Pervasive coexpression of spatially proximal genes is buffered at the protein level
Abstract Genes are not randomly distributed in the genome. In humans, 10% of protein‐coding genes are transcribed from bidirectional promoters and many more are organised in larger clusters. Intriguingly, neighbouring genes are frequently coexpressed but rarely functionally related. Here we show tha...
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| Format: | Article |
| Language: | English |
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Springer Nature
2017-08-01
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| Series: | Molecular Systems Biology |
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| Online Access: | https://doi.org/10.15252/msb.20177548 |
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| author | Georg Kustatscher Piotr Grabowski Juri Rappsilber |
| author_facet | Georg Kustatscher Piotr Grabowski Juri Rappsilber |
| author_sort | Georg Kustatscher |
| collection | DOAJ |
| description | Abstract Genes are not randomly distributed in the genome. In humans, 10% of protein‐coding genes are transcribed from bidirectional promoters and many more are organised in larger clusters. Intriguingly, neighbouring genes are frequently coexpressed but rarely functionally related. Here we show that coexpression of bidirectional gene pairs, and closeby genes in general, is buffered at the protein level. Taking into account the 3D architecture of the genome, we find that co‐regulation of spatially close, functionally unrelated genes is pervasive at the transcriptome level, but does not extend to the proteome. We present evidence that non‐functional mRNA coexpression in human cells arises from stochastic chromatin fluctuations and direct regulatory interference between spatially close genes. Protein‐level buffering likely reflects a lack of coordination of post‐transcriptional regulation of functionally unrelated genes. Grouping human genes together along the genome sequence, or through long‐range chromosome folding, is associated with reduced expression noise. Our results support the hypothesis that the selection for noise reduction is a major driver of the evolution of genome organisation. |
| format | Article |
| id | doaj-art-e2943f44803e47ba9a9b5bfb7009ddd7 |
| institution | Kabale University |
| issn | 1744-4292 |
| language | English |
| publishDate | 2017-08-01 |
| publisher | Springer Nature |
| record_format | Article |
| series | Molecular Systems Biology |
| spelling | doaj-art-e2943f44803e47ba9a9b5bfb7009ddd72025-08-20T04:03:12ZengSpringer NatureMolecular Systems Biology1744-42922017-08-0113811410.15252/msb.20177548Pervasive coexpression of spatially proximal genes is buffered at the protein levelGeorg Kustatscher0Piotr Grabowski1Juri Rappsilber2Wellcome Trust Centre for Cell Biology, University of EdinburghChair of Bioanalytics, Institute of Biotechnology, Technische Universität BerlinWellcome Trust Centre for Cell Biology, University of EdinburghAbstract Genes are not randomly distributed in the genome. In humans, 10% of protein‐coding genes are transcribed from bidirectional promoters and many more are organised in larger clusters. Intriguingly, neighbouring genes are frequently coexpressed but rarely functionally related. Here we show that coexpression of bidirectional gene pairs, and closeby genes in general, is buffered at the protein level. Taking into account the 3D architecture of the genome, we find that co‐regulation of spatially close, functionally unrelated genes is pervasive at the transcriptome level, but does not extend to the proteome. We present evidence that non‐functional mRNA coexpression in human cells arises from stochastic chromatin fluctuations and direct regulatory interference between spatially close genes. Protein‐level buffering likely reflects a lack of coordination of post‐transcriptional regulation of functionally unrelated genes. Grouping human genes together along the genome sequence, or through long‐range chromosome folding, is associated with reduced expression noise. Our results support the hypothesis that the selection for noise reduction is a major driver of the evolution of genome organisation.https://doi.org/10.15252/msb.20177548gene expression noisegenome organisationproteomicsregulatory interferencetranscriptomics |
| spellingShingle | Georg Kustatscher Piotr Grabowski Juri Rappsilber Pervasive coexpression of spatially proximal genes is buffered at the protein level Molecular Systems Biology gene expression noise genome organisation proteomics regulatory interference transcriptomics |
| title | Pervasive coexpression of spatially proximal genes is buffered at the protein level |
| title_full | Pervasive coexpression of spatially proximal genes is buffered at the protein level |
| title_fullStr | Pervasive coexpression of spatially proximal genes is buffered at the protein level |
| title_full_unstemmed | Pervasive coexpression of spatially proximal genes is buffered at the protein level |
| title_short | Pervasive coexpression of spatially proximal genes is buffered at the protein level |
| title_sort | pervasive coexpression of spatially proximal genes is buffered at the protein level |
| topic | gene expression noise genome organisation proteomics regulatory interference transcriptomics |
| url | https://doi.org/10.15252/msb.20177548 |
| work_keys_str_mv | AT georgkustatscher pervasivecoexpressionofspatiallyproximalgenesisbufferedattheproteinlevel AT piotrgrabowski pervasivecoexpressionofspatiallyproximalgenesisbufferedattheproteinlevel AT jurirappsilber pervasivecoexpressionofspatiallyproximalgenesisbufferedattheproteinlevel |