Zoe M. Länger, Elisa Israel, Jan Engelhardt, Agata I. Kalita, Claudia I. Keller Valsecchi, Joachim Kurtz, Sonja J. Prohaska
{"title":"Multiomics Reveal Associations Between CpG Methylation, Histone Modifications and Transcription in a Species That has Lost DNMT3, the Colorado Potato Beetle","authors":"Zoe M. Länger, Elisa Israel, Jan Engelhardt, Agata I. Kalita, Claudia I. Keller Valsecchi, Joachim Kurtz, Sonja J. Prohaska","doi":"10.1002/jez.b.23303","DOIUrl":"10.1002/jez.b.23303","url":null,"abstract":"<p>Insects display exceptional phenotypic plasticity, which can be mediated by epigenetic modifications, including CpG methylation and histone modifications. In vertebrates, both are interlinked and CpG methylation is associated with gene repression. However, little is known about these regulatory systems in invertebrates, where CpG methylation is mainly restricted to gene bodies of transcriptionally active genes. A widely conserved mechanism involves the co-transcriptional deposition of H3K36 trimethylation and the targeted methylation of unmethylated CpGs by the <i>de novo</i> DNA methyltransferase DNMT3. However, DNMT3 has been lost multiple times in invertebrate lineages raising the question of how the links between CpG methylation, histone modifications and gene expression are affected by its loss. Here, we report the epigenetic landscape of <i>Leptinotarsa decemlineata</i>, a beetle species that has lost DNMT3 but retained CpG methylation. We combine RNA-seq, enzymatic methyl-seq and CUT&Tag to study gene expression, CpG methylation and patterns of H3K36me3 and H3K27ac histone modifications on a genome-wide scale. Despite the loss of DNMT3, H3K36me3 mirrors CpG methylation patterns. Together, they give rise to signature profiles for expressed and not expressed genes. H3K27ac patterns show a prominent peak at the transcription start site that is predictive of expressed genes irrespective of their methylation status. Our study provides new insights into the evolutionary flexibility of epigenetic modification systems that urge caution when generalizing across species.</p>","PeriodicalId":15682,"journal":{"name":"Journal of experimental zoology. Part B, Molecular and developmental evolution","volume":"344 7","pages":"454-469"},"PeriodicalIF":1.7,"publicationDate":"2025-05-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/jez.b.23303","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143985729","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Chi-Chun Fang, Arjuna Rajakumar, Andrew Kenny, Ulrich G. Mueller, Ehab Abouheif, David Stein
{"title":"Embryogenesis in Myrmicine Ants Combines Features of Short Germ-Band Development With a Progressive Mode of Segmentation","authors":"Chi-Chun Fang, Arjuna Rajakumar, Andrew Kenny, Ulrich G. Mueller, Ehab Abouheif, David Stein","doi":"10.1002/jez.b.23296","DOIUrl":"10.1002/jez.b.23296","url":null,"abstract":"<p>Ants exhibit complex social organization, morphologically and functionally distinct castes, and the exploitation of diverse ecological niches. How these features have influenced embryonic development relative to other insects remains unclear. Insect embryogenesis has been classified into three modes: In long germ-band development, exemplified by the fruit fly <i>Drosophila melanogaster</i>, segments along the entire anterior–posterior axis of the embryonic primordium are established almost simultaneously, before gastrulation, with the initial embryonic primordium surrounding almost the entire volume of the egg. In short and intermediate germ-band modes, the embryonic primordium occupies a smaller proportion of the egg surface, with anterior segments initially specified, and remaining segments being added sequentially from a posterior growth zone. Here, we examine embryogenesis in three myrmicine ants, the fungus-gardening ants <i>Atta texana</i> and <i>Mycocepurus smithii</i>, and the red imported fire ant <i>Solenopsis invicta</i>. We find that these ant embryos combine features of short germ-band development with a newly characterized progressive pattern of segmentation that