Advances in Vertebrate (Cyto)Genomics Shed New Light on Fish Compositional Genome Evolution

Abstract

Cytogenetic and compositional studies considered fish genomes rather poor in guanine-cytosine content (GC%) because of a putative “sharp increase in genic GC% during the evolution of higher vertebrates”. However, the available genomic data have not been exploited to confirm this viewpoint. In contrast, further misunderstandings in GC%, mostly of fish genomes, originated from a misapprehension of the current flood of data. Utilizing public databases, we calculated the GC% in animal genomes of three different, technically well-established fractions: DNA (entire genome), cDNA (complementary DNA), and cds (exons). Our results across chordates help set borders of GC% values that are still incorrect in literature and show: (i) fish in their immense diversity possess comparably GC-rich (or even GC-richer) genomes as higher vertebrates, and fish exons are GC-enriched among vertebrates; (ii) animal genomes generally show a GC-enrichment from the DNA, over cDNA, to the cds level (i.e., not only the higher vertebrates); (iii) fish and invertebrates show a broad(er) inter-quartile range in GC%, while avian and mammalian genomes are more constrained in their GC%. These results indicate no sharp increase in the GC% of genes during the transition to higher vertebrates, as stated and numerously repeated before. We present our results in 2D and 3D space to explore the compositional genome landscape and prepared an online platform to explore the AT/GC compositional genome evolution.

Abandoning the Isochore Theory Can Help Explain Genome Compositional Organization in Fish

“…A quantitative approach adding fish cytogenomics to GC biology research that was traditionally focused on birds and mammals revealed a large variability in the relationship between the chromosome size and their GC% across fish lineages [37]. Moreover, a recent study also falsified the putative "sharp increase in genic GC% during the evolution of birds and mammals" [27] proposed by Bernardi [26] along with the isochore theory. This means that a new viewpoint is needed to explore and explain the AT/GC heterogeneity in eukaryotes.…”

“…The overall genome size is roughly two and a half times higher in mammals than in teleost fishes. Despite these pronounced differences in chromosome and genome size, fish genomes have comparable GC% values [27] although they have undergone an additional whole-genome duplication [38].…”

“…Proponents of the gBGC mostly explore protein-coding regions (exons) that are, however, of a rather negligible genomic proportion (e.g., approx. 1.5% in the human genome [44] to about 5-10% in fish, [27]), and (2) the neo-selection hypothesis explaining GC-rich isochores as an adaptation to the increased body temperature in homeotherms [26]. However, the mammalian-like AT/GC heterogeneity in the cold-blooded ancient gars excludes both these directions because (1) according to the gBGC, the significantly smaller chromosome size should result in higher GC% values in fishes because of the stronger recombination, and (2) gars are cold-blooded vertebrates with their body temperature dependent on the environment (discussed in detail by [5]).…”

“…To explain the compositional differences between anamniotes and amniotes, authors of the isochore theory coined the concept of a "compositional transition" [24,25], stating that "during evolution of reptiles towards birds and mammals, the gene-rich, moderately GC-rich isochores of the ancestors underwent a GC increase" [26]. However, a recent study showed that no such compositional transition occurred since the GC% of fish coding regions is higher than in birds and mammals [27].…”

Rapid Targeted Assembly of the Proteome Reveals Evolutionary Variation of GC Content in Avian Lice

“…A disproportionate amount of genomic research has focused on vertebrate groups, particularly mammals and birds. 20 , 21 Insects have been given much less attention yet are the most diverse group of animals in the world 22 and are facing catastrophic declines. 23 Parasitic lice (Phthiraptera) are of particular interest due to their global distribution, fast rate of evolution, and high level of diversification, 24 - 28 providing an ideal system to study GC content and protein evolution in a closely related group of organisms 29 .…”