Abstract
Supernumerary B chromosomes (Bs) are dispensable genetic elements widespread in eukaryotes and are poorly understood mainly in relation to mechanisms of maintenance and transmission. The cichlid Astatotilapia latifasciata can harbor Bs in a range of 0 (named B −) and 1–2 (named B +). The B in A. latifasciata is rich in several classes of repetitive DNA sequences, contains protein coding genes, and affects hosts in diverse ways, including sex-biased effects. To advance in the knowledge about the mechanisms of maintenance and transmission of B chromosomes in A. latifasciata, here, we studied the meiotic behavior in males and transmission rates of A. latifasciata B chromosome. We also analyzed structurally and functionally the predicted B chromosome copies of the cell cycle genes separin-like, tubb1-like and kif11-like. We identified in the meiotic structure relative to the B chromosome the presence of proteins associated with Synaptonemal Complex organization (SMC3, SYCP1 and SYCP3) and found that the B performs self-pairing. These data suggest that isochromosome formation was a step during B chromosome evolution and this element is in a stage of diversification of the two arms keeping the self-pairing behavior to protect the A chromosome complement of negative effects of recombination. Moreover, we observed no occurrence of B-drive and confirmed the presence of cell cycle genes copies in the B chromosome and their transcription in encephalon, muscle and gonads, which can indicates beneficial effects to hosts and contribute to B maintenance.
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Availability of data and materials
The datasets used in the current study are available at SaciBase database (http://186.217.131.253/jbrowse/JBrowse-1.12.1/) and from the corresponding author on reasonable request.
Abbreviations
- 5mC:
-
5-Methylcytosine
- 5hmC:
-
5-Hydroxymethylcytosine
- AE:
-
Axial elements
- B:
-
B chromosome
- B −:
-
Sample without B chromosome
- B + :
-
Sample with B chromosome
- BncDNA:
-
B chromosome noncoding DNA
- DAPI:
-
4',6-Diamidino-2-phenylindole, dihydrochloride
- DTT:
-
Dithiothreitol
- FB −:
-
Female without B chromosome
- FB + :
-
Female with B chromosome
- FISH:
-
Fluorescent in situ hybridization
- GDR:
-
Gene dose ratio
- KCl:
-
Potassium chloride
- kif11-like :
-
Kinesin-like protein
- MB −:
-
Male without B chromosome
- MB + :
-
Male with B chromosome
- LE:
-
Lateral elements
- PBS:
-
Phosphate-buffered saline
- PCR:
-
Polymerase chain reaction
- qPCR:
-
Quantitative PCR
- RT:
-
Reverse transcription
- RT-PCR:
-
Reverse transcription PCR
- RT-qPCR:
-
Quantitative reverse transcription PCR
- SMC3:
-
Structural maintenance of chromosomes 3
- SYCP1:
-
Synaptonemal complex protein 1
- SYCP3:
-
Synaptonemal complex protein 3
- tubb1-like :
-
Tubulin beta-1 chain-like
- SaciBase:
-
Search and analysis for cytogenomic integration database
- SC:
-
Synaptonemal complex
- SIM:
-
Structured-illumination microscopy
- SNV:
-
Single nucleotide variation
- SSC:
-
Saline-sodium citrate
- ubce :
-
Ubiquitin-conjugating enzyme
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Funding
This work was supported by grants from the São Paulo Research Foundation (FAPESP) (grant numbers 2013/19898-7; 2013/25234-4; 2014/15756-6; 2015/16661-1; 2016/03912-9; 2016/07743-7; 2017/07484-4) and the National Counsel of Technological and Scientific Development (CNPq) (305321/2015-3; 304111/2020-1) to C.M. laboratory team as well as the German Science Foundation (DFG) grant Be1168/8-1 to R.B.
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ALC: performed cytogenetic analyses, sperm-FISH experiments and active B-copies validation, and write the manuscript. NBV: performed immunodetection and crossing experiments, and write the manuscript. IC: performed immunodetection experiments. FMSP: performed bioinformatics analyses. DM: performed sperm-FISH experiments. RAO: performed statistical analyses. RB: designed and contributed to immunodetection experiments. CM: conceived the study and participated in its design and coordination.
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Cardoso, A.L., Venturelli, N.B., da Cruz, I. et al. Meiotic behavior, transmission and active genes of B chromosomes in the cichlid Astatotilapia latifasciata: new clues about nature, evolution and maintenance of accessory elements. Mol Genet Genomics 297, 1151–1167 (2022). https://doi.org/10.1007/s00438-022-01911-4
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DOI: https://doi.org/10.1007/s00438-022-01911-4