Comparisons of cell proliferation and cell death from tornaria larva to juvenile worm in the hemichordate Schizocardium californicum
Abstract Background There are a wide range of developmental strategies in animal phyla, but most insights into adult body plan formation come from direct-developing species. For indirect-developing species, there are distinct larval and adult body plans that are linked together by metamorphosis. Som...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2022-06-01
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| Series: | EvoDevo |
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| Online Access: | https://doi.org/10.1186/s13227-022-00198-1 |
| _version_ | 1818207466631987200 |
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| author | Paul Bump Margarita Khariton Clover Stubbert Nicole E. Moyen Jia Yan Bo Wang Christopher J. Lowe |
| author_facet | Paul Bump Margarita Khariton Clover Stubbert Nicole E. Moyen Jia Yan Bo Wang Christopher J. Lowe |
| author_sort | Paul Bump |
| collection | DOAJ |
| description | Abstract Background There are a wide range of developmental strategies in animal phyla, but most insights into adult body plan formation come from direct-developing species. For indirect-developing species, there are distinct larval and adult body plans that are linked together by metamorphosis. Some outstanding questions in the development of indirect-developing organisms include the extent to which larval tissue undergoes cell death during the process of metamorphosis and when and where the tissue that will give rise to the adult originates. How do the processes of cell division and cell death redesign the body plans of indirect developers? In this study, we present patterns of cell proliferation and cell death during larval body plan development, metamorphosis, and adult body plan formation, in the hemichordate Schizocardium californium (Cameron and Perez in Zootaxa 3569:79–88, 2012) to answer these questions. Results We identified distinct patterns of cell proliferation between larval and adult body plan formation of S. californicum. We found that some adult tissues proliferate during the late larval phase prior to the start of overt metamorphosis. In addition, using an irradiation and transcriptomic approach, we describe a genetic signature of proliferative cells that is shared across the life history states, as well as markers that are unique to larval or juvenile states. Finally, we observed that cell death is minimal in larval stages but begins with the onset of metamorphosis. Conclusions Cell proliferation during the development of S. californicum has distinct patterns in the formation of larval and adult body plans. However, cell death is very limited in larvae and begins during the onset of metamorphosis and into early juvenile development in specific domains. The populations of cells that proliferated and gave rise to the larvae and juveniles have a genetic signature that suggested a heterogeneous pool of proliferative progenitors, rather than a set-aside population of pluripotent cells. Taken together, we propose that the gradual morphological transformation of S. californicum is mirrored at the cellular level and may be more representative of the development strategies that characterize metamorphosis in many metazoan animals. |
| first_indexed | 2024-12-12T04:29:22Z |
| format | Article |
| id | doaj.art-a434febc0f2a4788867048572feadb9e |
| institution | Directory Open Access Journal |
| issn | 2041-9139 |
| language | English |
| last_indexed | 2024-12-12T04:29:22Z |
| publishDate | 2022-06-01 |
| publisher | BMC |
| record_format | Article |
| series | EvoDevo |
| spelling | doaj.art-a434febc0f2a4788867048572feadb9e2022-12-22T00:38:08ZengBMCEvoDevo2041-91392022-06-0113112010.1186/s13227-022-00198-1Comparisons of cell proliferation and cell death from tornaria larva to juvenile worm in the hemichordate Schizocardium californicumPaul Bump0Margarita Khariton1Clover Stubbert2Nicole E. Moyen3Jia Yan4Bo Wang5Christopher J. Lowe6Hopkins Marine Station, Department of Biology, Stanford UniversityDepartment of Bioengineering, Stanford UniversityCalifornia State University of Monterey BayHopkins Marine Station, Department of Biology, Stanford UniversityCZ BiohubDepartment of Bioengineering, Stanford UniversityHopkins Marine Station, Department of Biology, Stanford UniversityAbstract Background There are a wide range of developmental strategies in animal phyla, but most insights into adult body plan formation come from direct-developing species. For indirect-developing species, there are distinct larval and adult body plans that are linked together by metamorphosis. Some outstanding questions in the development of indirect-developing organisms include the extent to which larval tissue undergoes cell death during the process of metamorphosis and when and where the tissue that will give rise to the adult originates. How do the processes of cell division and cell death redesign the body plans of indirect developers? In this study, we present patterns of cell proliferation and cell death during larval body plan development, metamorphosis, and adult body plan formation, in the hemichordate Schizocardium californium (Cameron and Perez in Zootaxa 3569:79–88, 2012) to answer these questions. Results We identified distinct patterns of cell proliferation between larval and adult body plan formation of S. californicum. We found that some adult tissues proliferate during the late larval phase prior to the start of overt metamorphosis. In addition, using an irradiation and transcriptomic approach, we describe a genetic signature of proliferative cells that is shared across the life history states, as well as markers that are unique to larval or juvenile states. Finally, we observed that cell death is minimal in larval stages but begins with the onset of metamorphosis. Conclusions Cell proliferation during the development of S. californicum has distinct patterns in the formation of larval and adult body plans. However, cell death is very limited in larvae and begins during the onset of metamorphosis and into early juvenile development in specific domains. The populations of cells that proliferated and gave rise to the larvae and juveniles have a genetic signature that suggested a heterogeneous pool of proliferative progenitors, rather than a set-aside population of pluripotent cells. Taken together, we propose that the gradual morphological transformation of S. californicum is mirrored at the cellular level and may be more representative of the development strategies that characterize metamorphosis in many metazoan animals.https://doi.org/10.1186/s13227-022-00198-1MetamorphosisHemichordateTornariaCell proliferationCell death |
| spellingShingle | Paul Bump Margarita Khariton Clover Stubbert Nicole E. Moyen Jia Yan Bo Wang Christopher J. Lowe Comparisons of cell proliferation and cell death from tornaria larva to juvenile worm in the hemichordate Schizocardium californicum EvoDevo Metamorphosis Hemichordate Tornaria Cell proliferation Cell death |
| title | Comparisons of cell proliferation and cell death from tornaria larva to juvenile worm in the hemichordate Schizocardium californicum |
| title_full | Comparisons of cell proliferation and cell death from tornaria larva to juvenile worm in the hemichordate Schizocardium californicum |
| title_fullStr | Comparisons of cell proliferation and cell death from tornaria larva to juvenile worm in the hemichordate Schizocardium californicum |
| title_full_unstemmed | Comparisons of cell proliferation and cell death from tornaria larva to juvenile worm in the hemichordate Schizocardium californicum |
| title_short | Comparisons of cell proliferation and cell death from tornaria larva to juvenile worm in the hemichordate Schizocardium californicum |
| title_sort | comparisons of cell proliferation and cell death from tornaria larva to juvenile worm in the hemichordate schizocardium californicum |
| topic | Metamorphosis Hemichordate Tornaria Cell proliferation Cell death |
| url | https://doi.org/10.1186/s13227-022-00198-1 |
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