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Out of patterns, the euchromatic B chromosome of the grasshopper Abracris flavolineata is not enriched in high-copy repeats

Abstract

In addition to the normal set of standard (A) chromosomes, some eukaryote species harbor supernumerary (B) chromosomes. In most cases, B chromosomes show differential condensation with respect to A chromosomes and display dark C-bands of heterochromatin, and some of them are highly enriched in repetitive DNA. Here we perform a comprehensive NGS (next-generation sequencing) analysis of the repeatome in the grasshopper Abracris flavolineata aimed at uncovering the molecular composition and origin of its B chromosome. Our results have revealed that this B chromosome shows a DNA repeat content highly similar to the DNA repeat content observed for euchromatic (non-C-banded) regions of A chromosomes. Moreover, this B chromosome shows little enrichment for high-copy repeats, with only a few elements showing overabundance in B-carrying individuals compared to the 0B individuals. Consequently, the few satellite DNAs (satDNAs) mapping on the B chromosome were mostly restricted to its centromeric and telomeric regions, and they displayed much smaller bands than those observed on the A chromosomes. Our data support the intraspecific origin of the B chromosome from the longest autosome by misdivision, isochromosome formation, and additional restructuring, with accumulation of specific repeats in one or both B chromosome arms, yielding a submetacentric B. Finally, the absence of B-specific satDNAs, which are frequent in other species, along with its euchromatic nature, suggest that this B chromosome arose recently and might still be starting a heterochromatinization process. On this basis, it could be a good model to investigate the initial steps of B chromosome evolution.

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Fig. 1: Relative abundance of several types of repetitive DNA in A. flavolineata genomes carrying 1B and 2B, in comparison with the B-lacking genome, measured by the log2 transformed 1B/0B and 2B/0B quotients.
Fig. 2: Comparative genomic proportion between the 0B, 1B, and 2B genomes for the most abundant TEs in Abracris flavolineata.
Fig. 3: Subtractive repetitive landscape (genome proportion versus sequence divergence based on Kimura substitution level) obtained from average counts for satDNAs in two males with 2B chromosomes and three with no B chromosome of Abracris flavolineata.
Fig. 4: Comparative genomic proportion and FISH mapping for eight satDNAs occurring in the B chromosomes with a banded pattern.
Fig. 5: Comparative C-banding and FISH for repeat location between the L1 and B chromosomes of A. flavolineata.

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Acknowledgements

We acknowledge the three anonymous reviewers for helpful comments that contributed significantly to improve the manuscript. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES), by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (process numbers 2014/11763-8 and 2015/16661-1), and Conselho Nacional de Desenvolvimento Científiico e Tecnológico (CNPq). DCC-d-M is a recipient of a research productivity fellowship from the Conselho Nacional de Desenvolvimento Científico e Tecnológico-CNPq (process number 308290/2020-8). FJRR hold posdoctoral fellowships from Junta de Andalucía fellowship (Spain), Sven och Lilly Lawskis fond (Sweden), and a Marie Skłodowska-Curie Individual Fellowship (grant agreement 875732, European Commission).

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DM and DCC-d-M conceived the study; DM and FJRR performed the bioinformatic analysis; DM performed the chromosomal analysis; DM, FJRR, JPMC, and DCC-d-M performed formal data analysis and wrote the paper; DCC-d-M led the project management. All authors read and approved the manuscript..

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Correspondence to Diogo C. Cabral-de-Mello.

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Milani, D., Ruiz-Ruano, F.J., Camacho, J.P.M. et al. Out of patterns, the euchromatic B chromosome of the grasshopper Abracris flavolineata is not enriched in high-copy repeats. Heredity 127, 475–483 (2021). https://doi.org/10.1038/s41437-021-00470-5

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