Alternative Splicing Profile and Sex-Preferential Gene Expression in the Female and Male Pacific Abalone Haliotis discus hannai

Kim, Mi Ae; Rhee, Jae-Sung; Kim, Tae Ha; Lee, Jung Sick; Choi, Ahyoung; Choi, Beom-Soon; Choi, Ik‐Young; Sohn, Young Chang

doi:10.3390/genes8030099

Cited by 37 publications

(30 citation statements)

References 57 publications

(68 reference statements)

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“…elegans , and also in the protein ubiquitination pathway ( Doniach and Hodgkin 1984 ). Two other genes that seem well represented in bivalves, and more generally in mollusks ( Kim et al. 2017 ), are Bar-1 / Arm / Ctnnb1 ( Beta-catenin ) and Tra-1 ( table 4 ).…”

Section: Resultsmentioning

confidence: 99%

Deciphering the Link between Doubly Uniparental Inheritance of mtDNA and Sex Determination in Bivalves: Clues from Comparative Transcriptomics

Capt

Renaut

Ghiselli

et al. 2018

Genome Biology and Evolution

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Bivalves exhibit an astonishing diversity of sexual systems and sex-determining mechanisms. They can be gonochoric, hermaphroditic or androgenetic, with both genetic and environmental factors known to determine or influence sex. One unique sex-determining system involving the mitochondrial genome has also been hypothesized to exist in bivalves with doubly uniparental inheritance (DUI) of mtDNA. However, the link between DUI and sex determination remains obscure. In this study, we performed a comparative gonad transcriptomics analysis for two DUI-possessing freshwater mussel species to better understand the mechanisms underlying sex determination and DUI in these bivalves. We used a BLAST reciprocal analysis to identify orthologs between Venustaconcha ellipsiformis and Utterbackia peninsularis and compared our results with previously published sex-specific bivalve transcriptomes to identify conserved sex-determining genes. We also compared our data with other DUI species to identify candidate genes possibly involved in the regulation of DUI. A total of ∼12,000 orthologous relationships were found, with 2,583 genes differentially expressed in both species. Among these genes, key sex-determining factors previously reported in vertebrates and in bivalves (e.g., Sry, Dmrt1, Foxl2) were identified, suggesting that some steps of the sex-determination pathway may be deeply conserved in metazoans. Our results also support the hypothesis that a modified ubiquitination mechanism could be responsible for the retention of the paternal mtDNA in male bivalves, and revealed that DNA methylation could also be involved in the regulation of DUI. Globally, our results suggest that sets of genes associated with sex determination and DUI are similar in distantly-related DUI species.

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Section: Resultsmentioning

confidence: 99%

Deciphering the Link between Doubly Uniparental Inheritance of mtDNA and Sex Determination in Bivalves: Clues from Comparative Transcriptomics

Capt

Renaut

Ghiselli

et al. 2018

Genome Biology and Evolution

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“…An additional problem is that it is still a challenge to correctly identify spliced exons from short-read RNA-seq (e.g., Illumina sequencer) as ≈95% of multi-exon genes undergo alternative splicing, which results in ≈100,000 alternative splicing events in major human tissues [64]. One potential solution is to use "Iso-Seq" [65][66][67][68][69][70][71][72][73][74][75][76], which allows for the capturing of transcripts over kilo nucleotides (nt) in length, recording isoforms with increased accuracy compared to shorter sequences (e.g., <200 nt). However, the analysis of long reads is difficult due to the low sequence coverage, which also leads to missing of RNA editing sites to be identified.…”

