A transcriptomic examination of encased rotifer embryos reveals the developmental trajectory leading to long-term dormancy; are they “animal seeds”?
Abstract Background Organisms from many distinct evolutionary lineages acquired the capacity to enter a dormant state in response to environmental conditions incompatible with maintaining normal life activities. Most studied organisms exhibit seasonal or annual episodes of dormancy, but numerous les...
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| Format: | Article |
| Language: | English |
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BMC
2024-01-01
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| Series: | BMC Genomics |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s12864-024-09961-1 |
| _version_ | 1797340279575937024 |
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| author | Tamar Hashimshony Liron Levin Andreas C. Fröbius Nitsan Dahan Vered Chalifa-Caspi Reini Hamo Oshri Gabai-Almog Idit Blais Yehuda G. Assaraf Esther Lubzens |
| author_facet | Tamar Hashimshony Liron Levin Andreas C. Fröbius Nitsan Dahan Vered Chalifa-Caspi Reini Hamo Oshri Gabai-Almog Idit Blais Yehuda G. Assaraf Esther Lubzens |
| author_sort | Tamar Hashimshony |
| collection | DOAJ |
| description | Abstract Background Organisms from many distinct evolutionary lineages acquired the capacity to enter a dormant state in response to environmental conditions incompatible with maintaining normal life activities. Most studied organisms exhibit seasonal or annual episodes of dormancy, but numerous less studied organisms enter long-term dormancy, lasting decades or even centuries. Intriguingly, many planktonic animals produce encased embryos known as resting eggs or cysts that, like plant seeds, may remain dormant for decades. Herein, we studied a rotifer Brachionus plicatilis as a model planktonic species that forms encased dormant embryos via sexual reproduction and non-dormant embryos via asexual reproduction and raised the following questions: Which genes are expressed at which time points during embryogenesis? How do temporal transcript abundance profiles differ between the two types of embryos? When does the cell cycle arrest? How do dormant embryos manage energy? Results As the molecular developmental kinetics of encased embryos remain unknown, we employed single embryo RNA sequencing (CEL-seq) of samples collected during dormant and non-dormant embryogenesis. We identified comprehensive and temporal transcript abundance patterns of genes and their associated enriched functional pathways. Striking differences were uncovered between dormant and non-dormant embryos. In early development, the cell cycle-associated pathways were enriched in both embryo types but terminated with fewer nuclei in dormant embryos. As development progressed, the gene transcript abundance profiles became increasingly divergent between dormant and non-dormant embryos. Organogenesis was suspended in dormant embryos, concomitant with low transcript abundance of homeobox genes, and was replaced with an ATP-poor preparatory phase characterized by very high transcript abundance of genes encoding for hallmark dormancy proteins (e.g., LEA proteins, sHSP, and anti-ROS proteins, also found in plant seeds) and proteins involved in dormancy exit. Surprisingly, this period appeared analogous to the late maturation phase of plant seeds. Conclusions The study highlights novel divergent temporal transcript abundance patterns between dormant and non-dormant embryos. Remarkably, several convergent functional solutions appear during the development of resting eggs and plant seeds, suggesting a similar preparatory phase for long-term dormancy. This study accentuated the broad novel molecular features of long-term dormancy in encased animal embryos that behave like “animal seeds”. |
| first_indexed | 2024-03-08T10:00:42Z |
| format | Article |
| id | doaj.art-45a70f7e27474d2dbeb243320128d86c |
| institution | Directory Open Access Journal |
| issn | 1471-2164 |
| language | English |
| last_indexed | 2024-03-08T10:00:42Z |
| publishDate | 2024-01-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Genomics |
