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2023, 5(4): 431-434.
doi: 10.1007/s42995-023-00208-8
Abstract:
Abstract:
The ascidian Styela clava is an ecologically important species that is distributed along coastal regions worldwide. It has a long history as a model animal for evolutionary and developmental biology research owing to its phylogenetic position between vertebrates and invertebrates, and its classical mosaic expression patterns. However, the standard developmental atlas and protocols and tools for molecular manipulation of this organism are inadequate. In this study, we established a standard developmental table and provided a web-based digital image resource for S. clava embryogenesis at each developmental stage from fertilized eggs to hatching larvae by utilizing confocal laser microscopy and 3D reconstruction images. It takes around 10 h for fertilized eggs to develop into swimming larvae and 20–30 min to complete the tail regression processes at the metamorphic stage. We observed that the notochord cells in S. clava embryos did not produce an extracellular lumen like Ciona robusta, but showed polarized elongation behaviors, providing us an ideal comparative model to study tissue morphogenesis. In addition, we established a chemical-washing procedure to remove the chorion easily from the fertilized eggs. Based on the dechorionation technique, we further realized transgenic manipulation by electroporation and successfully applied tissue-specific fluorescent labeling in S. clava embryos. Our work provides a standard imaging atlas and powerful genetic tools for investigating embryogenesis and evolution using S. clava as a model organism.
The ascidian Styela clava is an ecologically important species that is distributed along coastal regions worldwide. It has a long history as a model animal for evolutionary and developmental biology research owing to its phylogenetic position between vertebrates and invertebrates, and its classical mosaic expression patterns. However, the standard developmental atlas and protocols and tools for molecular manipulation of this organism are inadequate. In this study, we established a standard developmental table and provided a web-based digital image resource for S. clava embryogenesis at each developmental stage from fertilized eggs to hatching larvae by utilizing confocal laser microscopy and 3D reconstruction images. It takes around 10 h for fertilized eggs to develop into swimming larvae and 20–30 min to complete the tail regression processes at the metamorphic stage. We observed that the notochord cells in S. clava embryos did not produce an extracellular lumen like Ciona robusta, but showed polarized elongation behaviors, providing us an ideal comparative model to study tissue morphogenesis. In addition, we established a chemical-washing procedure to remove the chorion easily from the fertilized eggs. Based on the dechorionation technique, we further realized transgenic manipulation by electroporation and successfully applied tissue-specific fluorescent labeling in S. clava embryos. Our work provides a standard imaging atlas and powerful genetic tools for investigating embryogenesis and evolution using S. clava as a model organism.
Abstract:
The D-quadrant organizer sets up the dorsal–ventral (DV) axis and regulates mesodermal development of spiralians. Studies have revealed an important role of mitogen-activated protein kinase (MAPK) signaling in organizer function, but the related molecules have not been fully revealed. The association between fibroblast growth factor receptor (FGFR) and MAPK signaling in regulating organizer specification has been established in the annelid Owenia fusiformis. Now, comparable studies in other spiralian phyla are required to decipher whether this organizer-inducing function of FGFR is prevalent in Spiralia. Here, we indicate that treatment with the FGFR inhibitor SU5402 resulted in deficiency of organizer specification in the mollusk Lottia peitaihoensis. Subsequently, the bone morphogenetic protein (BMP) signaling gradient and DV patterning were disrupted, suggesting the roles of FGFR in regulating organizer function. Changes in multiple aspects of organizer function (the morphology of vegetal blastomeres, BMP signaling gradient, expression of DV patterning markers, etc.) indicate that these developmental functions have different sensitivities to FGFR/MAPK signaling. Our results reveal a functional role of FGFR in organizer specification as well as DV patterning of Lottia embryos, which expands our knowledge of spiralian organizers.
The D-quadrant organizer sets up the dorsal–ventral (DV) axis and regulates mesodermal development of spiralians. Studies have revealed an important role of mitogen-activated protein kinase (MAPK) signaling in organizer function, but the related molecules have not been fully revealed. The association between fibroblast growth factor receptor (FGFR) and MAPK signaling in regulating organizer specification has been established in the annelid Owenia fusiformis. Now, comparable studies in other spiralian phyla are required to decipher whether this organizer-inducing function of FGFR is prevalent in Spiralia. Here, we indicate that treatment with the FGFR inhibitor SU5402 resulted in deficiency of organizer specification in the mollusk Lottia peitaihoensis. Subsequently, the bone morphogenetic protein (BMP) signaling gradient and DV patterning were disrupted, suggesting the roles of FGFR in regulating organizer function. Changes in multiple aspects of organizer function (the morphology of vegetal blastomeres, BMP signaling gradient, expression of DV patterning markers, etc.) indicate that these developmental functions have different sensitivities to FGFR/MAPK signaling. Our results reveal a functional role of FGFR in organizer specification as well as DV patterning of Lottia embryos, which expands our knowledge of spiralian organizers.
