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Genomic organization and comparative chromosome mapping of the U1 snRNA gene in cichlid fish, with an emphasis in Oreochromis niloticus

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Abstract

To better understand genomic and chromosomal organization and evolutionary patterns of the U1 snRNA gene in cichlid fish, the gene was cytogenetically mapped and comparatively analyzed in 19 species belonging to several clades of the group. Moreover, the distribution and organization of U1 snRNA gene was analyzed in the Oreochromis niloticus genome. The results indicated high conservation of one chromosomal cluster of U1 snRNA in the African, Asian, and South American species, with few variations in the chromosomal position of the clusters in the South American species. The genomic analysis of U1 revealed a distinct scenario from that observed under the cytogenetic mapping. An enrichment of the U1 gene on linkage group (LG) 14 was observed that did not correspond to the same chromosome that harbors the U1 cluster identified by cytogenetic mapping. Moreover, it was revealed that the presence of several distinct transposable elements in the U1 gene flanking regions could be involved in the spreading of this sequence, but the generation of new, large snRNA clusters (detectable by fluorescent in situ hybridization, FISH) is apparently hampered. These results contribute to the understanding of multigene families' evolution and reinforce the utility of integrative analysis and the use of cytogenetic and bioinformatic methods to address the genomic and chromosomal evolutionary patterns of repeated DNAs among vertebrates. Moreover, the U1 gene represents a useful new chromosomal marker for cytogenetic studies.

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Abbreviations

aa:

Amino acid

BAC:

Bacterial artificial chromosome

CLDN13:

Claudin 13 gene

DAPI:

4′,6-Diamidino-2-phenylindole

FISH:

Fluorescence in situ hybridization

FR:

Flanking region

FRU:

Flanking region including the U1 gene

LG:

Linkage group

MYA:

Million years ago

NCBI:

National Center for Biotechnology Information

NTS:

Nontranscribed spacer

ORF:

Open reading frame

PCR:

Polymerase chain reaction

snRNA:

Small nuclear RNA

TE:

Transposable element

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Acknowledgements

The authors are grateful to PC Venere for the fieldwork assistance, J Mazzuchelli for assistance with BAC probes hybridization, and to T Kocher for providing animal sample and BAC clones. This study was supported by Fundação de Amparo a Pesquisa do Estado de São Paulo (FAPESP), Coordenadoria de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) from Brazil.

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Authors and Affiliations

  1. Departamento de Biologia, UNESP—Univ Estadual Paulista, Instituto de Biociências/IB, CEP 13506-900, Rio Claro, São Paulo, Brazil

    D. C. Cabral-de-Mello

  2. Departamento de Morfologia, UNESP—Univ Estadual Paulista, Instituto de Biociências/IB, Botucatu, São Paulo, Brazil

    G. T. Valente, R. T. Nakajima & C. Martins

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  1. D. C. Cabral-de-Mello
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  2. G. T. Valente
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  3. R. T. Nakajima
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  4. C. Martins
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Correspondence to D. C. Cabral-de-Mello.

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Responsible Editor: Fengtang Yang.

Electronic supplementary material

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Supplementary material S1

a U1 snRNA gene copies identified in the O. niloticus genome version Tilapia_broad_v1 that were used as queries in the blast search against the NCBI nucleotide collection. The number of copies and their relative scaffolds are described. The numbers indicated by “|” represent the start and end positions in the scaffold. Bold, E value of blastn search. b The sequences of FRs used as queries in the blast search against the NCBI nucleotide collection. Up and down descriptions indicate that the sequences are upstream or downstream of the respective U1 copies. The numbers indicated by “|” represent the start and end positions in the scaffold. c The FRU sequences used as queries in Repbase analysis. The numbers indicated by “|” represent the start and end positions in the scaffold. Underlined bases represent the putative U1 copies; the arrow represents the direction of transcription. d The aa residues of translated ORFs with positive results after analysis in Repbase. These sequences were used as queries in Pfam analysis. The numbers indicated by “|” represents the start and end positions in the scaffold (DOC 106 kb)

Supplementary material S2

Excluded regions of data presented in Fig. 1 (DOC 41 kb)

Supplementary material S3

Blast results using the U1 copies of O. niloticus as queries against the NCBI nucleotide collection (DOC 195 kb)

Supplementary material S4

Comparative analysis of blast results of U1_6 with other U1 results (DOC 70 kb)

Supplementary material S5

Selection of representative blast results using the FRs of U1 snRNA gene as queries in the search against the NCBI nucleotide collection (DOC 26 kb)

Supplementary material S6

Schematic representation of the overlap of the U1 copies (blue arrows) and U1_LV (Lytechinus variegatus; purple arrows). Box, details of the sequences of Lytechinus variegatus (purple arrows) and T. nigroviridis genomes (orange arrow). The sequence of new_U1 identified in Repbase and alignment with other U1 copies are also shown. The numbers indicated by “|” represent the start and end positions in the scaffold (DOC 1195 kb)

Supplementary material S7

The aa residues of translated ORFs with positive results after analysis in Repbase followed by a table with a summary of the results obtained. The colors indicate the positions of the TEs in the sequences. The numbers indicated by “|” represent the start and end positions in the scaffold (DOC 47 kb)

Supplementary material S8

Alignment of predicted aa residues of O. niloticus like-TEs and several TEs (L1-55_XT, L1-56_XT, KenoFr1, KenoDr1, Tx1-13). The yellow arrows indicate the Pfam identified domains (DOC 367 kb)

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Cabral-de-Mello, D.C., Valente, G.T., Nakajima, R.T. et al. Genomic organization and comparative chromosome mapping of the U1 snRNA gene in cichlid fish, with an emphasis in Oreochromis niloticus . Chromosome Res 20, 279–292 (2012). https://doi.org/10.1007/s10577-011-9271-y

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