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Title: A chitin-binding domain-containing gene is essential for shell development in the mollusc Tritia
T. Kim Dao, Kailey Ferger, J. David Lambert, A chitin-binding domain-containing gene is essential for shell development in the mollusc Tritia, Developmental Biology, Volume 520, 2025, Pages 1-12, ISSN 0012-1606, https://doi.org/10.1016/j.ydbio.2024.12.016. (https://www.sciencedirect.com/science/article/pii/S0012160624002884) Abstract: Mollusc shells are diverse in shape and size. They are created by a shell epithelium which secretes a chitinous periostracum membrane at the growing edge of the shell, and then coordinates biomineral deposition on the underside of this membrane. Although mollusc shells are important for studying the evolution of morphology, the molecular basis of the shell development is poorly understood. In this paper, we investigate genes involved in the shell development of the gastropod mollusc Tritia (previously known as Ilyanassa). We characterize the contributions of the 2d micromere to the shell and other non-shell structures. We identify eight shell-specific genes and five non-shell specific genes by comparing the transcriptomes of wild-type and 2d ablated embryos. Morpholino knockdown of one of the shell-specific genes, ToChitin-binding domain-containing (ToChitin BD), results in shell defects. The chitinous periostracal membranes in ToChitin BD morpholino knockdown embryos lose their well-defined edge and peroxidase gradient. more »« less
Varney, Rebecca M; Speiser, Daniel I; McDougall, Carmel; Degnan, Bernard M; Kocot, Kevin M
(, Genome Biology and Evolution)
Venkatesh, B
(Ed.)
Abstract Molluscs biomineralize structures that vary in composition, form, and function, prompting questions about the genetic mechanisms responsible for their production and the evolution of these mechanisms. Chitons (Mollusca, Polyplacophora) are a promising system for studies of biomineralization because they build a range of calcified structures including shell plates and spine- or scale-like sclerites. Chitons also harden the calcified teeth of their rasp-like radula with a coat of iron (as magnetite). Here we present the genome of the West Indian fuzzy chiton Acanthopleura granulata, the first from any aculiferan mollusc. The A. granulata genome contains homologs of many genes associated with biomineralization in conchiferan molluscs. We expected chitons to lack genes previously identified from pathways conchiferans use to make biominerals like calcite and nacre because chitons do not use these materials in their shells. Surprisingly, the A. granulata genome has homologs of many of these genes, suggesting that the ancestral mollusc may have had a more diverse biomineralization toolkit than expected. The A. granulata genome has features that may be specialized for iron biomineralization, including a higher proportion of genes regulated directly by iron than other molluscs. A. granulata also produces two isoforms of soma-like ferritin: one is regulated by iron and similar in sequence to the soma-like ferritins of other molluscs, and the other is constitutively translated and is not found in other molluscs. The A. granulata genome is a resource for future studies of molluscan evolution and biomineralization.
Huang, Chi; Yi, Wenjun; Seng, Jian; Xu, Wei
(, The Society for Integrative and Comparative Biology)
Calcium waves and oscillation during embryonic development are key elements in the intricate process of molluscan shell formation. However, understanding calcium dynamics in the early embryonic shell formation in gastropod development is still insufficient. The present study explores the role of calcium flux in early shell formation within the embryo of gastropod Biomphalaria glabrata. We hypothesized that the role of calcium is not only in providing a critical element for shell formation but also in serving as a signaling molecule for the genetic regulation of calcification. The calcium flux was visualized using the Fura-2 and Fluo-4 calcium indicators through the trochophore (72 hours) and veliger (120 hours) stages of B. glabrata development. The dynamics of calcium signals were correlated to the rapid transition from motile trochophore to veliger, marked by cilia-mediated movement and premature shell and foot development. According to our observation, the intracellular calcium signals were attenuated from 72 to 120 hours of embryo development. The expression profiles of genes encoding calmodulin and related protein kinase following the calcium flux in embryos suggested a critical role of the calcium-binding proteins in the early shell development of gastropods. Although the embryonic calcium dynamics and the related signaling pathway of shell formation are under further observation and analysis, the role of calcium in the singling pathway of shell formation has been demonstrated by this preliminary study.
