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Intrachromosomal colocalization strengthens co-expression, co-modification and evolutionary conservation of neighboring genes.

ABSTRACT: BACKGROUND:Gene order and location in chromosomes of species are non-random. Neighboring gene pairs tend to display some similarities, such as co-expression and co-modification. However, the contribution of linear proximity, spatial proximity, and evolutionary proximity to these similarities remain unclear, together with whether the presence of several types of proximity can strengthens the similarities. RESULTS:In this study, we investigated the properties of three kinds of colocalized gene pairs: intrachromosomal colocalized gene pairs, always-neighboring gene pairs, and evolutionary neighboring gene pairs. Our analysis showed that (1) Different types of colocalized genes differentially contribute to co-expression, co-modifications and conservation across species; (2) Intrachromosomal colocalization can strengthen co-expression and co-modification of neighboring gene pairs and their conservation across species; (3) The combination of the three kinds of colocalization can lead to the strongest co-modification and is most strongly conserved across species. (4) Colocalized gene pairs are indicative of phylogenetic relationships and whole genome duplications (WGDs). CONCLUSIONS:These results provide valuable clues for future efforts to understand the characteristics of colocalized gene pairs and how the neighborhood affects their interactions.

SUBMITTER: Lian S

PROVIDER: S-EPMC6000932 | biostudies-literature | 2018 Jun

REPOSITORIES: biostudies-literature

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Intrachromosomal colocalization strengthens co-expression, co-modification and evolutionary conservation of neighboring genes.

Lian Shuaibin S Liu Tianliang T Jing Shengli S Yuan Hongyu H Zhang Zaibao Z Cheng Lin L

BMC genomics 20180613 1

<h4>Background</h4>Gene order and location in chromosomes of species are non-random. Neighboring gene pairs tend to display some similarities, such as co-expression and co-modification. However, the contribution of linear proximity, spatial proximity, and evolutionary proximity to these similarities remain unclear, together with whether the presence of several types of proximity can strengthens the similarities.<h4>Results</h4>In this study, we investigated the properties of three kinds of coloc ...[more]

PMID: 29898652

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Project description:The structure of eukaryotic genes is generally a combination of exons interrupted by intragenic non-coding DNA regions (introns) removed by RNA splicing to generate the mature mRNA. A fraction of genes, however, comprise a single coding exon with introns in their untranslated regions or are intronless genes (IGs), lacking introns entirely. The latter code for essential proteins involved in development, growth, and cell proliferation and their expression has been proposed to be highly specialized for neuro-specific functions and linked to cancer, neuropathies, and developmental disorders. The abundant presence of introns in eukaryotic genomes is pivotal for the precise control of gene expression. Notwithstanding, IGs exempting splicing events entail a higher transcriptional fidelity, making them even more valuable for regulatory roles. This work aimed to infer the functional role and evolutionary history of IGs centered on the mouse genome. IGs consist of a subgroup of genes with one exon including coding genes, non-coding genes, and pseudogenes, which conform approximately 6% of a total of 21,527 genes. To understand their prevalence, biological relevance, and evolution, we identified and studied 1,116 IG functional proteins validating their differential expression in transcriptomic data of embryonic mouse telencephalon. Our results showed that overall expression levels of IGs are lower than those of MEGs. However, strongly up-regulated IGs include transcription factors (TFs) such as the class 3 of POU (HMG Box), Neurog1, Olig1, and BHLHe22, BHLHe23, among other essential genes including the β-cluster of protocadherins. Most striking was the finding that IG-encoded BHLH TFs fit the criteria to be classified as microproteins. Finally, predicted protein orthologs in other six genomes confirmed high conservation of IGs associated with regulating neural processes and with chromatin organization and epigenetic regulation in Vertebrata. Moreover, this study highlights that IGs are essential modulators of regulatory processes, such as the Wnt signaling pathway and biological processes as pivotal as sensory organ developing at a transcriptional and post-translational level. Overall, our results suggest that IG proteins have specialized, prevalent, and unique biological roles and that functional divergence between IGs and MEGs is likely to be the result of specific evolutionary constraints.

Dataset Information

Intrachromosomal colocalization strengthens co-expression, co-modification and evolutionary conservation of neighboring genes.

Publications

Intrachromosomal colocalization strengthens co-expression, co-modification and evolutionary conservation of neighboring genes.

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