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. 2006 Jan 7;273(1582):27-32.
doi: 10.1098/rspb.2005.3266.

Genome Size and Metabolic Intensity in Tetrapods: A Tale of Two Lines

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Free PMC article

Genome Size and Metabolic Intensity in Tetrapods: A Tale of Two Lines

Alexander E Vinogradov et al. Proc Biol Sci. .
Free PMC article

Abstract

We show the negative link between genome size and metabolic intensity in tetrapods, using the heart index (relative heart mass) as a unified indicator of metabolic intensity in poikilothermal and homeothermal animals. We found two separate regression lines of heart index on genome size for reptiles-birds and amphibians-mammals (the slope of regression is steeper in reptiles-birds). We also show a negative correlation between GC content and nucleosome formation potential in vertebrate DNA, and, consistent with this relationship, a positive correlation between genome GC content and nuclear size (independent of genome size). It is known that there are two separate regression lines of genome GC content on genome size for reptiles-birds and amphibians-mammals: reptiles-birds have the relatively higher GC content (for their genome sizes) compared to amphibians-mammals. Our results suggest uniting all these data into one concept. The slope of negative regression between GC content and nucleosome formation potential is steeper in exons than in non-coding DNA (where nucleosome formation potential is generally higher), which indicates a special role of non-coding DNA for orderly chromatin organization. The chromatin condensation and nuclear size are supposed to be key parameters that accommodate the effects of both genome size and GC content and connect them with metabolic intensity. Our data suggest that the reptilian-birds clade evolved special relationships among these parameters, whereas mammals preserved the amphibian-like relationships. Surprisingly, mammals, although acquiring a more complex general organization, seem to retain certain genome-related properties that are similar to amphibians. At the same time, the slope of regression between nucleosome formation potential and GC content is steeper in poikilothermal than in homeothermal genomes, which suggests that mammals and birds acquired certain common features of genomic organization.

Figures

Figure 1
Figure 1
Regression of heart index (ratio of heart mass to body mass) on genome size (circles, birds; squares, reptiles; triangles, mammals; diamonds, amphibians). Both lines are approximated by second-order polynomial regression (note that even in this case the regression for reptiles–birds looks linear). If approximated by linear regression, for reptiles–birds: r=−0.89, p<10−8, n=72; for amphibians–mammals: r=−0.92, p<10−8, n=66 (the difference between slopes of regression lines is highly significant, p<10−8). The regression holds within separate phylogenetic groups: birds, r=−0.58, p<10−4, n=53 (Spearman r=−0.53, p<10−4); reptiles, r=−0.82, p<10−4, n=19 (Spearman r=−0.75, p<10−3); mammals, r=−0.76, p<10−6, n=40 (Spearman r=−0.73, p<10−4); amphibians, r=−0.88, p<10−6, n=26 (Spearman r=−0.90, p<10−4); anurans, r=−0.61, p<0.01, n=16 (Spearman r=−0.73, p<0.01); caudata, r=−0.71, p<0.02, n=10 (Spearman r=−0.59, p<0.05). The significance levels for pair-wise differences between the slopes of regression lines: birds versus reptiles, p>0.8; mammals versus amphibians, p<0.01; anurans versus caudata, p>0.9. (Dotted lines, confidence intervals for p=0.95.) If controlled for body mass using multiple regression analysis, the picture was similar.
Figure 2
Figure 2
Regression of nucleosome formation potential on GC content in vertebrate genomes (green, human, r=−0.70, p<10−8; blue, chicken, r=−0.68, p<10−8; yellow, mouse, r=−0.68, p<10−8; red, clawed frog, r=−0.67, p<10−8; brown, zebrafish, r=−0.73, p<10−8; violet, tetraodon, r=−0.92, p<10−8). For each species, the nucleosome formation potential and GC content were determined for 10 000 sequences of 10 kb length, randomly extracted from genomic contigs (and averaged for each sequence over its length). (Dashed lines, confidence intervals for p=0.95.)
Figure 3
Figure 3
Genome size and erythrocyte nuclear volume. (a) Regression of nuclear volume on genome size (squares, reptiles–birds; circles, amphibians). For reptiles–birds: r=0.70, p<10−6, n=47; for amphibians: r=0.90, p<10−8, n=68. In linear regression, the difference between the intercepts is highly significant (p<10−4). (Dotted lines, confidence intervals for p=0.95.) (b) The difference in mean nuclear volume between the reptiles–birds and amphibians with the effect of genome size being removed using GLM (general linear model): means with 95% LSD (least significant difference) intervals (for difference, p<10−6).

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