heterogeneity can reduce the statistical power of mapping studies (Manchia et al. 2013;Wray and Maier 2014) and may involve multiple variants segregating in the same gene (allelic heterogeneity) or different genes (nonallelic heterogeneity) (Risch 2000). Work to date has shown that allelic heterogeneity is widespread (e.g., McClellan and King 2010;Ehrenreich et al. 2012;Long et al. 2014) and often involves two or more null or partial loss-of-function variants segregating in a single phenotypically important gene (e.g., Nogee et al. 2000;Sutcliffe et al. 2005;Will et al. 2010). However, the prominence and underlying mechanisms of nonallelic heterogeneity are less understood.In this paper we describe an example of nonallelic heterogeneity using heritable variation in the ability of Saccharomyces cerevisiae strains to undergo haploid invasive growth as our model. Invasive growth is a phenotype that is triggered by low carbon or nitrogen availability and is thought to be an adaptive response that allows yeast cells to adhere to and penetrate surfaces (Cullen and Sprague 2000). Invasion typically requires expression of FLO11, which encodes a cell surface glycoprotein that facilitates cell-cell and cell-surface adhes...

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“…The loss or gain of FLO11D allele events can be explained by the dendrogram, which suggested that the FLO11D allele originated from a single origin and that sequence alteration in the third FLO11D allele occurred in Z3 after its acquisition. In S. cerevisiae, it has been reported that the length and type of repetitive units in the Flo11p coding repeats domain affect the Flo11p-associated functions, including cellular hydrophobicity (Fidalgo et al 2006;Fidalgo et al 2008;Zara et al 2009); however, the relationship between its functions and the copy number of the FLO gene itself has not been elucidated. To investigate this relationship, we measured the cellular hydrophobicity of FLO11D mutants in Z3.…”

mentioning

confidence: 99%

“…The latter domain is also referred to as a domain with intragenic tandem repeats. The variation in the intragenic repeat number and/or the distribution of the different repetitive units provides a functional diversity of the cellsurface antigens that allows rapid adaptation to the environment (Verstrepen et al 2005;Fidalgo et al 2006Fidalgo et al , 2008Zara et al 2009). However, the relationship between adaptation and the copy number of the FLO gene itself, but not the number of the intragenic repeat units, has not been investigated.…”

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confidence: 99%

Adaptation of the Osmotolerant Yeast Zygosaccharomyces rouxii to an Osmotic Environment Through Copy Number Amplification of FLO11D

2013

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Copy number variations (CNVs) contribute to the adaptation process in two possible ways. First, they may have a direct role, in which a certain number of copies often provide a selective advantage. Second, CNVs can also indirectly contribute to adaptation because a higher copy number increases the so-called "mutational target size." In this study, we show that the copy number amplification of FLO11D in the osmotolerant yeast Zygosaccharomyces rouxii promotes its further adaptation to a florformative environment, such as osmostress static culture conditions. We demonstrate that a gene, which was identified as FLO11D, is responsible for flor formation and that its expression is induced by osmostress under glucose-free conditions, which confer unique characteristics to Z. rouxii, such as osmostress-dependent flor formation. This organism possesses zero to three copies of FLO11D, and it appears likely that the FLO11D copy number increased in a branch of the Z. rouxii tree. The cellular hydrophobicity correlates with the FLO11D copy number, and the strain with a higher copy number of FLO11D exhibits a fitness advantage compared to a reference strain under osmostress static culture conditions. Our data indicate that the FLO gene-related system in Z. rouxii has evolved remarkably to adapt to osmostress environments.A N organism adapts to adverse environments to survive and produce progeny. Adaptive evolution is the process through which a population becomes better suited to its environment via mutation, selection, and random drift (Bürger 2000;Cressman 2003;Ewens 2004;Nowak and Sigmund 2004). Types of mutations include nucleotide changes (Steiner et al. 2007;Barrick and Lenski 2009), transposition events (Wilke and Adams 1992;Aminetzach et al. 2005), and copy number variations (CNVs), including gene amplifications (duplication) and deletions (Brown et al. 1998;Perry et al. 2007;Gresham et al. 2010). CNVs can have a phenotypic impact and can consequently alter the fitness of an allele through the following mechanisms: (i) changing the coding sequence of a gene (Yamanaka et al. 2009;Schlattl et al. 2011), (ii) creating paralogs that can diverge from each other and take on new or specialized functions (neofunctionalization or subfunctionalization, respectively) (Ohno 1970;Innan and Kondrashov 2010), and (iii) altering the expression level of a gene (gene dosage effect) (Stranger et al. 2007;Yamanaka et al. 2009;Iskow et al. 2012). In humans, most CNVs overlapping genes are under purifying (negative) selection (Conrad et al. 2010), but a handful of CNVs are thought to be under positive selection (Cooper et al. 2007;Hurles et al. 2010;Iskow et al. 2012) such as AMY1 (Perry et al. 2007). In yeast, there are several examples of how the (increased) copy number can provide a direct selective advantage (Gresham et al. 2008;Voordeckers et al. 2012).In nature, budding yeast exhibits a number of adaptive responses, such as filamentation, invasive growth, flocculation, and biofilm formation, to overcome a deleterious enviro...

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Coding repeat instability in the FLO11 gene of Saccharomyces yeasts

Cited by 52 publications

References 36 publications

FLO11 gene length and transcriptional level affect biofilm-forming ability of wild flor strains of Saccharomyces cerevisiae

FLO11 gene length and transcriptional level affect biofilm-forming ability of wild flor strains of Saccharomyces cerevisiae

Regulatory Rewiring in a Cross Causes Extensive Genetic Heterogeneity

Adaptation of the Osmotolerant Yeast Zygosaccharomyces rouxii to an Osmotic Environment Through Copy Number Amplification of FLO11D

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