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.2003 Sep 1;31(17):5212-20.
doi: 10.1093/nar/gkg699.

Isochores and tissue-specificity

Affiliations

Isochores and tissue-specificity

Alexander E Vinogradov. Nucleic Acids Res..

Abstract

The housekeeping (ubiquitously expressed) genes in the mammal genome were shown here to be on average slightly GC-richer than tissue-specific genes. Both housekeeping and tissue-specific genes occupy similar ranges of GC content, but the former tend to concentrate in the upper part of the range. In the human genome, tissue-specific genes show two maxima, GC-poor and GC-rich. The strictly tissue-specific human genes tend to concentrate in the GC-poor region; their distribution is left-skewed and thus reciprocal to the distribution of housekeeping genes. The intermediately tissue-specific genes show an intermediate GC content and the right-skewed distribution. Both in the human and mouse, genes specific for some tissues (e.g., parts of the central nervous system) have a higher average GC content than housekeeping genes. Since they are not transcribed in the germ line (in contrast to housekeeping genes), and therefore have a lower probability of inheritable gene conversion, this finding contradicts the biased gene conversion (BGC) explanation for elevated GC content in the heavy isochores of mammal genome. Genes specific for germ-line tissues (ovary, testes) show a low average GC content, which is also in contradiction to the BGC explanation. Both for the total data set and for the most part of tissues taken separately, a weak positive correlation was found between gene GC content and expression level. The fraction of ubiquitously expressed genes is nearly 1.5-fold higher in the mouse than in the human. This suggests that mouse tissues are comparatively less differentiated (on the molecular level), which can be related to a less pronounced isochoric structure of the mouse genome. In each separate tissue (in both species), tissue-specific genes do not form a clear-cut frequency peak (in contrast to housekeeping genes), but constitute a continuum with a gradually increasing degree of tissue-specificity, which probably reflects the path of cell differentiation and/or an independent use of the same protein in several unrelated tissues.

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Figures

Figure 1
Figure 1
Bivariate distribution of GC3 versus number of tissues where a given gene is expressed. (A) Human, (B) mouse.
Figure 2
Figure 2
Histograms of human genes expressed in different numbers of tissues. (A) Cumulative for all tissues (as in Fig. 1), (B) genes expressed in the spleen (a picture typical for all tissues except testis), (C) genes expressed in the testis.
Figure 3
Figure 3
Comparison of GC3 of genes expressed in different number of tissues in the human genome. (A) Histograms of housekeeping versus strictly tissue-specific genes, (B) histograms of housekeeping versus intermediately tissue-specific genes, (C) means with least significant differences (LSD) intervals. Medians of GC3 of housekeeping, intermediately and strictly tissue-specific genes also differ significantly (68.3, 63.1, 55.9%; Kruskall–Wallis,P < 10–12). Standardized skewness indicates that the distributions of housekeeping and intermediately tissue-specific genes are significantly right-skewed (–2.5,P < 0.01; and –4.9,P < 10–4, respectively), whereas the distribution of strictly tissue-specific genes is left-skewed (4.3,P < 10–4).
Figure 4
Figure 4
Comparison of GC3 of genes expressed in different numbers of tissues in the mouse genome. (A) Histograms of housekeeping versus strictly tissue-specific genes, (B) histograms of housekeeping versus intermediately tissue-specific genes, (C) means with LSD intervals. Medians of GC3 of housekeeping, intermediately and strictly tissue-specific genes also differ significantly (63.4, 62.1, 60.8%; Kruskall–Wallis,P < 10–4). Standardized skewness indicates that all distributions are significantly right-skewed (–4.3,P < 10–4; –7.4,P < 10–4; and –2.5,P < 0.05, respectively).
Figure 5
Figure 5
The regression of (log-transformed) gene expression level averaged for all tissues on GC3. (A) Human (r = 0.20,P < 10–6), (B) mouse (r = 0.11,P < 10–6). Dashed lines, confidence limits; dotted lines, prediction limits.
Figure 6
Figure 6
Bivariate distribution of GC3 versus number of tissues where a given gene is expressed for the homologous genes/homologous tissues data sets (1791 genes and 20 tissues). (A) Human, (B) mouse.
Figure 7
Figure 7
The GC3 for different groups of mouse genes from the homologous genes/homologous tissues data set (HS+MM+, genes expressed in all tissues of both species; HS+MM–, genes expressed in all tissues of human but not mouse; HS–MM+, genes expressed in all tissues of mouse but not human; HS–MM–, genes expressed in all tissues in both species). (A) Means with LSD intervals, (B) box-plot. The values within the first and the second pairs of gene groups do not differ significantly while the first pair differ from the second both in parametric and non-parametric (Mann–Whitney and Kruskall–Wallis) tests (P < 10–5).
Figure 8
Figure 8
The GC3 for different groups of mouse genes from the homologous genes/homologous tissues data set (HS+MM+, genes expressed in all tissues of both species; HS+MM–, genes expressed in all tissues of human but not mouse; HS–MM+, genes expressed in all tissues of mouse but not human; HS–MM–, genes expressed in all tissues in both species). (A) Means with LSD intervals, (B) box-plot. The values within the first and the second pairs of gene groups do not differ significantly while the first pair differ from the second both in parametric and non-parametric (Mann–Whitney and Kruskall–Wallis) tests (P < 10–4).
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