Developmental hourglass and heterochronic shifts in fin and limb development
How genetic changes are linked to morphological novelties and developmental constraints remains elusive. Here, we investigate genetic apparatuses that distinguish fish fins from tetrapod limbs by analyzing transcriptomes and open-chromatin regions (OCRs). Specifically, we compared mouse forelimb bud...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2021-02-01
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| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/62865 |
| _version_ | 1828168877309165568 |
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| author | Koh Onimaru Kaori Tatsumi Chiharu Tanegashima Mitsutaka Kadota Osamu Nishimura Shigehiro Kuraku |
| author_facet | Koh Onimaru Kaori Tatsumi Chiharu Tanegashima Mitsutaka Kadota Osamu Nishimura Shigehiro Kuraku |
| author_sort | Koh Onimaru |
| collection | DOAJ |
| description | How genetic changes are linked to morphological novelties and developmental constraints remains elusive. Here, we investigate genetic apparatuses that distinguish fish fins from tetrapod limbs by analyzing transcriptomes and open-chromatin regions (OCRs). Specifically, we compared mouse forelimb buds with the pectoral fin buds of an elasmobranch, the brown-banded bamboo shark (Chiloscyllium punctatum). A transcriptomic comparison with an accurate orthology map revealed both a mass heterochrony and hourglass-shaped conservation of gene expression between fins and limbs. Furthermore, open-chromatin analysis suggested that access to conserved regulatory sequences is transiently increased during mid-stage limb development. During this stage, stage-specific and tissue-specific OCRs were also enriched. Together, early and late stages of fin/limb development are more permissive to mutations than middle stages, which may have contributed to major morphological changes during the fin-to-limb evolution. We hypothesize that the middle stages are constrained by regulatory complexity that results from dynamic and tissue-specific transcriptional controls. |
| first_indexed | 2024-04-12T02:42:00Z |
| format | Article |
| id | doaj.art-5aaba729177449ceb36f3e304910e7c9 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T02:42:00Z |
| publishDate | 2021-02-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-5aaba729177449ceb36f3e304910e7c92022-12-22T03:51:17ZengeLife Sciences Publications LtdeLife2050-084X2021-02-011010.7554/eLife.62865Developmental hourglass and heterochronic shifts in fin and limb developmentKoh Onimaru0https://orcid.org/0000-0002-2428-9510Kaori Tatsumi1Chiharu Tanegashima2Mitsutaka Kadota3Osamu Nishimura4https://orcid.org/0000-0003-1969-2580Shigehiro Kuraku5https://orcid.org/0000-0003-1464-8388Laboratory for Phyloinformatics, RIKEN Center for Biosystems Dynamics Research (BDR), Kobe, Japan; Laboratory for Bioinformatics Research, RIKEN BDR, Wako City, Japan; Molecular Oncology Laboratory, Graduate School of Medicine, Nagoya University, Nagoya, JapanLaboratory for Phyloinformatics, RIKEN Center for Biosystems Dynamics Research (BDR), Kobe, JapanLaboratory for Phyloinformatics, RIKEN Center for Biosystems Dynamics Research (BDR), Kobe, JapanLaboratory for Phyloinformatics, RIKEN Center for Biosystems Dynamics Research (BDR), Kobe, JapanLaboratory for Phyloinformatics, RIKEN Center for Biosystems Dynamics Research (BDR), Kobe, JapanLaboratory for Phyloinformatics, RIKEN Center for Biosystems Dynamics Research (BDR), Kobe, JapanHow genetic changes are linked to morphological novelties and developmental constraints remains elusive. Here, we investigate genetic apparatuses that distinguish fish fins from tetrapod limbs by analyzing transcriptomes and open-chromatin regions (OCRs). Specifically, we compared mouse forelimb buds with the pectoral fin buds of an elasmobranch, the brown-banded bamboo shark (Chiloscyllium punctatum). A transcriptomic comparison with an accurate orthology map revealed both a mass heterochrony and hourglass-shaped conservation of gene expression between fins and limbs. Furthermore, open-chromatin analysis suggested that access to conserved regulatory sequences is transiently increased during mid-stage limb development. During this stage, stage-specific and tissue-specific OCRs were also enriched. Together, early and late stages of fin/limb development are more permissive to mutations than middle stages, which may have contributed to major morphological changes during the fin-to-limb evolution. We hypothesize that the middle stages are constrained by regulatory complexity that results from dynamic and tissue-specific transcriptional controls.https://elifesciences.org/articles/62865brown-banded bamboo sharkfin developmentlimb developmentmorphological evolutiontranscriptomeATAC-seq |
| spellingShingle | Koh Onimaru Kaori Tatsumi Chiharu Tanegashima Mitsutaka Kadota Osamu Nishimura Shigehiro Kuraku Developmental hourglass and heterochronic shifts in fin and limb development eLife brown-banded bamboo shark fin development limb development morphological evolution transcriptome ATAC-seq |
| title | Developmental hourglass and heterochronic shifts in fin and limb development |
| title_full | Developmental hourglass and heterochronic shifts in fin and limb development |
| title_fullStr | Developmental hourglass and heterochronic shifts in fin and limb development |
| title_full_unstemmed | Developmental hourglass and heterochronic shifts in fin and limb development |
| title_short | Developmental hourglass and heterochronic shifts in fin and limb development |
| title_sort | developmental hourglass and heterochronic shifts in fin and limb development |
| topic | brown-banded bamboo shark fin development limb development morphological evolution transcriptome ATAC-seq |
| url | https://elifesciences.org/articles/62865 |
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