Differential expression of miRNAs in the presence of B chromosome in the cichlid fish Astatotilapia latifasciata

Jordana Inácio Nascimento-Oliveira; Bruno Evaristo Almeida Fantinatti; Ivan Rodrigo Wolf; Adauto Lima Cardoso; Erica Ramos; Nathalie Rieder; Rogerio de Oliveira; Cesar Martins

doi:10.1186/s12864-021-07651-w

Differential expression of miRNAs in the presence of B chromosome in the cichlid fish Astatotilapia latifasciata

BMC Genomics. 2021 May 12;22(1):344. doi: 10.1186/s12864-021-07651-w.

Authors

Jordana Inácio Nascimento-Oliveira¹, Bruno Evaristo Almeida Fantinatti², Ivan Rodrigo Wolf¹, Adauto Lima Cardoso¹, Erica Ramos¹, Nathalie Rieder³, Rogerio de Oliveira⁴, Cesar Martins⁵

Affiliations

¹ Department of Structural and Functional Biology, Institute of Bioscience at Botucatu, São Paulo State University (UNESP), Botucatu, SP, 18618-689, Brazil.
² Medical School, University of Ninth of July (UNINOVE), Bauru, SP, Brazil.
³ Faculty of Mathematics and Natural Sciences, University of Bonn, Bonn, Germany.
⁴ Department of Biostatistics, Plant Biology, Parasitology and Zoology, Institute of Bioscience at Botucatu, São Paulo State University (UNESP), Botucatu, SP, Brazil.
⁵ Department of Structural and Functional Biology, Institute of Bioscience at Botucatu, São Paulo State University (UNESP), Botucatu, SP, 18618-689, Brazil. cesar.martins@unesp.br.

Abstract

Background: B chromosomes (Bs) are extra elements observed in diverse eukaryotes, including animals, plants and fungi. Although Bs were first identified a century ago and have been studied in hundreds of species, their biology is still enigmatic. Recent advances in omics and big data technologies are revolutionizing the B biology field. These advances allow analyses of DNA, RNA, proteins and the construction of interactive networks for understanding the B composition and behavior in the cell. Several genes have been detected on the B chromosomes, although the interaction of B sequences and the normal genome remains poorly understood.

Results: We identified 727 miRNA precursors in the A. latifasciata genome, 66% which were novel predicted sequences that had not been identified before. We were able to report the A. latifasciata-specific miRNAs and common miRNAs identified in other fish species. For the samples carrying the B chromosome (B⁺), we identified 104 differentially expressed (DE) miRNAs that are down or upregulated compared to samples without B chromosome (B^-) (p < 0.05). These miRNAs share common targets in the brain, muscle and gonads. These targets were used to construct a protein-protein-miRNA network showing the high interaction between the targets of differentially expressed miRNAs in the B⁺ chromosome samples. Among the DE-miRNA targets there are protein-coding genes reported for the B chromosome that are present in the protein-protein-miRNA network. Additionally, Gene Ontology (GO) terms related to nuclear matrix organization and response to stimulus are exclusive to DE miRNA targets of B⁺ samples.

Conclusions: This study is the first to report the connection of B chromosomes and miRNAs in a vertebrate species. We observed that the B chromosome impacts the miRNAs expression in several tissues and these miRNAs target several mRNAs involved with important biological processes.

Keywords: Cichlid; Fish; Genomic; RNA-seq; Selfish element; Small noncoding RNAs; Supernumerary chromosome; Teleost; Transcriptome.

MeSH terms

Animals
Chromosomes / genetics
Cichlids* / genetics
Gene Expression Profiling
Gene Ontology
Genome
MicroRNAs* / genetics

Substances

MicroRNAs