has been associated with some long germ-band-developing insects. Despite similarities in the size of ant and <i>Drosophila</i> eggs, embryogenesis in the three ant species is 10- to 20-fold longer than in <i>Drosophila</i> and is also significantly longer than in two other hymenopteran species that have been studied, the honeybee <i>Apis mellifera</i> and the jewel wasp <i>Nasonia vitripennis</i>. Moreover, the embryos produced by <i>A. texana</i> foundress queens develop to first instar larvae 25% faster than embryos produced by mature queens. We discuss these results in the context of the eusocial lifestyle of ants.</p>","PeriodicalId":15682,"journal":{"name":"Journal of experimental zoology. Part B, Molecular and developmental evolution","volume":"344 5","pages":"284-302"},"PeriodicalIF":1.8,"publicationDate":"2025-05-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/jez.b.23296","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143983177","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Grant Batzel, Yiqun Wang, Antonia Bock, Elbereth Chen, Stephanie Neal, Rebecca N. Lopez-Anido, Yoon Lee, Evan Tjeerdema, Emily Ignatoff, Tejasvi Patil, Gabriela Ramirez, Maryna P. Lesoway, Amro Hamdoun, Deirdre C. Lyons
{"title":"CRISPR/Cas9 Knockout of Shell Matrix Protein 1 in the Slipper-Snail Crepidula atrasolea","authors":"Grant Batzel, Yiqun Wang, Antonia Bock, Elbereth Chen, Stephanie Neal, Rebecca N. Lopez-Anido, Yoon Lee, Evan Tjeerdema, Emily Ignatoff, Tejasvi Patil, Gabriela Ramirez, Maryna P. Lesoway, Amro Hamdoun, Deirdre C. Lyons","doi":"10.1002/jez.b.23293","DOIUrl":"10.1002/jez.b.23293","url":null,"abstract":"<p>Over the course of hundreds of millions of years, biomineralization has evolved independently many times across all kingdoms of life. Among animals, the phylum Mollusca displays a remarkable diversity in biomineral structures, particularly the molluscan shell, which varies greatly in shape, size, pigmentation, and patterning. Shell matrix proteins (SMPs) are key components of these shells, and are thought to drive the precipitation of calcium carbonate minerals and influence shell morphology. However, this structure-function relationship has rarely been studied directly because tools for knocking out genes did not exist in molluscs until recently. In this study, we report the first successful use of CRISPR/Cas9 gene editing to target an SMP in gastropod molluscs. Using the emerging model gastropod <i>Crepidula atrasolea</i>, we generated knockouts of the <i>SMP1</i> gene. Successful gene editing was confirmed by Sanger and MiSeq sequencing, and loss of <i>SMP1</i> expression was validated through high-content imaging of crispant embryos. This study establishes <i>C. atrasolea</i> as a valuable model for investigating the genetic basis of shell formation and provides a framework for applying CRISPR/Cas9 technology in other molluscan species. Our approach will enable future studies to thoroughly test the role of SMPs in shaping the diverse array of molluscan shell structures.</p>","PeriodicalId":15682,"journal":{"name":"Journal of experimental zoology. Part B, Molecular and developmental evolution","volume":"344 5","pages":"266-283"},"PeriodicalIF":1.8,"publicationDate":"2025-05-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/jez.b.23293","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144022062","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"In the Spotlight—Early Career Researcher","authors":"Leslie S. Babonis","doi":"10.1002/jez.b.23302","DOIUrl":"10.1002/jez.b.23302","url":null,"abstract":"","PeriodicalId":15682,"journal":{"name":"Journal of experimental zoology. Part B, Molecular and developmental evolution","volume":"344 5","pages":"241-242"},"PeriodicalIF":1.8,"publicationDate":"2025-05-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143969331","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Elena L. Novikova, Zinaida I. Starunova, Ksenia V. Shunkina, Alexandra I. Chava, Valeriia R. Khabibulina, Galina A. Barmasova, Clementine Z. Aster, Viktor V. Starunov
