Quantitative Approach to Fish Cytogenetics in the Context of Vertebrate Genome Evolution

Abstract

Our novel Python-based tool EVANGELIST allows the visualization of GC and repeats percentages along chromosomes in sequenced genomes and has enabled us to perform quantitative large-scale analyses on the chromosome level in fish and other vertebrates. This is a different approach from the prevailing analyses, i.e., analyses of GC% in the coding sequences that make up not more than 2% in human. We identified GC content (GC%) elevations in microchromosomes in ancient fish lineages similar to avian microchromosomes and a large variability in the relationship between the chromosome size and their GC% across fish lineages. This raises the question as to what extent does the chromosome size drive GC% as posited by the currently accepted explanation based on the recombination rate. We ascribe the differences found across fishes to varying GC% of repetitive sequences. Generally, our results suggest that the GC% of repeats and proportion of repeats are independent of the chromosome size. This leaves an open space for another mechanism driving the GC evolution in vertebrates.

Why Do Some Vertebrates Have Microchromosomes?

“…Generally, the GC-content of chromosomes increases exponentially with the reduction in chromosomal size (ICGSC, 2004 [ 52 , 120 , 121 ]; however, a few exceptions are evident. For instance, this tendency is not seen in most teleosts [ 122 ], whereas primitive fish such as lamprey show a significant association between GC% and chromosome sizes. Furthermore, amphibians, e.g., salamander and frog species ( Ambystoma mexicanum , Xenopus laevis , X. tropicalis ), do not show a correlation between GC% and chromosome size either [ 122 ].…”

“…For instance, this tendency is not seen in most teleosts [ 122 ], whereas primitive fish such as lamprey show a significant association between GC% and chromosome sizes. Furthermore, amphibians, e.g., salamander and frog species ( Ambystoma mexicanum , Xenopus laevis , X. tropicalis ), do not show a correlation between GC% and chromosome size either [ 122 ]. This indicates that GC% increases together with genome size in these instances, suggesting that lineages comprising several microchromosomes might be the counterparts of mammalian GC-rich chromosomal segments.…”

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

“…However, the isochore theory disregarded the tiny size of avian microchromosomes, increasing the recombination rate per megabase that elevates the regional GC% [40]. 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.…”

“…To visualize the effect of the sliding window size on the distribution of GC% values, we merged histograms originating from five different window sizes into single plots in a panel of fish and fish-like species with highly diversified genomes sizes, GC% and overall genome organization sensu [37]. The selected species include the highly fragmentary and GC-rich genome of lamprey with numerous tiny chromosomes (Lethenteron reissneri, ca.…”

Fish Cytogenetics: Present and Future

“…As GC% is associated with gene density and chromatin structure, the results could explain the inability to produce G-banding with traditional cytogenetic methods: in some species, it might provide an alternative occasional banding pattern along the chromosomes. The last paper compares chromosome size, genome size, GC% of repeats and proportion of repeats across fishes and with other vertebrates [ 29 ]. This quantitative approach showed that GC% of repeats and proportion of repeats are independent of chromosome size and disclosed an immense diversity in fish, spanning from the enrichment of GC% in the compact genomes observed in modern lineages to lower enrichment of GC% in the larger genomes present in basal fish lineages (with micro-chromosomes).…”