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

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.

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B Chromosomes in Populations of Mammals Revisited

Genes ◽

10.3390/genes9100487 ◽

2018 ◽

Vol 9 (10) ◽

pp. 487 ◽

Cited By ~ 11

Author(s):

Mladen Vujošević ◽

Marija Rajičić ◽

Jelena Blagojević

Keyword(s):

Mammalian Species ◽

B Chromosome ◽

Molecular Techniques ◽

B Chromosomes ◽

General View ◽

Protein Coding ◽

Host Parasite Interactions ◽

Quantitative Characteristics ◽

Host Parasite

The study of B chromosomes (Bs) started more than a century ago, while their presence in mammals dates since 1965. As the past two decades have seen huge progress in application of molecular techniques, we decided to throw a glance on new data on Bs in mammals and to review them. We listed 85 mammals with Bs that make 1.94% of karyotypically studied species. Contrary to general view, a typical B chromosome in mammals appears both as sub- or metacentric that is the same size as small chromosomes of standard complement. Both karyotypically stable and unstable species possess Bs. The presence of Bs in certain species influences the cell division, the degree of recombination, the development, a number of quantitative characteristics, the host-parasite interactions and their behaviour. There is at least some data on molecular structure of Bs recorded in nearly a quarter of species. Nevertheless, a more detailed molecular composition of Bs presently known for six mammalian species, confirms the presence of protein coding genes, and the transcriptional activity for some of them. Therefore, the idea that Bs are inert is outdated, but the role of Bs is yet to be determined. The maintenance of Bs is obviously not the same for all species, so the current models must be adapted while bearing in mind that Bs are not inactive as it was once thought.

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Genomic Characterization of a B Chromosome in Lake Malawi Cichlid Fishes

10.20944/preprints201811.0110.v1 ◽

2018 ◽

Author(s):

Frances Clark ◽

Matthew Conte ◽

Thomas Kocher

Keyword(s):

Dna Sequence ◽

Sequence Data ◽

Cichlid Fish ◽

B Chromosome ◽

Lake Malawi ◽

B Chromosomes ◽

Sequence Coverage ◽

Specific Sequence ◽

Genomic Characterization ◽

B Chromosome Evolution

B chromosomes (Bs) were discovered a century ago, and since then most studies have focused on describing their distribution and abundance using traditional cytogenetics. Only recently have attempts been made to understand their structure and evolution at the level of DNA sequence. Many questions regarding the origin, structure, function and evolution of B chromosomes remain unanswered. Here we identify B chromosome sequences from several species of cichlid fish from Lake Malawi by examining the ratios of DNA sequence coverage in individuals with and without B chromosomes. We examine the efficiency of this method, and compare results using both Illumina and PacBio sequence data. The B chromosome sequences detected in 13 individuals from 7 species were compared to assess the rates of sequence replacement. B-specific sequence common to at least 12 of the 13 datasets are identified as the “Core” B chromosome. The location of B sequence homologs throughout the genome provides further support for theories of B chromosome evolution. Finally, we identified candidate genes located on the B chromosome which may regulate the segregation and maintenance of the B chromosome.

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Changing sex for selfish gain: B chromosomes of Lake Malawi cichlid fish

Scientific Reports ◽

10.1038/s41598-019-55774-8 ◽

2019 ◽

Vol 9 (1) ◽

Cited By ~ 6

Author(s):

Frances E. Clark ◽

Thomas D. Kocher

Keyword(s):

Linkage Group ◽

Transmission Rate ◽

Cichlid Fish ◽

Meiotic Drive ◽

B Chromosome ◽

Lake Malawi ◽

B Chromosomes ◽

Normal Complement ◽

Biased Sex Ratio ◽

Average Transmission

AbstractB chromosomes are extra, non-essential chromosomes present in addition to the normal complement of A chromosomes. Many species of cichlid fish in Lake Malawi carry a haploid, female-restricted B chromosome. Here we show that this B chromosome exhibits drive, with an average transmission rate of 70%. The offspring of B-transmitting females exhibit a strongly female-biased sex ratio. Genotyping of these offspring reveals the B chromosome carries a female sex determiner that is epistatically dominant to an XY system on linkage group 7. We suggest that this sex determiner evolved to enhance the meiotic drive of the B chromosome. This is some of the first evidence that female meiotic drive can lead to the invasion of new sex chromosomes solely to benefit the driver, and not to compensate for skewed sex ratios.

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Long-term persistence of supernumerary B chromosomes in multiple species of Astyanax fish

BMC Biology ◽

10.1186/s12915-021-00991-9 ◽

2021 ◽

Vol 19 (1) ◽

Author(s):

Duílio Mazzoni Zerbinato de Andrade Silva ◽

Francisco J. Ruiz-Ruano ◽

Ricardo Utsunomia ◽

María Martín-Peciña ◽

Jonathan Pena Castro ◽

...

