Uncovering the molecular organization of unusual highly scattered 5S rDNA: The case of Chariesterus armatus (Heteroptera)

Abstract

One cluster of 5S rDNA per haploid genome is the most common pattern among Heteroptera. However, in Chariesterus armatus, highly scattered signals were noticed. We isolated and characterized the entire 5S rDNA unit of C. armatus aiming to a deeper knowledge of molecular organization of the 5S rDNA among Heteroptera and to understand possible causes and consequences of 5S rDNA chromosomal spreading. For a comparative analysis, we performed the same approach in Holymenia histrio with 5S rDNA restricted to one bivalent. Multiple 5S rDNA variants were observed in both species, though they were more variable in C. armatus, with some of variants corresponding to pseudogenes. These pseudogenes suggest birth-and-death mechanism, though homogenization was also observed (concerted evolution), indicating evolution through mixed model. Association between transposable elements and 5S rDNA was not observed, suggesting spreading of 5S rDNA through other mechanisms, like ectopic recombination. Scattered organization is a rare example for 5S rDNA, and such organization in C. armatus genome could have led to the high diversification of sequences favoring their pseudogenization.

The relevance of chromosome fissions for major ribosomal DNA dispersion in hymenopteran insects

“…We also found that the occurrence of rDNA loci in certain sites on chromosomes are more prone to diverge in sequence between them. This was noticed for other repetitive DNAs—for example, satellite DNA in Drosophila melanogaster (Kuhn et al., 2012) and Holhymenia histrio (Heteroptera) (Bardella et al., 2020), and 5S rDNA in Chariesterus armatus (Heteroptera) (Bardella & Cabral‐de‐Mello, 2018).…”

Cytogenomic analysis unveils mixed molecular evolution and recurrent chromosomal rearrangements shaping the multigene families onSchistocercagrasshopper genomes

“…At the same time, the concerted evolution is responsible for maintaining the array by the homogenization of units, and can also foster the fixation of new variants by spreading them throughout the other arrays. A mixed model of multigene family evolution as observed here for Schistocerca has been observed in fishes (Pinhal et al 2011;Cabral-de-Mello et al 2012) and other invertebrates, including grasshoppers (Freire et al 2010;Anjos et al 2015;Bardella and Cabral-de-Mello 2018).…”

“…Persisting copies may then suffer divergence by mutations and sub-or neofunctionalization, or pseudogenization (Hughes and Nei 1992;Nei and Rooney 2005;Eirin-Lopez et al 2012). Recent studies suggested a mixed effect of concerted and birth-and-death evolution to be involved in some multigene families dynamics (Mount et al 2007;Freire et al 2010;Pinhal et al 2011;Merlo et al 2012; Bardella and Cabral-de-Mello 2018;Zhang et al 2021).…”