{"title":"Comparative Regeneration Dynamics of Platynereis dumerilii and Pygospio elegans (Annelida): Morphological and Cellular Events","authors":"Elena L. Novikova, Zinaida I. Starunova, Ksenia V. Shunkina, Alexandra I. Chava, Valeriia R. Khabibulina, Galina A. Barmasova, Clementine Z. Aster, Viktor V. Starunov","doi":"10.1002/jez.b.23298","DOIUrl":"10.1002/jez.b.23298","url":null,"abstract":"<div>\u0000 \u0000 <p>In this paper we compared the morphological and histological events during the regeneration process of two annelids–<i>Platynereis dumerilii</i> and <i>Pygospio elegans</i>. <i>P. dumerilii</i> is an errantial annelid capable of tail regrowth. <i>P. elegans</i> belongs to the Sedentaria clade and can regenerate both head and tail after amputation. To elucidate when the failure of anterior regeneration in <i>P. dumerilii</i> occurs we explored the wound closure, the proliferation and apoptotic events at the regeneration sites of both species. Our findings indicate that <i>P. dumerilii</i> fails to regenerate the head structures at the very early stages of the restoration process.</p></div>","PeriodicalId":15682,"journal":{"name":"Journal of experimental zoology. Part B, Molecular and developmental evolution","volume":"344 5","pages":"243-265"},"PeriodicalIF":1.8,"publicationDate":"2025-04-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144010650","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"","authors":"","doi":"","DOIUrl":"","url":null,"abstract":"","PeriodicalId":15682,"journal":{"name":"Journal of experimental zoology. Part B, Molecular and developmental evolution","volume":"346 3","pages":"172-187"},"PeriodicalIF":1.7,"publicationDate":"2025-04-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"148099527","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"From Genes to Pathways: A Curated Gene Approach to Accurate Pathway Reconstruction in Teleost Fish Transcriptomics","authors":"Marcela Herrera, Stefano Vianello, Laurie Mitchell, Zoé Chamot, Catherine Lorin-Nebel, Edith Bonnelye, Natacha Roux, Laurence Besseau, Yann Gibert, Vincent Laudet","doi":"10.1002/jez.b.23299","DOIUrl":"10.1002/jez.b.23299","url":null,"abstract":"<div>\u0000 \u0000 <p>Interpreting the vast amounts of data generated by high-throughput sequencing technologies can often present a significant challenge, particularly for non-model organisms. While automated approaches like GO (Gene Ontology) and KEGG (Kyoto Encyclopedia of Genes and Genomes) enrichment analyses are widely used, they often lack specificity for non-model organisms. To bridge this gap, we present a manually curated gene list tailored for teleost fish transcriptomics. This resource focuses on key biological processes crucial for understanding teleost fish physiology, development, and adaptation, including hormone signaling, various metabolic pathways, appetite regulation, digestion, gastrointestinal function, vision, ossification, osmoregulation, and pigmentation. Developed through collaborative efforts of specialists in diverse fields, the list prioritizes genes with established roles in teleost physiology, experimental evidence, and conservation across species. This curated list aims to provide researchers with a reliable starting point for transcriptomic analyses, offering a carefully evaluated set of genes relevant to current research priorities. By streamlining the process of gene selection and interpretation, this resource supports the broader teleost fish research community in designing and analyzing studies that investigate molecular responses to developmental and environmental changes. We encourage the scientific community to collaboratively expand and refine this list, ensuring its continued relevance and utility for teleost fish research.</p></div>","PeriodicalId":15682,"journal":{"name":"Journal of experimental zoology. Part B, Molecular and developmental evolution","volume":"344 5","pages":"303-317"},"PeriodicalIF":1.8,"publicationDate":"2025-04-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144002570","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Amanda Glaser-Schmitt, Marie Lebherz, Ezgi Saydam, Erich Bornberg-Bauer, John Parsch