Keyword(s):

B Chromosome ◽

B Chromosomes ◽

Population Divergence ◽

Nucleotide Polymorphisms ◽

Term Survival ◽

Single Nucleotide ◽

Protein Coding ◽

Species Formation ◽

Multiple Species

Abstract Background Eukaryote genomes frequently harbor supernumerary B chromosomes in addition to the “standard” A chromosome set. B chromosomes are thought to arise as byproducts of genome rearrangements and have mostly been considered intraspecific oddities. However, their evolutionary transcendence beyond species level has remained untested. Results Here we reveal that the large metacentric B chromosomes reported in several fish species of the genus Astyanax arose in a common ancestor at least 4 million years ago. We generated transcriptomes of A. scabripinnis and A. paranae 0B and 1B individuals and used these assemblies as a reference for mapping all gDNA and RNA libraries to quantify coverage differences between B-lacking and B-carrying genomes. We show that the B chromosomes of A. scabripinnis and A. paranae share 19 protein-coding genes, of which 14 and 11 were also present in the B chromosomes of A. bockmanni and A. fasciatus, respectively. Our search for B-specific single-nucleotide polymorphisms (SNPs) identified the presence of B-derived transcripts in B-carrying ovaries, 80% of which belonged to nobox, a gene involved in oogenesis regulation. Importantly, the B chromosome nobox paralog is expressed > 30× more than the A chromosome paralog. This indicates that the normal regulation of this gene is altered in B-carrying females, which could potentially facilitate B inheritance at higher rates than Mendelian law prediction. Conclusions Taken together, our results demonstrate the long-term survival of B chromosomes despite their lack of regular pairing and segregation during meiosis and that they can endure episodes of population divergence leading to species formation.

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Genomic Characterization of a B Chromosome in Lake Malawi Cichlid Fishes

Genes ◽

10.3390/genes9120610 ◽

2018 ◽

Vol 9 (12) ◽

pp. 610 ◽

Cited By ~ 9

Author(s):

Frances E. Clark ◽

Matthew A. Conte ◽

Thomas D. Kocher

Keyword(s):

Dna Sequence ◽

Sequence Data ◽

Cichlid Fish ◽

B Chromosome ◽

Lake Malawi ◽

B Chromosomes ◽

Sequence Coverage ◽

Specific Sequence ◽

Genomic Characterization ◽

B Chromosome Evolution

B chromosomes (Bs) were discovered a century ago, and since then, most studies have focused on describing their distribution and abundance using traditional cytogenetics. Only recently have attempts been made to understand their structure and evolution at the level of DNA sequence. Many questions regarding the origin, structure, function, and evolution of B chromosomes remain unanswered. Here, we identify B chromosome sequences from several species of cichlid fish from Lake Malawi by examining the ratios of DNA sequence coverage in individuals with or without B chromosomes. We examined the efficiency of this method, and compared results using both Illumina and PacBio sequence data. The B chromosome sequences detected in 13 individuals from 7 species were compared to assess the rates of sequence replacement. B-specific sequence common to at least 12 of the 13 datasets were identified as the “Core” B chromosome. The location of B sequence homologs throughout the genome provides further support for theories of B chromosome evolution. Finally, we identified genes and gene fragments located on the B chromosome, some of which may regulate the segregation and maintenance of the B chromosome.

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Evolutionary success of a parasitic B chromosome rests on gene content

10.1101/683417 ◽

2019 ◽

Cited By ~ 1

Author(s):

Francisco J. Ruiz-Ruano ◽

Beatriz Navarro-Domínguez ◽

María Dolores López-León ◽

Josefa Cabrero ◽

Juan Pedro M. Camacho

Keyword(s):