Abstract:
Many marine invertebrate phyla are characterized by indirect development. These animals transit from planktonic larvae to benthic spats via settlement and metamorphosis, which contributes to their adaption to the marine environment. Studying the biological process of metamorphosis is, thus, key to understanding the origin and evolution of indirect development. Although numerous studies have been conducted on the relationship between metamorphosis and the marine environment, microorganisms, and neurohormones, little is known about gene regulation network (GRN) dynamics during metamorphosis. Metamorphosis-competent pediveligers of the Pacific oyster Crassostrea gigas were assayed in this study. By assaying gene expression patterns and open chromatin region changes of different samples of larvae and spats, the dynamics of molecular regulation during metamorphosis were examined. The results indicated significantly different gene regulation networks before, during and post-metamorphosis. Genes encoding membrane-integrated receptors and those related to the remodeling of the nervous system were upregulated before the initiation of metamorphosis. Massive biogenesis, e.g., of various enzymes and structural proteins, occurred during metamorphosis as inferred from the comprehensive upregulation of the protein synthesis system post epinephrine stimulation. Hierarchical downstream gene networks were then stimulated. Some transcription factors, including homeobox, basic helix–loop–helix and nuclear receptors, showed different temporal response patterns, suggesting a complex GRN during the transition stage. Nuclear receptors, as well as their retinoid X receptor partner, may participate in the GRN controlling oyster metamorphosis, indicating an ancient role of the nuclear receptor regulation system in animal metamorphosis.
Many marine invertebrate phyla are characterized by indirect development. These animals transit from planktonic larvae to benthic spats via settlement and metamorphosis, which contributes to their adaption to the marine environment. Studying the biological process of metamorphosis is, thus, key to understanding the origin and evolution of indirect development. Although numerous studies have been conducted on the relationship between metamorphosis and the marine environment, microorganisms, and neurohormones, little is known about gene regulation network (GRN) dynamics during metamorphosis. Metamorphosis-competent pediveligers of the Pacific oyster Crassostrea gigas were assayed in this study. By assaying gene expression patterns and open chromatin region changes of different samples of larvae and spats, the dynamics of molecular regulation during metamorphosis were examined. The results indicated significantly different gene regulation networks before, during and post-metamorphosis. Genes encoding membrane-integrated receptors and those related to the remodeling of the nervous system were upregulated before the initiation of metamorphosis. Massive biogenesis, e.g., of various enzymes and structural proteins, occurred during metamorphosis as inferred from the comprehensive upregulation of the protein synthesis system post epinephrine stimulation. Hierarchical downstream gene networks were then stimulated. Some transcription factors, including homeobox, basic helix–loop–helix and nuclear receptors, showed different temporal response patterns, suggesting a complex GRN during the transition stage. Nuclear receptors, as well as their retinoid X receptor partner, may participate in the GRN controlling oyster metamorphosis, indicating an ancient role of the nuclear receptor regulation system in animal metamorphosis.
Abstract:
The evolution of a two-chambered heart, with an atrium and a ventricle, has improved heart function in both deuterostomes (vertebrates) and some protostomes (invertebrates). Although studies have examined the unique structure and function of these two chambers, molecular comparisons are few and limited to vertebrates. Here, we focus on the two-chambered protostome heart of the mollusks, offering data that may provide a better understanding of heart evolution. Specifically, we asked if the atrium and ventricle differ at the molecular level in the mollusk heart. To do so, we examined two very different species, the giant African land snail (Lissachatina fulica) and the relatively small, aquatic yesso scallop (Mizuhopecten yessoensis), with the assumption that if they exhibited commonality these similarities would likely reflect those across the phylum. We found that, although the hearts of these two species differed histologically, their cardiac gene function enrichments were similar, as revealed by transcriptomic analysis. Furthermore, the atrium and ventricle in each species had distinct gene function clusters, suggesting an evolutionary differentiation of cardiac chambers in mollusks. Finally, to explore the relationship between vertebrate and invertebrate two-chambered hearts, we compared our transcriptomic data with published data from the zebrafish, a well-studied vertebrate model with a two-chambered heart. Our analysis indicated a functional similarity of ventricular genes between the mollusks and the zebrafish, suggesting that the ventricle was differentiated to achieve the same functions in invertebrates and vertebrates. As the first such study on protostomes, our findings offered initial insights into how the two-chambered heart arose, including a possible understanding of its occurrence in both protostomes and deuterostomes.