{"title":"Expression of De Novo Open Reading Frames in Natural Populations of Drosophila melanogaster","authors":"Amanda Glaser-Schmitt, Marie Lebherz, Ezgi Saydam, Erich Bornberg-Bauer, John Parsch","doi":"10.1002/jez.b.23297","DOIUrl":"10.1002/jez.b.23297","url":null,"abstract":"<p><i>De novo</i> genes, which originate from noncoding DNA, are known to have a high rate of turnover over short evolutionary timescales, such as within a species. Thus, their expression is often lineage- or genetic background-specific. However, little is known about their levels and breadth of expression as populations of a species diverge. In this study, we utilized publicly available RNA-seq data to examine the expression of newly evolved open reading frames (neORFs) in comparison to non- and protein-coding genes in <i>Drosophila melanogaster</i> populations from the derived species range in Europe and the ancestral range in sub-Saharan Africa. Our datasets included two adult tissue types as well as whole bodies at two temperatures for both sexes and three larval/prepupal developmental stages in a single tissue and sex, which allowed us to examine neORF expression and divergence across multiple sample types as well as sex and population. We detected a relatively large proportion (approximately 50%) of annotated neORFs as expressed in the population samples, with neORFs often showing greater expression divergence between populations than non- or protein-coding genes. However, differential expression of neORFs between populations tended to occur in a sample type-specific manner. On the other hand, neORFs displayed less sex-biased expression than the other two gene classes, with the majority of sex-biased neORFs detected in whole bodies, which may be attributable to the presence of the gonads. We also found that neORFs shared among multiple lines in the original set of inbred lines in which they were first detected were more likely to be both expressed and differentially expressed in the new population samples, suggesting that neORFs at a higher frequency (i.e. present in more individuals) within a species are more likely to be functional.</p>","PeriodicalId":15682,"journal":{"name":"Journal of experimental zoology. Part B, Molecular and developmental evolution","volume":"344 7","pages":"415-427"},"PeriodicalIF":1.7,"publicationDate":"2025-04-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/jez.b.23297","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144018282","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Ereskovsky Alexander, Vyacheslav V. Khalaman, Godefroy Nelly, Chenesseau Sandrine, Nadezhda Yu. Rogovskaja, Konstantin A. Krasnov, Polina A. Manoylina, Alexander Yu. Komendantov, Le Goff Emilie
{"title":"Halichondria panicea (Porifera, Demospongiae) Reparative Regeneration: An Integrative Approach to Better Understand Wound Healing","authors":"Ereskovsky Alexander, Vyacheslav V. Khalaman, Godefroy Nelly, Chenesseau Sandrine, Nadezhda Yu. Rogovskaja, Konstantin A. Krasnov, Polina A. Manoylina, Alexander Yu. Komendantov, Le Goff Emilie","doi":"10.1002/jez.b.23295","DOIUrl":"10.1002/jez.b.23295","url":null,"abstract":"<div>\u0000 \u0000 <p>Sponges have a remarkable capacity to rapidly regenerate in response to injury. In addition, sponges rapidly renew their aquiferous system to maintain a healthy. This study describes the reparative regeneration in the cold-water demosponge <i>Halichondria panicea</i>. The wide range of methods allow us to make a comprehensive analysis of mechanisms, which contribute to the regeneration in this species, including morphogenetic process, cell proliferation, apoptosis and cytotoxicity. The regeneration in <i>H. panicea</i> includes three main stages: internal milieu isolation, wound healing - epithelization, and restoration of damaged structures. The main morphogenetical mechanisms of regeneration are epithelial-to-mesenchymal transition during the first 12 h post operation (hpo) followed by blastema formation and mesenchymal-to-epithelial