The BEN domain is a recently recognized DNA binding module that is present in diverse metazoans and certain viruses. Several BEN domain factors are known as transcriptional repressors, but, overall, relatively little is known of how BEN factors identify their targets in humans. In particular, X-ray structures of BEN domain:DNA complexes are only known for Drosophila factors bearing a single BEN domain, which lack direct vertebrate orthologs. Here, we characterize several mammalian BEN domain (BD) factors, including from two NACC family BTB-BEN proteins and from BEND3, which has four BDs. In vitro selection data revealed sequence-specific binding activities of isolated BEN domains from all of these factors. We conducted detailed functional, genomic, and structural studies of BEND3. We show that BD4 is a major determinant for in vivo association and repression of endogenous BEND3 targets. We obtained a high-resolution structure of BEND3-BD4 bound to its preferred binding site, which reveals how BEND3 identifies cognate DNA targets and shows differences with one of its non-DNA-binding BEN domains (BD1). Finally, comparison with our previous invertebrate BEN structures, along with additional structural predictions using AlphaFold2 and RoseTTAFold, reveal distinct strategies for target DNA recognition by different types of BEN domain proteins. Together, these studies expand the DNA recognition activities of BEN factors and provide structural insights into sequence-specific DNA binding by mammalian BEN proteins.
Abstract BackgroundMorphologic sex differences between males and females typically emerge after the primordial germ cell migration and gonad formation, although sex is determined at fertilization based on chromosome composition. A key debated sexual difference is the embryonic developmental rate, within vitroproduced male embryos often developing faster. However, the molecular mechanisms driving early embryonic sex differences remain unclear. ResultsTo investigate the transcriptional sex difference during early development,in vitroproduced bovine blastocysts were collected and sexed by PCR. A significant male-biased development was observed in expanded blastocysts. Ultra-low input RNA-seq analysis identified 837 DEGs, with 231 upregulated and 606 downregulated in males. Functional enrichment analysis revealed male-biased DEGs were associated with metabolic regulation, whereas female-biased DEGs were related to female gonad development, sex differentiation, inflammatory pathways, and TGF-beta signaling. Comparing X chromosome and autosome expression ratio, we found that female-biased DEGs contributed to the higher X-linked gene dosage, a phenomenon not observed in male embryos. Moreover, we identified the sex-biased transcription factors and RNA-bind proteins, including pluripotent factors such asSOX21andPRDM14, and splicing factorsFMR1andHNRNPH2. Additionally, we revealed 1,555 significantly sex-biased differential alternative splicing (AS), predominantly skipped exons, mapped to 906 genes, with 59 overlapping with DEGs enriched in metabolic and autophagy pathways. By incorporating novel isoforms from long reads sequencing, we identified 1,151 sex-biased differentially expressed isoforms (DEIs) associated with 1,017 genes. Functional analysis showed that female-biased DEIs were involved in the negative regulation of transcriptional activity, while male-biased DEIs were related to energy metabolism. Furthermore, we identified sex-biased differential exon usage inDENND1B, DIS3L2, DOCK11, IL1RAPL2,andZRSR2Y,indicating their sex-specific regulation in early embryo development. ConclusionThis study provided a comprehensive analysis of transcriptome differences between male and female bovine blastocysts, integrating sex-biased gene expression, alternative splicing, and isoform dynamics. Our findings indicate that enriched metabolism processes in male embryos may contribute to the faster developmental pace, providing insights into sex-specific regulatory mechanisms during early embryogenesis. Plain English summaryMale and female early embryos develop at different speeds, with male embryos often developing faster than female embryos. However, the reasons behind these early differences remain unclear. In this study, we examined gene activity in bovine embryos to uncover the biological factors regulating these early sex differences. We collected in vitro-produced bovine blastocysts, examined their sex, and confirmed that male embryos develop faster. By analyzing global gene activity, including alternative splicing, which allows one gene to code for multiple RNA isoforms and proteins, we found distinct gene expression profiles between male and female embryos. Male embryos showed higher activity in genes related to metabolism and cellular functions, while female embryos had increased