Dataset Information

Genetic Characteristic and RNA-Seq Analysis in Transparent Mutant of Carp-Goldfish Nucleocytoplasmic Hybrid.

ABSTRACT: In teleost, pigment in the skin and scales played important roles in various biological processes. Iridophores, one of the main pigment cells in teleost, could produce silver pigments to reflect light. However, the specific mechanism of the formation of silver pigments is still unclear. In our previous study, some transparent mutant individuals were found in the carp-goldfish nucleocytoplasmic hybrid (CyCa hybrid) population. In the present study, using transparent mutants (TM) and wild type (WT) of the CyCa hybrid as a model, firstly, microscopic observations showed that the silver pigments and melanin were both lost in the scales of transparent mutants compared to that in wild types. Secondly, genetic study demonstrated that the transparent trait in the CyCa hybrid was recessively inherent, and controlled by an allele in line with Mendelism. Thirdly, RNA-Seq analysis showed that differential expression genes (DEGs) between wild type and transparent mutants were mainly enriched in the metabolism of guanine, such as hydrolase, guanyl nucleotide binding, guanyl ribonucleotide binding, and GTPase activity. Among the DEGs, purine nucleoside phosphorylase 4a (pnp4a) and endothelin receptor B (ednrb) were more highly expressed in the wild type compared to the transparent mutant (p < 0.05). Finally, miRNA-Seq analysis showed that miRNA-146a and miR-153b were both more highly expressed in the transparent mutant compared to that in wild type (p < 0.05). Interaction analysis between miRNAs and mRNAs indicated that miRNA-146a was associated with six DEGs (MGAT5B, MFAP4, GP2, htt, Sema6b, Obscn) that might be involved in silver pigmentation.

SUBMITTER: Zhou L

PROVIDER: S-EPMC6771007 | biostudies-literature | 2019 Sep

REPOSITORIES: biostudies-literature

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Genetic Characteristic and RNA-Seq Analysis in Transparent Mutant of Carp-Goldfish Nucleocytoplasmic Hybrid.

Zhou Lingling L Liang Hongwei H Zhou Xiaoyun X Jia Jingyi J Ye Cheng C Hu Qiongyao Q Xu Shaohua S Yu Yongning Y Zou Guiwei G Hu Guangfu G

Genes 20190912 9

In teleost, pigment in the skin and scales played important roles in various biological processes. Iridophores, one of the main pigment cells in teleost, could produce silver pigments to reflect light. However, the specific mechanism of the formation of silver pigments is still unclear. In our previous study, some transparent mutant individuals were found in the carp-goldfish nucleocytoplasmic hybrid (CyCa hybrid) population. In the present study, using transparent mutants (TM) and wild type (WT ...[more]

PMID: 31547242

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Project description:Previously, a homodiploid goldfish-like fish (2n = 100; GF-L) was spontaneously generated by self-crossing a homodiploid red crucian carp-like fish (2n = 100; RCC-L), which was in turn produced via the distant hybridization of female koi carp (Cyprinus carpio haematopterus, KOC, 2n = 100) and male blunt snout bream (Megalobrama amblycephala, BSB, 2n = 48). The phenotypes and genotypes of RCC-L and GF-L differed from those of the parental species but were similar to diploid red crucian carp (2n = 100; RCC) and goldfish (2n = 100; GF), respectively. We sequenced the complete mitochondrial DNAs (mtDNAs) of the KOC, BSB, RCC-L, GF-L, and subsequent generations produced by self-crossing [the self-mating offspring of RCC-L (RCC-L-F2) to the self-mating offspring of RCC-L-F2 (RCC-L-F3) and the self-mating offspring of GF-L (GF-L-F2)]. Paternal mtDNA fragments were stably embedded in the mtDNAs of both lineages, forming chimeric DNA fragments. In addition to these chimeras, several nucleotide positions in the RCC-L and GF-L lineages differed from the parental bases, and were instead identical with RCC and GF, respectively. Moreover, RCC-L and GF-L mtDNA organization and nucleotide composition were more similar to those of RCC and GF, respectively, compared to parental mtDNA. Finally, phylogenetic analyses indicated that RCC-L and GF-L clustered with RCC and GF, not with the parental species. The molecular dating time shows that the divergence time of KOC and GF was about 21.26 Mya [95% highest posterior density (HPD): 24.41-16.67 Mya], which fell within the period of recent. The heritable chimeric DNA fragments and mutant loci identified in the mtDNA of the RCC-L and GF-L lineages provided important evidence that hybridizations might lead to changes in the mtDNA and the subsequent generation of new lineages. Our findings also demonstrated for the first time that the paternal mtDNA was transmitted into the mtDNA of homodiploid lineages (RCC-L and GF-L), which provided evidence that paternal DNA plays a role in inherited mtDNA. These evolutionary analyses in mtDNA suggest that GF might have diverged from RCC after RCC diverged from koi carp.

Project description:Incompatibilities between the nucleus and the cytoplasm of sufficiently distant species result in developmental arrest of hybrid and nucleocytoplasmic hybrid (cybrid) embryos. Several hypotheses have been proposed to explain their lethality, including problems in embryonic genome activation (EGA) and/or nucleo-mitochondrial interactions. However, conclusive identification of the causes underlying developmental defects of cybrid embryos is still lacking. We show here that while over 80% of both Xenopus laevis and Xenopus (Silurana) tropicalis same-species androgenetic haploids develop to the swimming tadpole stage, the androgenetic cybrids formed by the combination of X. laevis egg cytoplasm and X. tropicalis sperm nucleus invariably fail to gastrulate properly and never reach the swimming tadpole stage. In spite of this arrest, these cybrids show quantitatively normal EGA and energy levels at the stage where their initial gastrulation defects are manifested. The nucleocytoplasmic incompatibility between these two species instead results from a combination of factors, including a reduced emission of induction signal from the vegetal half, a decreased sensitivity of animal cells to induction signals, and differences in a key embryonic protein (Xbra) concentration between the two species, together leading to inefficient induction and defective convergence-extension during gastrulation. Indeed, increased exposure to induction signals and/or Xbra signalling partially rescues the induction response in animal explants and whole cybrid embryos. Altogether, our study demonstrates that the egg cytoplasm of one species may not support the development promoted by the nucleus of another species, even if this nucleus does not interfere with the cytoplasmic/maternal functions of the egg, while the egg cytoplasm is also capable of activating the genome of that nucleus. Instead, our results provide evidence that inefficient signalling and differences in the concentrations of key proteins between species lead to developmental defects in cybrids. Finally, they show that the incompatibilities of cybrids can be corrected by appropriate treatments.

Dataset Information

Genetic Characteristic and RNA-Seq Analysis in Transparent Mutant of Carp-Goldfish Nucleocytoplasmic Hybrid.

Publications

Genetic Characteristic and RNA-Seq Analysis in Transparent Mutant of Carp-Goldfish Nucleocytoplasmic Hybrid.

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