Long-read genome assembly of the insect model organismTribolium castaneumreveals extensive propagation of satellite DNA long arrays in gene-rich regions

Abstract

AbstractEukaryotic genomes are replete with satellite DNAs (satDNAs), large stretches of tandemly repeated sequences which are mostly underrepresented in genome assemblies. As a result, we know little about their spread, movement, and rearrangement across the genome or about their potential impact on the genome. Here, we have combined Oxford Nanopore long-read sequencing with a reference-guided assembly approach to generate a new, high-quality genome assembly (TcasONT) of the model beetleTribolium castaneum. The new TcasONT is enriched by 50 Mb in the repetitive genome part, which is as much as 1/4 ofT. castaneumgenome size. Therefore, we used the enhanced assembly to conduct global and in-depth analyses of abundant non-(peri)centromeric satDNAs, Cast1-Cast9. We found a large proportion of long arrays of Cast1-Cast9 satDNAs embedded in gene-rich regions. In addition, occurrence of Cast1-Cast9 satDNAs and transposable elements often did not overlap. Contrary to accepted opinion, our finding clearly speaks to the ability of satDNAs to expand in gene-rich regions and also demonstrate the flexibility of gene-rich regions to tolerate and accommodate satDNA sequences. In addition, we found that suppressed recombination on X chromosomes has less effect on the spread of Cast1-Cast9 satDNAs, but rather tolerates amplification of these satDNAs into longer arrays. Our results also show the extensive spread of Cast1-Cast9 satDNAs, characterized by distribution along the entire chromosome length and between different chromosomes. This observed pattern points out very efficient mechanisms of propagation of satDNAs on the whole genome scale including gene-rich regions. The presence of such a large portion of satDNAs with extensive propagation and amplification potential in gene-rich regions of theT. castaneumgenome can strongly influence both gene expression and the dynamics of genome evolution.