| spelling | doaj.art-45a70f7e27474d2dbeb243320128d86c2024-01-29T11:00:02ZengBMCBMC Genomics1471-21642024-01-0125112710.1186/s12864-024-09961-1A transcriptomic examination of encased rotifer embryos reveals the developmental trajectory leading to long-term dormancy; are they “animal seeds”?Tamar Hashimshony0Liron Levin1Andreas C. Fröbius2Nitsan Dahan3Vered Chalifa-Caspi4Reini Hamo5Oshri Gabai-Almog6Idit Blais7Yehuda G. Assaraf8Esther Lubzens9Faculty of Biology, Technion-Israel Institute of TechnologyNational Institute of Biotechnology in the Negev, Ben-Gurion University of the NegevMolecular Andrology, Biomedical Research Center Seltersberg (BFS), Justus Liebig University GießenInterdisciplinary Center for Life Sciences and Engineering, Technion-Israel Institute of TechnologyNational Institute of Biotechnology in the Negev, Ben-Gurion University of the NegevFaculty of Biology, Technion-Israel Institute of TechnologyFaculty of Biology, Technion-Israel Institute of TechnologyDepartment of Obstetrics and Gynecology, Division of Reproductive Endocrinology and IVF, Lady Davis Carmel Medical CenterThe Fred Wyszkowski Cancer Research Laboratory, Faculty of Biology, Technion-Israel Institute of TechnologyFaculty of Biology, Technion-Israel Institute of TechnologyAbstract Background Organisms from many distinct evolutionary lineages acquired the capacity to enter a dormant state in response to environmental conditions incompatible with maintaining normal life activities. Most studied organisms exhibit seasonal or annual episodes of dormancy, but numerous less studied organisms enter long-term dormancy, lasting decades or even centuries. Intriguingly, many planktonic animals produce encased embryos known as resting eggs or cysts that, like plant seeds, may remain dormant for decades. Herein, we studied a rotifer Brachionus plicatilis as a model planktonic species that forms encased dormant embryos via sexual reproduction and non-dormant embryos via asexual reproduction and raised the following questions: Which genes are expressed at which time points during embryogenesis? How do temporal transcript abundance profiles differ between the two types of embryos? When does the cell cycle arrest? How do dormant embryos manage energy? Results As the molecular developmental kinetics of encased embryos remain unknown, we employed single embryo RNA sequencing (CEL-seq) of samples collected during dormant and non-dormant embryogenesis. We identified comprehensive and temporal transcript abundance patterns of genes and their associated enriched functional pathways. Striking differences were uncovered between dormant and non-dormant embryos. In early development, the cell cycle-associated pathways were enriched in both embryo types but terminated with fewer nuclei in dormant embryos. As development progressed, the gene transcript abundance profiles became increasingly divergent between dormant and non-dormant embryos. Organogenesis was suspended in dormant embryos, concomitant with low transcript abundance of homeobox genes, and was replaced with an ATP-poor preparatory phase characterized by very high transcript abundance of genes encoding for hallmark dormancy proteins (e.g., LEA proteins, sHSP, and anti-ROS proteins, also found in plant seeds) and proteins involved in dormancy exit. Surprisingly, this period appeared analogous to the late maturation phase of plant seeds. Conclusions The study highlights novel divergent temporal transcript abundance patterns between dormant and non-dormant embryos. Remarkably, several convergent functional solutions appear during the development of resting eggs and plant seeds, suggesting a similar preparatory phase for long-term dormancy. This study accentuated the broad novel molecular features of long-term dormancy in encased animal embryos that behave like “animal seeds”.https://doi.org/10.1186/s12864-024-09961-1Long-term dormancyTranscriptomeEncased embryosEmbryogenesisRotifer |
| spellingShingle | Tamar Hashimshony Liron Levin Andreas C. Fröbius Nitsan Dahan Vered Chalifa-Caspi Reini Hamo Oshri Gabai-Almog Idit Blais Yehuda G. Assaraf Esther Lubzens A transcriptomic examination of encased rotifer embryos reveals the developmental trajectory leading to long-term dormancy; are they “animal seeds”? BMC Genomics Long-term dormancy Transcriptome Encased embryos Embryogenesis Rotifer |
| title | A transcriptomic examination of encased rotifer embryos reveals the developmental trajectory leading to long-term dormancy; are they “animal seeds”? |
| title_full | A transcriptomic examination of encased rotifer embryos reveals the developmental trajectory leading to long-term dormancy; are they “animal seeds”? |
| title_fullStr | A transcriptomic examination of encased rotifer embryos reveals the developmental trajectory leading to long-term dormancy; are they “animal seeds”? |
| title_full_unstemmed | A transcriptomic examination of encased rotifer embryos reveals the developmental trajectory leading to long-term dormancy; are they “animal seeds”? |
| title_short | A transcriptomic examination of encased rotifer embryos reveals the developmental trajectory leading to long-term dormancy; are they “animal seeds”? |
| title_sort | transcriptomic examination of encased rotifer embryos reveals the developmental trajectory leading to long term dormancy are they animal seeds |
| topic | Long-term dormancy Transcriptome Encased embryos Embryogenesis Rotifer |
| url | https://doi.org/10.1186/s12864-024-09961-1 |
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