Section: Discussionmentioning

confidence: 99%

Investigation of RNA Editing Sites within Bound Regions of RNA-Binding Proteins

et al. 2019

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Studies in epitranscriptomics indicate that RNA is modified by a variety of enzymes. Among these RNA modifications, adenosine to inosine (A-to-I) RNA editing occurs frequently in the mammalian transcriptome. These RNA editing sites can be detected directly from RNA sequencing (RNA-seq) data by examining nucleotide changes from adenosine (A) to guanine (G), which substitutes for inosine (I). However, a careful investigation of such nucleotide changes must be conducted to distinguish sequencing errors and genomic mutations from the genuine editing sites. Building upon our recent introduction of an easy-to-use bioinformatics tool, RNA Editor, to detect RNA editing events from RNA-seq data, we examined the extent by which RNA editing events affect the binding of RNA-binding proteins (RBP). Through employing bioinformatic techniques, we uncovered that RNA editing sites occur frequently in RBP-bound regions. Moreover, the presence of RNA editing sites are more frequent when RNA editing islands were examined, which are regions in which RNA editing sites are present in clusters. When the binding of one RBP, human antigen R [HuR; encoded by ELAV-like protein 1 (ELAV1)], was quantified experimentally, its binding was reduced upon silencing of the RNA editing enzyme adenosine deaminases acting on RNA (ADAR) compared to the control—suggesting that the presence of RNA editing islands influence HuR binding to its target regions. These data indicate RNA editing as an important mediator of RBP–RNA interactions—a mechanism which likely constitutes an additional mode of post-transcription gene regulation in biological systems.

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“…The abalone H. discus hannai is an ecologically and economically important marine species that is naturally distributed in Korea, Japan, China, and Taiwan. Several recent studies have identified a number of reproductive and metabolic genes in H. discus hannai (Mendoza-Porras et al 2014;Kim et al 2017). Additionally, neuropeptide precursors that influence sexual maturation in female Pacific abalone have been recently reported by Kim et al (2019).…”

Section: Introductionmentioning

confidence: 99%

In silico prediction of neuropeptides from the neural ganglia of Pacific abalone Haliotis discus hannai (Mollusca: Gastropoda)

Sharker

Sukhan

Kim

et al. 2020

The European Zoological Journal

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Neuropeptides play a central role in the regulation of reproduction, growth, development, and various other physiological processes. In our study, 26 neuropeptide precursors were identified from the pleuropedal and cerebral ganglia of Pacific abalone using transcriptome analysis. Of them, two (neuromacin and neuroglian) were potentially novel and two (myomodulin and FMRFamide) were involved in the reproductive regulation of mollusks. A BLAST search indicated that most of these neuropeptides exhibited the highest homologies with neuropeptides of other protostomian species. Myomodulin, FMRFamide, and molluscan insulin-related peptides shared 87%, 72%, and 88% sequence identities with homologous peptides of the tropical gastropod mollusk, Haliotis asinina. In silico analysis revealed that these identified neuropeptide precursors were likely to be extracellular secreted proteins. Alignment of multiple cerebrin, FFamide, and insulin-related peptide sequences illustrated that most of their biologically active residues were highly conserved with other invertebrate homologous neuropeptide residues. Three-dimensional (3D) structures of adipokinetic hormone, allatostain (A, B, and C), allatotropin, cerebrin, clionin, conopressin, elevenin, and neuromycin precursors in H. discus hannai exhibited a helix-loophelix structure. Based on phylogenetic analysis, buccalin A1 and A2, allatostain B, and FCAP neuropeptide precursors of Pacific abalone formed a clade with other gastropod and bivalve mollusks neuropeptide precursors. This study provides a novel insight for further functional studies of abalone and other gastropod mollusks.

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Alternative Splicing Profile and Sex-Preferential Gene Expression in the Female and Male Pacific Abalone Haliotis discus hannai

Cited by 37 publications

References 57 publications

Deciphering the Link between Doubly Uniparental Inheritance of mtDNA and Sex Determination in Bivalves: Clues from Comparative Transcriptomics

Deciphering the Link between Doubly Uniparental Inheritance of mtDNA and Sex Determination in Bivalves: Clues from Comparative Transcriptomics

Investigation of RNA Editing Sites within Bound Regions of RNA-Binding Proteins

In silico prediction of neuropeptides from the neural ganglia of Pacific abalone Haliotis discus hannai (Mollusca: Gastropoda)

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