The evolution of a two-chambered heart, with an atrium and a ventricle, has improved heart function in both deuterostomes (vertebrates) and some protostomes (invertebrates). Although studies have examined the unique structure and function of these two chambers, molecular comparisons are few and limited to vertebrates. Here, we focus on the two-chambered protostome heart of the mollusks, offering data that may provide a better understanding of heart evolution. Specifically, we asked if the atrium and ventricle differ at the molecular level in the mollusk heart. To do so, we examined two very different species, the giant African land snail (Lissachatina fulica) and the relatively small, aquatic yesso scallop (Mizuhopecten yessoensis), with the assumption that if they exhibited commonality these similarities would likely reflect those across the phylum. We found that, although the hearts of these two species differed histologically, their cardiac gene function enrichments were similar, as revealed by transcriptomic analysis. Furthermore, the atrium and ventricle in each species had distinct gene function clusters, suggesting an evolutionary differentiation of cardiac chambers in mollusks. Finally, to explore the relationship between vertebrate and invertebrate two-chambered hearts, we compared our transcriptomic data with published data from the zebrafish, a well-studied vertebrate model with a two-chambered heart. Our analysis indicated a functional similarity of ventricular genes between the mollusks and the zebrafish, suggesting that the ventricle was differentiated to achieve the same functions in invertebrates and vertebrates. As the first such study on protostomes, our findings offered initial insights into how the two-chambered heart arose, including a possible understanding of its occurrence in both protostomes and deuterostomes.
Abstract:
The Gli transcription factors are the primary mediators of Hedgehog (Hh) signaling. Vertebrate genomes contain multiple Gli paralogues with different functions downstream of Hh signal receipt, in part explaining the complexity of cellular responses to Hh that allow concentration-dependent target gene activation. Amphioxus is a chordate that split from the vertebrate lineage early in the evolution of chordates, before the genome duplications that occurred in early vertebrate evolution. It has a single Gli gene whose transcripts can be alternately spliced to yield two protein isoforms called GliS and GliL. We generated two knockout mutations in amphioxus Gli, one that affects the whole gene and a second that only affects GliL. Both knockouts showed major morphological and molecular defects in the development of left–right asymmetry, a phenotype that is similar but not identical to that previously found in Hh mutants. Hh signaling also patterns the amphioxus neural tube. Here, however, knockout of GliL showed no identifiable phenotype, while knockout of the full gene showed only small changes to the expression of one gene family, Olig. Other genes that were prominently affected by Hh knockout were not altered in expression in either knockout. Reasons for the differences between Hh and Gli knockouts in the pharynx and neural tube are discussed in the context of the likely different functions of amphioxus Gli isoforms.
The Gli transcription factors are the primary mediators of Hedgehog (Hh) signaling. Vertebrate genomes contain multiple Gli paralogues with different functions downstream of Hh signal receipt, in part explaining the complexity of cellular responses to Hh that allow concentration-dependent target gene activation. Amphioxus is a chordate that split from the vertebrate lineage early in the evolution of chordates, before the genome duplications that occurred in early vertebrate evolution. It has a single Gli gene whose transcripts can be alternately spliced to yield two protein isoforms called GliS and GliL. We generated two knockout mutations in amphioxus Gli, one that affects the whole gene and a second that only affects GliL. Both knockouts showed major morphological and molecular defects in the development of left–right asymmetry, a phenotype that is similar but not identical to that previously found in Hh mutants. Hh signaling also patterns the amphioxus neural tube. Here, however, knockout of GliL showed no identifiable phenotype, while knockout of the full gene showed only small changes to the expression of one gene family, Olig. Other genes that were prominently affected by Hh knockout were not altered in expression in either knockout. Reasons for the differences between Hh and Gli knockouts in the pharynx and neural tube are discussed in the context of the likely different functions of amphioxus Gli isoforms.
2019, 1(1): 41-49.
doi: 10.1007/s42995-019-00002-5
2019, 1(1): 28-40.
doi: 10.1007/s42995-019-00016-z
Marine Life Science & Technology
(Started in 2019)
- Editor-in-Chief: Weibo Song
- Executive Deputy Editor: Xiao-Hua Zhang
- Frequency of Publication: Quarterly
- ISSN: 2096-6490
- eISSN: 2662-1746
- CN: 37-1519/Q
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- Updats about page charges 2022-09-19
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- Good news--MLST has been indexed by Scopus 2021-08-24
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