De Novo ◽

Large Subunit ◽

B Chromosome ◽

B Chromosomes ◽

Anaphase Promoting Complex ◽

Protein Coding ◽

Migratory Locust ◽

Similar Frequency ◽

Protein Coding Genes ◽

Evolutionary Success

AbstractSupernumerary (B) chromosomes are dispensable genomic elements found in most kinds of eukaryotic genomes. Many show drive mechanisms that give them an advantage in transmission, but how they achieve it remains a mystery. The recent finding of protein-coding genes in B chromosomes has opened the possibility that their evolutionary success is based on their genetic content. Using a protocol based on mapping genomic DNA Illumina reads from B-carrying and B-lacking individuals on the coding sequences of de novo transcriptomes from the same individuals, we identified 25 protein-coding genes in the B chromosome of the migratory locust, 15 of which showed a full coding region. Remarkably, one of these genes (apc1) codes for the large subunit of the Anaphase Promoting Complex or Cyclosome (APC/C), an E3 ubiquitin ligase involved in the metaphase-anaphase transition. Sequence comparison of A and B chromosome gene paralogs showed that the latter show B-specific nucleotide changes, neither of which putatively impairs protein function. These nucleotide signatures allowed identifying B-derived transcripts in B-carrying transcriptomes, and demonstrated that they show about similar frequency as A-derived ones. Since B-carrying individuals show higher amounts of apc1 transcripts than B-lacking ones, the putatively higher amount of APC1 protein might induce a faster metaphase-anaphase transition in spite of orientation of the two B chromosome chromatids towards the same pole during metaphase, thus facilitating B chromosome non-disjunction. Therefore, apc1 is the first protein-coding gene uncovered in a B chromosome that might be responsible for B chromosome drive.Significance StatementThe genome of the migratory locust harbors a parasitic chromosome that arose about 2 million years ago. It is widespread in natural populations from Asia, Africa, Australia and Europe, i.e. all continents where this species lives. The secret for such an extraordinary evolutionary success is unveiled in this report, as B chromosomes in this species contain active protein-coding genes whose transcripts might interfere with gene expression in the host genome (the A chromosomes), thus facilitating B chromosome mitotic and meiotic drive to provide the transmission advantage which grants its success. One of the B-chromosomal genes (apc1) codes for the large subunit of the Anaphase Promoting Complex or Cyclosome (APC/C) whose expression might provide a mechanistic explanation for B chromosome drive.

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Structural and Functional Analysis of Transposable Elements Focusing on B Chromosomes of the Cichlid Fish Astatotilapia latifasciata

10.20944/preprints201803.0145.v1 ◽

2018 ◽

Author(s):

Rafael Coan ◽

Cesar Martins

Keyword(s):

Transposable Elements ◽

Repetitive Sequences ◽

Chromosome Complement ◽

Cichlid Fish ◽

B Chromosome ◽

B Chromosomes ◽

Sequencing Data ◽

Taxonomic Groups ◽

African Cichlids

B chromosomes (B) are supernumerary elements found in many taxonomic groups. Most B chromosomes are rich in heterochromatin and composed of abundant repetitive sequences, especially transposable elements (TEs). Bs origin is generally linked to the A chromosome complement (A). The first report of a B chromosome in African cichlids was on Astatotilapia latifasciata, which can harbor 0, 1 or 2 B chromosomes. Classical cytogenetics studies found high TE content on the species B chromosome. In this study, we aim to understand TE composition and expression on A. latifasciata genome and its relation to the B chromosome. We use bioinformatics analysis to explore TEs genome organization and also their composition on the B chromosome. Bioinformatics findings were validated by fluorescent in situ hybridization (FISH) and real-time PCR (qPCR). A. latifasciata has a TE content similar to other cichlid fishes and several expanded elements on its B chromosome. With RNA sequencing data (RNA-seq) we showed that all major TE classes are transcribed in brain, muscle and male/female gonads. The evaluation of TE expression between B- and B+ individuals showed that few elements have differential expression among groups and expanded B elements were not highly transcribed. Putative silencing mechanisms may the acting on the B chromosome of A. latifasciata to prevent adverse consequences of repeat transcription and mobilization in the genome.

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Expression levels of the tetratricopeptide repeat protein gene ttc39b covary with carotenoid-based skin colour in cichlid fish

Biology Letters ◽

10.1098/rsbl.2020.0629 ◽

2020 ◽

Vol 16 (11) ◽

pp. 20200629

Author(s):

Ehsan Pashay Ahi ◽

Laurène A. Lecaudey ◽

Angelika Ziegelbecker ◽

Oliver Steiner ◽

Walter Goessler ◽

...

Keyword(s):

High Performance ◽

Cichlid Fish ◽

Differentially Expressed ◽

Tetratricopeptide Repeat ◽

Rna Seq ◽

Total Carotenoids ◽

Protein Coding ◽

Repeat Protein ◽

Tetratricopeptide Repeat Protein ◽

Body Colouration

Carotenoid pigments play a major role in animal body colouration, generating strong interest in the genes involved in the metabolic processes that lead from their dietary uptake to their storage in the integument. Here, we used RNA sequencing (RNA-Seq) to test for differentially expressed genes in a taxonomically replicated design using three pairs of related cichlid fish taxa from the genera Tropheus and Aulonocara . Within each pair, taxa differed in terms of red and yellow body colouration, and high‐performance liquid chromatography (HPLC) analyses of skin extracts revealed different carotenoid profiles and concentrations across the studied taxa. Five genes were differentially expressed in all three yellow–red skin contrasts ( dhrsx , nlrc3 , tcaf2 , urah and ttc39b ), but only the tetratricopeptide repeat protein-coding gene ttc39b , whose gene product is linked to mammalian lipid metabolism, was consistently expressed more highly in the red skin samples. The RNA-Seq results were confirmed by quantitative PCR. We propose ttc39b as a compelling candidate gene for variation in animal carotenoid colouration. Since differential expression of ttc39b was correlated with the presence/absence of yellow carotenoids in a previous study, we suggest that ttc39b is more likely associated with the concentration of total carotenoids than with the metabolic formation of red carotenoids.

