Coup-TF: A maternal factor essential for differentiation along the embryonic axes in the sea urchin Paracentrotus lividus

Tsironis, Ioannis; Paganos, Periklis; Gouvi, Georgia; Tsimpos, Panagiotis; Σταμοπούλου, Ανδριάνα; Arnone, Maria Ina; Flytzanis, Constantin N.

doi:10.1016/j.ydbio.2020.12.012

Cited by 11 publications

(16 citation statements)

References 83 publications

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“…In invertebrate deuterostomes, the single Nr2f1/2/5/6 orthologs are expressed in neural tissue of sea urchin ( Strongylocentrotus purpuratus ), amphioxus, and sea squirt embryos [ 11 , 64 – 66 ]. Recent functional analysis of the Mediterranean sea urchin ( Paracentrotus lividus ) Nr2f1/2/5/6 shows that it is required for the development of neural and ectodermal derivatives [ 67 ]. A Nr2f1/2/5/6 ortholog from the agnathan River lamprey ( Lampetra fluviatilis ) is also expressed in the developing nervous system [ 61 ].…”

Section: Discussionmentioning

confidence: 99%

Origin and evolutionary landscape of Nr2f transcription factors across Metazoa

Coppola

Waxman

2021

PLoS ONE

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Background Nuclear Receptor Subfamily 2 Group F (Nr2f) orphan nuclear hormone transcription factors (TFs) are fundamental regulators of many developmental processes in invertebrates and vertebrates. Despite the importance of these TFs throughout metazoan development, previous work has not clearly outlined their evolutionary history. Results We integrated molecular phylogeny with comparisons of intron/exon structure, domain architecture, and syntenic conservation to define critical evolutionary events that distinguish the Nr2f gene family in Metazoa. Our data indicate that a single ancestral eumetazoan Nr2f gene predated six main Bilateria subfamilies, which include single Nr2f homologs, here referred to as Nr2f1/2/5/6, that are present in invertebrate protostomes and deuterostomes, Nr2f1/2 homologs in agnathans, and Nr2f1, Nr2f2, Nr2f5, and Nr2f6 orthologs that are found in gnathostomes. Four cnidarian Nr2f1/2/5/6 and three agnathan Nr2f1/2 members are each due to independent expansions, while the vertebrate Nr2f1/Nr2f2 and Nr2f5/Nr2f6 members each form paralogous groups that arose from the established series of whole-genome duplications (WGDs). Nr2f6 members are the most divergent Nr2f subfamily in gnathostomes. Interestingly, in contrast to the other gnathostome Nr2f subfamilies, Nr2f5 has been independently lost in numerous vertebrate lineages. Furthermore, our analysis shows there are differential expansions and losses of Nr2f genes in teleosts following their additional rounds of WGDs. Conclusion Overall, our analysis of Nr2f gene evolution helps to reveal the origins and previously unrecognized relationships of this ancient TF family, which may allow for greater insights into the conservation of Nr2f functions that shape Metazoan body plans.

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Section: Discussionmentioning

confidence: 99%

Origin and evolutionary landscape of Nr2f transcription factors across Metazoa

Coppola

Waxman

2021

PLoS ONE

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“…In invertebrate deuterostomes, the single Nr2f1/2/5 orthologs are expressed in neural tissue of sea urchin (Strongylocentrotus purpuratus), amphioxus, and sea squirt embryos [11,57,58], [59]. Interestingly, recent functional analysis of the Mediterranean sea urchin (Paracentrotus lividus) Nr2f1/2/5 shows that it is maternally inherited and required for the development of neural and ectodermal derivatives [60]. A Nr2f1/2/5 ortholog from the agnathan river lamprey (Lampetra fluviatilis) is also expressed in the developing nervous system [53].…”

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

“…It is interesting that the single Nr2f1/2/5 homolog of flies (svp) is also required for dorsal vessel (heart) development [20]. However, if these similar roles in heart tissues reflect conserved requirements within metazoans for cardiac differentiation requires functional studies from many additional model organisms, though the analysis in sea urchins hints at conservation of more ancestral requirements in all germ layers [60]. With respect to the expansion of Nr2f1 and Nr2f2 in teleosts, Nr2f1b has been lost in the majority of surveyed teleosts.…”

Section: Discussionmentioning

confidence: 99%

“…In addition to the conservation of Nr2f1/2/5/6, Nr2f1/2/5, and Nr2f1/2 expression in neural tissues from cnidarians to agnathans, Nr2f genes have also evolved critical new expression and functionalities, such as copulation control in nematodes [61] or heart vessels specification in flies [20,21]. The recent work with the Mediterranean sea urchin suggests that it is required for the development of mesendodermal derivative [60], supporting that ancestral Nr2fs also acquired requirements in all 3 germ layers within the invertebrate lineage. However, the conservation of these requirements in the different germ layers throughout different metazoan phyla is not yet as clear, with present analyses suggesting functions in mesendodermal tissues are newly derived functions.…”

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confidence: 99%

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Origin and evolutionary landscape of Nr2f transcription factors across Metazoa

Coppola

Waxman

2021

Preprint

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Background: Nuclear Receptor Subfamily 2 Group F (Nr2f) orphan nuclear hormone transcription factors (TFs) are fundamental regulators of many developmental processes in invertebrates and vertebrates. Despite the importance of these TFs throughout metazoan development, previous work has not clearly outlined their evolutionary history. Results: We integrated molecular phylogeny with comparisons of intron/exon structure, domain architecture, and syntenic conservation to define critical evolutionary events that distinguish the Nr2f gene family in Metazoa. Our data indicate that a single ancestral pre-metazoan Nr2f gene, we have termed Nr2f1/2/5/6, predated six main Bilateria subfamilies, which include a single Nr2f1/2/5 homolog that is present throughout protostomes and invertebrate deuterostomes, Nr2f1/2 homologs in agnathans, and Nr2f1 , Nr2f2 , Nr2f5 , Nr2f6 orthologs that are found in gnathostomes. The three Nr2f1/2 members in agnathans are due to independent expansions not found in gnathostomes, while the vertebrate Nr2f1 , Nr2f2 , Nr2f5 members arose from whole-genome duplications (WGDs). However, Nr2f6 members are the most divergent subfamily, likely originating from an ancient duplication, and are only retained by gnathostomes. Interestingly, Nr2f5 TFs have been independently lost in both cartilaginous fish and amniotes, such as humans. Furthermore, our analysis shows there are differential expansions and losses of Nr2f genes in teleosts following their additional rounds of WGDs. Conclusion: Overall, our evolutionary genomic analysis of Nr2f proteins helps to reveal the origins and previously unrecognized relationships of this ancient transcription factor family, which may allow for greater insights into the conservation of Nr2f functions that shape Metazoan body plans.

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Dorsal-ventral axis formation in sea urchin embryos

2022

Current Topics in Developmental Biology

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Coup-TF: A maternal factor essential for differentiation along the embryonic axes in the sea urchin Paracentrotus lividus

Cited by 11 publications

References 83 publications

Origin and evolutionary landscape of Nr2f transcription factors across Metazoa

Origin and evolutionary landscape of Nr2f transcription factors across Metazoa

Origin and evolutionary landscape of Nr2f transcription factors across Metazoa

Dorsal-ventral axis formation in sea urchin embryos

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