Satellite DNAs Unveil Clues about the Ancestry and Composition of B Chromosomes in Three Grasshopper Species.

Diogo Milani,Rita Moura,Diogo Cabral-De-Mello,Hojun Song,Vanessa Bardella,Adriana Melo,Octavio Palacios-Gimenez,Ana Ferretti,Vilma Loreto

doi:10.3390/genes9110523

Abstract

Supernumerary (B) chromosomes are dispensable genomic elements occurring frequently among grasshoppers. Most B chromosomes are enriched with repetitive DNAs, including satellite DNAs (satDNAs) that could be implicated in their evolution. Although studied in some species, the specific ancestry of B chromosomes is difficult to ascertain and it was determined in only a few examples. Here we used bioinformatics and cytogenetics to characterize the composition and putative ancestry of B chromosomes in three grasshopper species, Rhammatocerus brasiliensis, Schistocerca rubiginosa, and Xyleus discoideus angulatus. Using the RepeatExplorer pipeline we searched for the most abundant satDNAs in Illumina sequenced reads, and then we generated probes used in fluorescent in situ hybridization (FISH) to determine chromosomal position. We used this information to infer ancestry and the events that likely occurred at the origin of B chromosomes. We found twelve, nine, and eighteen satDNA families in the genomes of R. brasiliensis, S. rubiginosa, and X. d. angulatus, respectively. Some satDNAs revealed clustered organization on A and B chromosomes varying in number of sites and position along chromosomes. We did not find specific satDNA occurring in the B chromosome. The satDNAs shared among A and B chromosomes support the idea of putative intraspecific ancestry from small autosomes in the three species, i.e., pair S11 in R. brasiliensis, pair S9 in S. rubiginosa, and pair S10 in X. d. angulatus. The possibility of involvement of other chromosomal pairs in B chromosome origin is also hypothesized. Finally, we discussed particular aspects in composition, origin, and evolution of the B chromosome for each species.

Highlights

Eukaryotic genomes exhibit repetitive DNA sequences including noncoding tandemly repeated satellite DNA
By combining genomics and cytogenetics, we aimed to elucidate the genome content of satellite DNAs (satDNAs) and used this information to track the possible ancestry of B chromosomes in three grasshopper species, Rhammatocerus brasiliensis (Acrididae: Gomphocerinae), Schistocerca rubiginosa (Acrididae: Cyrtacanthacridinae), and Xyleus discoideus angulatus (Romaleidae: Romaleinae) belonging to two families
Occurrence of a karyotype consisting of 2n = 23,X0, and presence of B chromosomes observed here for R. brasiliensis and X. d. angulatus were previously reported by different authors [14,35], including in the same population, i.e., Juazeiro do Norte/CE for X. d. angulatus [36]

Summary

Introduction

Eukaryotic genomes exhibit repetitive DNA sequences including noncoding tandemly repeated satellite DNA (satDNA). These sequences exhibit extensive variability in copy number and nucleotide sequence, even among phylogenetically related species. SatDNAs are frequently enriched on sex chromosomes and supernumerary (B) chromosomes, as they are greatly enriched in heterochromatin [1,2,3]. Supernumerary B chromosomes occur in approximately 15% of eukaryotes as dispensable elements (i.e., not required for normal organismal development), frequently heterochromatic and enriched repetitive DNAs, including the satDNAs, which can have implications for B chromosome evolution. SatDNAs have helped the understanding of the evolutionary history of B chromosomes with intraspecific (from host genome) or interspecific (resultant of species hybridization) origin, for example, in grasshoppers [7,8], wasps [9], fish [10], and plants [11], among others

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