{"title":"Duplication of spiralian-specific TALE genes and evolution of the blastomere specification mechanism in the bivalve lineage.","authors":"Supanat Phuangphong, Jumpei Tsunoda, Hiroshi Wada, Yoshiaki Morino","doi":"10.1186/s13227-021-00181-2","DOIUrl":null,"url":null,"abstract":"<p><strong>Background: </strong>Despite the conserved pattern of the cell-fate map among spiralians, bivalves display several modified characteristics during their early development, including early specification of the D blastomere by the cytoplasmic content, as well as the distinctive fate of the 2d blastomere. However, it is unclear what changes in gene regulatory mechanisms led to such changes in cell specification patterns. Spiralian-TALE (SPILE) genes are a group of spiralian-specific transcription factors that play a role in specifying blastomere cell fates during early development in limpets. We hypothesised that the expansion of SPILE gene repertoires influenced the evolution of the specification pattern of blastomere cell fates.</p><p><strong>Results: </strong>We performed a transcriptome analysis of early development in the purplish bifurcate mussel and identified 13 SPILE genes. Phylogenetic analysis of the SPILE gene in molluscs suggested that duplications of SPILE genes occurred in the bivalve lineage. We examined the expression patterns of the SPILE gene in mussels and found that some SPILE genes were expressed in quartet-specific patterns, as observed in limpets. Furthermore, we found that several SPILE genes that had undergone gene duplication were specifically expressed in the D quadrant, C and D quadrants or the 2d blastomere. These expression patterns were distinct from the expression patterns of SPILE in their limpet counterparts.</p><p><strong>Conclusions: </strong>These results suggest that, in addition to their ancestral role in quartet specification, certain SPILE genes in mussels contribute to the specification of the C and D quadrants. We suggest that the expansion of SPILE genes in the bivalve lineage contributed to the evolution of a unique cell fate specification pattern in bivalves.</p>","PeriodicalId":49076,"journal":{"name":"Evodevo","volume":null,"pages":null},"PeriodicalIF":4.1000,"publicationDate":"2021-10-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8524836/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Evodevo","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1186/s13227-021-00181-2","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"DEVELOPMENTAL BIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Background: Despite the conserved pattern of the cell-fate map among spiralians, bivalves display several modified characteristics during their early development, including early specification of the D blastomere by the cytoplasmic content, as well as the distinctive fate of the 2d blastomere. However, it is unclear what changes in gene regulatory mechanisms led to such changes in cell specification patterns. Spiralian-TALE (SPILE) genes are a group of spiralian-specific transcription factors that play a role in specifying blastomere cell fates during early development in limpets. We hypothesised that the expansion of SPILE gene repertoires influenced the evolution of the specification pattern of blastomere cell fates.
Results: We performed a transcriptome analysis of early development in the purplish bifurcate mussel and identified 13 SPILE genes. Phylogenetic analysis of the SPILE gene in molluscs suggested that duplications of SPILE genes occurred in the bivalve lineage. We examined the expression patterns of the SPILE gene in mussels and found that some SPILE genes were expressed in quartet-specific patterns, as observed in limpets. Furthermore, we found that several SPILE genes that had undergone gene duplication were specifically expressed in the D quadrant, C and D quadrants or the 2d blastomere. These expression patterns were distinct from the expression patterns of SPILE in their limpet counterparts.
Conclusions: These results suggest that, in addition to their ancestral role in quartet specification, certain SPILE genes in mussels contribute to the specification of the C and D quadrants. We suggest that the expansion of SPILE genes in the bivalve lineage contributed to the evolution of a unique cell fate specification pattern in bivalves.
背景:尽管在螺旋体中细胞命运图谱的模式是保守的，但双壳类动物在其早期发育过程中显示出一些改变的特征，包括细胞质含量对D裂球的早期规范，以及2d裂球的独特命运。然而，目前尚不清楚是什么基因调控机制的变化导致了细胞特异性模式的变化。螺旋- tale (SPILE)基因是一组螺旋特异性转录因子，在帽贝发育早期决定卵裂球细胞命运中起作用。我们假设SPILE基因库的扩增影响了卵裂球细胞命运规范模式的进化。结果:我们对紫色分叉贻贝的早期发育进行了转录组分析，并鉴定了13个SPILE基因。对软体动物SPILE基因的系统发育分析表明，SPILE基因在双壳类动物谱系中存在重复。我们检查了贻贝中SPILE基因的表达模式，发现一些SPILE基因以四组特异性模式表达，正如在帽贝中观察到的那样。此外，我们还发现一些经过基因复制的SPILE基因在D象限、C和D象限或2d卵裂球中特异性表达。这些表达模式不同于SPILE在帽贝中的表达模式。结论:这些结果表明，贻贝中的某些SPILE基因除了在四象限规范中发挥祖先作用外，还有助于C和D象限的规范。我们认为，SPILE基因在双壳类动物谱系中的扩展促进了双壳类动物独特的细胞命运规范模式的进化。
期刊介绍：
EvoDevo publishes articles on a broad range of topics associated with the translation of genotype to phenotype in a phylogenetic context. Understanding the history of life, the evolution of novelty and the generation of form, whether through embryogenesis, budding, or regeneration are amongst the greatest challenges in biology. We support the understanding of these processes through the many complementary approaches that characterize the field of evo-devo.
The focus of the journal is on research that promotes understanding of the pattern and process of morphological evolution.
All articles that fulfill this aim will be welcome, in particular: evolution of pattern; formation comparative gene function/expression; life history evolution; homology and character evolution; comparative genomics; phylogenetics and palaeontology
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