activity in genes associated with female-specific gonad development and gene expression regulation. We also examined differences in how genes on the X chromosome were expressed. Female embryos had higher X-linked gene expression, which may contribute to sex-specific developmental regulation. Additionally, we identified sex-specific transcription factors and RNA-binding proteins that regulate early embryo development, some of which are known to control pluripotency and gene splicing. Overall, our study provides new insights into how gene activity shapes early sex differences, suggesting that enhanced metabolism in male embryos may be a key driver of their faster developmental rate. HighlightsMale embryos develop faster due to increased gene expression in metabolism pathwaysFemale embryos exhibit higher X-linked gene expression, suggesting X-dosage compensation plays a role in early developmentSex-biased alternative splicing events contribute to embryonic metabolism, autophagy, and transcriptional regulation in embryosSex-biased isoform diversity contributes to distinct developmental regulation in male and female embryosKey pluripotency factors (SOX21, PRDM14) and splicing regulators (FMR1, HNRNPH2) drive sex-specific gene expression
Yang, Ran; Goedel, Alexander; Kang, Yu; Si, Chenyang; Chu, Chu; Zheng, Yi; Chen, Zhenzhen; Gruber, Peter J.; Xiao, Yao; Zhou, Chikai; et al
(, Nature Communications)
Abstract Embryonic development is largely conserved among mammals. However, certain genes show divergent functions. By generating a transcriptional atlas containing >30,000 cells from post-implantation non-human primate embryos, we uncover that ISL1 , a gene with a well-established role in cardiogenesis, controls a gene regulatory network in primate amnion. CRISPR/Cas9-targeting of ISL1 results in non-human primate embryos which do not yield viable offspring, demonstrating that ISL1 is critically required in primate embryogenesis. On a cellular level, mutant ISL1 embryos display a failure in mesoderm formation due to reduced BMP4 signaling from the amnion. Via loss of function and rescue studies in human embryonic stem cells we confirm a similar role of ISL1 in human in vitro derived amnion. This study highlights the importance of the amnion as a signaling center during primate mesoderm formation and demonstrates the potential of in vitro primate model systems to dissect the genetics of early human embryonic development.
Dao, T Kim, Ferger, Kailey, and Lambert, J David. A chitin-binding domain-containing gene is essential for shell development in the mollusc Tritia. Retrieved from https://par.nsf.gov/biblio/10567297. Developmental Biology 520.C Web. doi:10.1016/j.ydbio.2024.12.016.
Dao, T Kim, Ferger, Kailey, & Lambert, J David. A chitin-binding domain-containing gene is essential for shell development in the mollusc Tritia. Developmental Biology, 520 (C). Retrieved from https://par.nsf.gov/biblio/10567297. https://doi.org/10.1016/j.ydbio.2024.12.016
@article{osti_10567297,
place = {Country unknown/Code not available},
title = {A chitin-binding domain-containing gene is essential for shell development in the mollusc Tritia},
url = {https://par.nsf.gov/biblio/10567297},
DOI = {10.1016/j.ydbio.2024.12.016},
abstractNote = {T. Kim Dao, Kailey Ferger, J. David Lambert, A chitin-binding domain-containing gene is essential for shell development in the mollusc Tritia, Developmental Biology, Volume 520, 2025, Pages 1-12, ISSN 0012-1606, https://doi.org/10.1016/j.ydbio.2024.12.016. (https://www.sciencedirect.com/science/article/pii/S0012160624002884) Abstract: Mollusc shells are diverse in shape and size. They are created by a shell epithelium which secretes a chitinous periostracum membrane at the growing edge of the shell, and then coordinates biomineral deposition on the underside of this membrane. Although mollusc shells are important for studying the evolution of morphology, the molecular basis of the shell development is poorly understood. In this paper, we investigate genes involved in the shell development of the gastropod mollusc Tritia (previously known as Ilyanassa). We characterize the contributions of the 2d micromere to the shell and other non-shell structures. We identify eight shell-specific genes and five non-shell specific genes by comparing the transcriptomes of wild-type and 2d ablated embryos. Morpholino knockdown of one of the shell-specific genes, ToChitin-binding domain-containing (ToChitin BD), results in shell defects. The chitinous periostracal membranes in ToChitin BD morpholino knockdown embryos lose their well-defined edge and peroxidase gradient.},
journal = {Developmental Biology},
volume = {520},
number = {C},
publisher = {ScienceDirect},
author = {Dao, T Kim and Ferger, Kailey and Lambert, J David},
}
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