Architecture and evolution of the cis-regulatory system of the echinoderm kirrelL gene
The gene regulatory network (GRN) that underlies echinoderm skeletogenesis is a prominent model of GRN architecture and evolution. KirrelL is an essential downstream effector gene in this network and encodes an Ig-superfamily protein required for the fusion of skeletogenic cells and the formation of...
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2022-02-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/72834 |
| _version_ | 1797998421461696512 |
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| author | Jian Ming Khor Charles A Ettensohn |
| author_facet | Jian Ming Khor Charles A Ettensohn |
| author_sort | Jian Ming Khor |
| collection | DOAJ |
| description | The gene regulatory network (GRN) that underlies echinoderm skeletogenesis is a prominent model of GRN architecture and evolution. KirrelL is an essential downstream effector gene in this network and encodes an Ig-superfamily protein required for the fusion of skeletogenic cells and the formation of the skeleton. In this study, we dissected the transcriptional control region of the kirrelL gene of the purple sea urchin, Strongylocentrotus purpuratus. Using plasmid- and bacterial artificial chromosome-based transgenic reporter assays, we identified key cis-regulatory elements (CREs) and transcription factor inputs that regulate Sp-kirrelL, including direct, positive inputs from two key transcription factors in the skeletogenic GRN, Alx1 and Ets1. We next identified kirrelL cis-regulatory regions from seven other echinoderm species that together represent all classes within the phylum. By introducing these heterologous regulatory regions into developing sea urchin embryos we provide evidence of their remarkable conservation across ~500 million years of evolution. We dissected in detail the kirrelL regulatory region of the sea star, Patiria miniata, and demonstrated that it also receives direct inputs from Alx1 and Ets1. Our findings identify kirrelL as a component of the ancestral echinoderm skeletogenic GRN. They support the view that GRN subcircuits, including specific transcription factor–CRE interactions, can remain stable over vast periods of evolutionary history. Lastly, our analysis of kirrelL establishes direct linkages between a developmental GRN and an effector gene that controls a key morphogenetic cell behavior, cell–cell fusion, providing a paradigm for extending the explanatory power of GRNs. |
| first_indexed | 2024-04-11T10:48:29Z |
| format | Article |
| id | doaj.art-1b9ac13785c440b78c2dcb85414fbbb7 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-11T10:48:29Z |
| publishDate | 2022-02-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-1b9ac13785c440b78c2dcb85414fbbb72022-12-22T04:28:58ZengeLife Sciences Publications LtdeLife2050-084X2022-02-011110.7554/eLife.72834Architecture and evolution of the cis-regulatory system of the echinoderm kirrelL geneJian Ming Khor0https://orcid.org/0000-0002-1428-6770Charles A Ettensohn1https://orcid.org/0000-0002-3625-0955Department of Biological Sciences, Carnegie Mellon University, Pittsburgh, United StatesDepartment of Biological Sciences, Carnegie Mellon University, Pittsburgh, United StatesThe gene regulatory network (GRN) that underlies echinoderm skeletogenesis is a prominent model of GRN architecture and evolution. KirrelL is an essential downstream effector gene in this network and encodes an Ig-superfamily protein required for the fusion of skeletogenic cells and the formation of the skeleton. In this study, we dissected the transcriptional control region of the kirrelL gene of the purple sea urchin, Strongylocentrotus purpuratus. Using plasmid- and bacterial artificial chromosome-based transgenic reporter assays, we identified key cis-regulatory elements (CREs) and transcription factor inputs that regulate Sp-kirrelL, including direct, positive inputs from two key transcription factors in the skeletogenic GRN, Alx1 and Ets1. We next identified kirrelL cis-regulatory regions from seven other echinoderm species that together represent all classes within the phylum. By introducing these heterologous regulatory regions into developing sea urchin embryos we provide evidence of their remarkable conservation across ~500 million years of evolution. We dissected in detail the kirrelL regulatory region of the sea star, Patiria miniata, and demonstrated that it also receives direct inputs from Alx1 and Ets1. Our findings identify kirrelL as a component of the ancestral echinoderm skeletogenic GRN. They support the view that GRN subcircuits, including specific transcription factor–CRE interactions, can remain stable over vast periods of evolutionary history. Lastly, our analysis of kirrelL establishes direct linkages between a developmental GRN and an effector gene that controls a key morphogenetic cell behavior, cell–cell fusion, providing a paradigm for extending the explanatory power of GRNs.https://elifesciences.org/articles/72834kirrelLCis-regulatory analysisCis-regulatory elementsGene regulatory networkSkeletogenesisEchinoderm |
| spellingShingle | Jian Ming Khor Charles A Ettensohn Architecture and evolution of the cis-regulatory system of the echinoderm kirrelL gene eLife kirrelL Cis-regulatory analysis Cis-regulatory elements Gene regulatory network Skeletogenesis Echinoderm |
| title | Architecture and evolution of the cis-regulatory system of the echinoderm kirrelL gene |
| title_full | Architecture and evolution of the cis-regulatory system of the echinoderm kirrelL gene |
| title_fullStr | Architecture and evolution of the cis-regulatory system of the echinoderm kirrelL gene |
| title_full_unstemmed | Architecture and evolution of the cis-regulatory system of the echinoderm kirrelL gene |
| title_short | Architecture and evolution of the cis-regulatory system of the echinoderm kirrelL gene |
| title_sort | architecture and evolution of the cis regulatory system of the echinoderm kirrell gene |
| topic | kirrelL Cis-regulatory analysis Cis-regulatory elements Gene regulatory network Skeletogenesis Echinoderm |
| url | https://elifesciences.org/articles/72834 |
| work_keys_str_mv | AT jianmingkhor architectureandevolutionofthecisregulatorysystemoftheechinodermkirrellgene AT charlesaettensohn architectureandevolutionofthecisregulatorysystemoftheechinodermkirrellgene |