transformation leading to the restoration of damaged structures. These processes can be explained by active cell dedifferentiation and transdifferentiation, participation of resident pluripotent cells (archaeocyte-like cells and choanocytes), by migration of pluripotent cells (archaeocyte-like cells), and by activation of proliferation and apoptosis. The rate of apoptosis becomes homogeneous in regeneration area and in intact tissues at 12 hpo at a significantly higher rate than at 0 hpo. The reduction of sponge toxicity at 6 hpo looks like a necessary step for activation of repair processes. However, after 24 hpo, the toxicity exceeded the initial (0 hpo) level. At 96 hpo, the aquiferous system is completely restored. The ability for rapid wound epithelialization, as well as the morphological and functional restoration of damaged tissues, can be considered as a form of sponge's adaptation to extreme conditions in cold shallow water, acquired in the course of evolution.</p></div>","PeriodicalId":15682,"journal":{"name":"Journal of experimental zoology. Part B, Molecular and developmental evolution","volume":"344 4","pages":"214-235"},"PeriodicalIF":1.8,"publicationDate":"2025-04-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143811646","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Cristian Camillo Barrera Grijalba, Sonia Victoria Rodríguez Monje, Gabriela Ariza Aranguren, Kathrin Lunzer, Maik Scherholz, Emanuel Redl, Tim Wollesen
{"title":"Molluscan Shells, Spicules, and Gladii Are Evolutionarily Deeply Conserved","authors":"Cristian Camillo Barrera Grijalba, Sonia Victoria Rodríguez Monje, Gabriela Ariza Aranguren, Kathrin Lunzer, Maik Scherholz, Emanuel Redl, Tim Wollesen","doi":"10.1002/jez.b.23294","DOIUrl":"10.1002/jez.b.23294","url":null,"abstract":"<p>Shells, spicules, and chaetae are diverse among extant and extinct spiralians such as mollusks, annelids, or brachiopods. These hard parts serve different functions, but their formation process and evolutionary interrelationships are still contentious. We investigated the expression of evolutionarily conserved transcription factor encoding genes as well as the structural genes <i>chitin synthase</i> and <i>ferritin</i> in cells giving rise to shells and spicules of aculiferans, i.e. the polyplacophoran <i>Acanthochitona fascicularis</i> and the neomeniomorph <i>Wirenia argentea</i>, as well as the conchiferan cephalopod <i>Xipholeptos notoides</i> and the scaphopod <i>Antalis entalis</i>. Polyplacophorans and neomeniomorphs express <i>hox1</i> (only neomeniomorphs), <i>goosecoid</i>, <i>grainyhead</i>, and <i>chitin-synthase</i> in their spicules. <i>Grainyhead</i>, <i>notch</i>, <i>delta</i>, and <i>zic</i> are expressed in the polyplacophoran shell fields and spicule-bearing cells. In conchiferans, <i>hox1</i> (scaphopods and cephalopods), <i>goosecoid</i>, and <i>grainyhead</i> (scaphopods) are expressed in the shell fields. <i>Ferritin</i>, is a gene that has been shown to be expressed in the gastropod shell field; however, it is not expressed in the shell fields or by the spicule-bearing cells of the studied species. Our study shows that all candidate genes are expressed in epithelia that give rise to spicules and shells, revealing a close relationship between spicule-bearing cells and shell fields. In contrast, <i>ferritin</i> expression in the shell field appears to be a gastropod innovation. Building on previous research involving brachiopod and annelid chaetal sacs, our results suggest that spicules may have predated molluscan shells and may be homologous to brachiopod and annelid chaetae. If this were true, then conchiferan mollusks would have secondarily lost spicules.</p>","PeriodicalId":15682,"journal":{"name":"Journal of experimental zoology. Part B, Molecular and developmental evolution","volume":"344 4","pages":"198-213"},"PeriodicalIF":1.8,"publicationDate":"2025-04-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/jez.b.23294","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143811648","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}