The 3D Organization of the Yeast Genome Correlates with Co-Expression and Reflects Functional Relations between Genes

Homouz, Dirar; Kudlicki, Andrzej

doi:10.1371/journal.pone.0054699

Cited by 57 publications

(60 citation statements)

References 45 publications

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“…First, the interaction between the GAL1 reporters was only detected under the activating condition. This observation is consistent with previous statistical analysis, indicating that coregulated genes tend to cluster, and genes that are physically proximal tend to coexpress (21,31,32). Coactivated genes can also form "transcription factories" or "multigene complexes" in higher eukaryotic species (33,34), so our findings here are likely to be one example of a more general phenomenon.…”

Section: Discussionsupporting

confidence: 92%

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Interallelic interaction and gene regulation in budding yeast

Zhang

Bai

2016

Proc. Natl. Acad. Sci. U.S.A.

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In Drosophila, homologous chromosome pairing leads to "transvection," in which the enhancer of a gene can regulate the allelic transcription in trans. Interallelic interactions were also observed in vegetative diploid budding yeast, but their functional significance is unknown. Here, we show that a GAL1 reporter can interact with its homologous allele and affect its expression. By ectopically inserting two allelic reporters, one driven by wild-type GAL1 promoter (WT GAL1pr) and the other by a mutant promoter with delayed response to galactose induction, we found that the two reporters physically associate, and the WT GAL1pr triggers synchronized firing of the defective promoter and accelerates its activation without affecting its steady-state expression level. This interaction and the transregulatory effect disappear when the same reporters are located at nonallelic sites. We further demonstrated that the activator Gal4 is essential for the interallelic interaction, and the transregulation requires fully activated WT GAL1pr transcription. The mechanism of this phenomenon was further discussed. Taken together, our data revealed the existence of interallelic gene regulation in yeast, which serves as a starting point for understanding long-distance gene regulation in this genetically tractable system. homologous pairing | interallelic interaction | interallelic regulation | transvection | single-cell gene expression

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Section: Discussionsupporting

confidence: 92%

“…According to a statistical analysis of the Hi-C data, the Gal4 binding sites (GAL1 activator) cluster in the nucleus (21). β-estradiol-induced GAL1pr on two different chromosomes could form trans interactions under the activating condition in haploid yeast (22).…”

mentioning

confidence: 99%

Interallelic interaction and gene regulation in budding yeast

Zhang

Bai

2016

Proc. Natl. Acad. Sci. U.S.A.

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“…Compartmentalization of the nucleus, chromatin loops, and longrange interactions contribute to a complex regulatory network (Lieberman-Aiden et al 2009;Kalhor et al 2011;Dixon et al 2012;Homouz and Kudlicki 2013). In P. falciparum, little is known about the effect of genome organization on gene expression.…”

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confidence: 99%

Three-dimensional modeling of the P. falciparum genome during the erythrocytic cycle reveals a strong connection between genome architecture and gene expression

et al. 2014

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The development of the human malaria parasite Plasmodium falciparum is controlled by coordinated changes in gene expression throughout its complex life cycle, but the corresponding regulatory mechanisms are incompletely understood. To study the relationship between genome architecture and gene regulation in Plasmodium, we assayed the genome architecture of P. falciparum at three time points during its erythrocytic (asexual) cycle. Using chromosome conformation capture coupled with next-generation sequencing technology (Hi-C), we obtained high-resolution chromosomal contact maps, which we then used to construct a consensus three-dimensional genome structure for each time point. We observed strong clustering of centromeres, telomeres, ribosomal DNA, and virulence genes, resulting in a complex architecture that cannot be explained by a simple volume exclusion model. Internal virulence gene clusters exhibit domain-like structures in contact maps, suggesting that they play an important role in the genome architecture. Midway during the erythrocytic cycle, at the highly transcriptionally active trophozoite stage, the genome adopts a more open chromatin structure with increased chromosomal intermingling. In addition, we observed reduced expression of genes located in spatial proximity to the repressive subtelomeric center, and colocalization of distinct groups of parasite-specific genes with coordinated expression profiles. Overall, our results are indicative of a strong association between the P. falciparum spatial genome organization and gene expression. Understanding the molecular processes involved in genome conformation dynamics could contribute to the discovery of novel antimalarial strategies.

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“…Moreover, recently a correlation has been suggested between transcription factor network models and distances between average chromosome positions in human cells 19 . A series of studies further reported the co-localization of each of the following groups in SC: cohesin binding sites 20 , co-expressed genes, some identified GO terms 21 and gene targets of the same transcription factor 22 . Recently, an analysis of the genomic organization of the unique P. falciparum parasite throughout its cell cycle confirmed a relation between chromosome conformation and gene expression 18 .…”

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confidence: 99%

Three-dimensional eukaryotic genomic organization is strongly correlated with codon usage expression and function

2014

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It has been shown that the distribution of genes in eukaryotic genomes is not random; however, formerly reported relations between gene function and genomic organization were relatively weak. Previous studies have demonstrated that codon usage bias is related to all stages of gene expression and to protein function. Here we apply a novel tool for assessing functional relatedness, codon usage frequency similarity (CUFS), which measures similarity between genes in terms of codon and amino acid usage. By analyzing chromosome conformation capture data, describing the three-dimensional (3D) conformation of the DNA, we show that the functional similarity between genes captured by CUFS is directly and very strongly correlated with their 3D distance in Saccharomyces cerevisiae, Schizosaccharomyces pombe, Arabidopsis thaliana, mouse and human. This emphasizes the importance of threedimensional genomic localization in eukaryotes and indicates that codon usage is tightly linked to genome architecture.

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The 3D Organization of the Yeast Genome Correlates with Co-Expression and Reflects Functional Relations between Genes

Cited by 57 publications

References 45 publications

Interallelic interaction and gene regulation in budding yeast

Interallelic interaction and gene regulation in budding yeast

Three-dimensional modeling of the P. falciparum genome during the erythrocytic cycle reveals a strong connection between genome architecture and gene expression

Three-dimensional eukaryotic genomic organization is strongly correlated with codon usage expression and function

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