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Sex-Biased lncRNA Signature in Fetal Growth Restriction (FGR)

Cells ◽

10.3390/cells10040921 ◽

2021 ◽

Vol 10 (4) ◽

pp. 921

Author(s):

Aleksandra Lipka ◽

Jan Pawel Jastrzebski ◽

Lukasz Paukszto ◽

Karol Gustaw Makowczenko ◽

Elzbieta Lopienska-Biernat ◽

...

Keyword(s):

Fetal Growth ◽

Fetal Growth Restriction ◽

Target Genes ◽

Active Regions ◽

Bioinformatic Analysis ◽

Growth Restriction ◽

Differentially Expressed ◽

Circular Rnas ◽

Differential Analysis ◽

Protein Coding

Impaired fetal growth is one of the most important causes of prematurity, stillbirth and infant mortality. The pathogenesis of idiopathic fetal growth restriction (FGR) is poorly understood but is thought to be multifactorial and comprise a range of genetic causes. This research aimed to investigate non-coding RNAs (lncRNAs) in the placentas of male and female fetuses affected by FGR. RNA-Seq data were analyzed to detect lncRNAs, their potential target genes and circular RNAs (circRNAs); a differential analysis was also performed. The multilevel bioinformatic analysis enabled the detection of 23,137 placental lncRNAs and 4263 of them were classified as novel. In FGR-affected female fetuses’ placentas (ff-FGR), among 19 transcriptionally active regions (TARs), five differentially expressed lncRNAs (DELs) and 12 differentially expressed protein-coding genes (DEGs) were identified. Within 232 differentially expressed TARs identified in male fetuses (mf-FGR), 33 encompassed novel and 176 known lncRNAs, and 52 DEGs were upregulated, while 180 revealed decreased expression. In ff-FGR ACTA2-AS1, lncRNA expression was significantly correlated with five DEGs, and in mf-FGR, 25 TARs were associated with DELs correlated with 157 unique DEGs. Backsplicing circRNA processes were detected in the range of H19 lncRNA, in both ff- and mf-FGR placentas. The performed global lncRNAs characteristics in terms of fetal sex showed dysregulation of DELs, DEGs and circRNAs that may affect fetus growth and pregnancy outcomes. In female placentas, DELs and DEGs were associated mainly with the vasculature, while in male placentas, disturbed expression predominantly affected immune processes.

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Repetitive DNA landscape in essential A and supernumerary B chromosomes of Festuca pratensis Huds

Scientific Reports ◽

10.1038/s41598-019-56383-1 ◽

2019 ◽

Vol 9 (1) ◽

Author(s):

Rahman Ebrahimzadegan ◽

Andreas Houben ◽

Ghader Mirzaghaderi

Keyword(s):

Repetitive Sequences ◽

Nuclear Genome ◽

B Chromosome ◽

B Chromosomes ◽

Festuca Pratensis ◽

Ltr Retrotransposons ◽

Chromosome Identification ◽

Satellite Repeats ◽

Low Pass ◽

Illumina Sequence

AbstractHere, we characterized the basic properties of repetitive sequences in essential A and supernumerary B chromosomes of Festuca pratensis Huds. This was performed by comparative analysis of low-pass Illumina sequence reads of B chromosome lacking (−B) and B chromosome containing (+B) individuals of F. pratensis. 61% of the nuclear genome is composed of repetitive sequences. 43.1% of the genome are transposons of which DNA transposons and retrotransposons made up 2.3% and 40.8%, respectively. LTR retrotransposons are the most abundant mobile elements and contribute to 40.7% of the genome and divided into Ty3-gypsy and Ty1-copia super families with 32.97% and 7.78% of the genome, respectively. Eighteen different satellite repeats were identified making up 3.9% of the genome. Five satellite repeats were used as cytological markers for chromosome identification and genome analysis in the genus Festuca. Four satellite repeats were identified on B chromosomes among which Fp-Sat48 and Fp-Sat253 were specific to the B chromosome of F. pratensis.

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