Conserved developmental expression of Fezf in chordates and Drosophila and the origin of the Zona Limitans Intrathalamica (ZLI) brain organizer

Irimia, Manuel; Piñeiro, Cristina; Maeso, Ignacio; Gómez-Skármeta, José Luis; Casares, Fernando; Garcia‐Fernàndez, Jordi

doi:10.1186/2041-9139-1-7

Cited by 56 publications

(53 citation statements)

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“…6). This gene is involved in establishing a deeply conserved early anterior-posterior (A-P) brain patterning (Simeone et al 1992;Hirth et al 2003;Castro et al 2006;Irimia et al 2010) and is expressed in the anterior nervous system of nearly all studied bilaterians (Simeone et al 1992;Williams and Holland 1996;Hirth et al 2003;Lowe et al 2003;Scholpp et al 2007). We found that Otx is linked to Ehbp1 (EH domain binding protein 1) in nearly all species, from placozoans to humans, spanning over 700 MY (Fig.…”

Section: Experimental Evidence For Grbs In Vertebrate Developmentmentioning

confidence: 99%

Extensive conservation of ancient microsynteny across metazoans due to cis-regulatory constraints

et al. 2012

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The order of genes in eukaryotic genomes has generally been assumed to be neutral, since gene order is largely scrambled over evolutionary time. Only a handful of exceptional examples are known, typically involving deeply conserved clusters of tandemly duplicated genes (e.g., Hox genes and histones). Here we report the first systematic survey of microsynteny conservation across metazoans, utilizing 17 genome sequences. We identified nearly 600 pairs of unrelated genes that have remained tightly physically linked in diverse lineages across over 600 million years of evolution. Integrating sequence conservation, gene expression data, gene function, epigenetic marks, and other genomic features, we provide extensive evidence that many conserved ancient linkages involve (1) the coordinated transcription of neighboring genes, or (2) genomic regulatory blocks (GRBs) in which transcriptional enhancers controlling developmental genes are contained within nearby bystander genes. In addition, we generated ChIP-seq data for key histone modifications in zebrafish embryos, which provided further evidence of putative GRBs in embryonic development. Finally, using chromosome conformation capture (3C) assays and stable transgenic experiments, we demonstrate that enhancers within bystander genes drive the expression of genes such as Otx and Islet, critical regulators of central nervous system development across bilaterians. These results suggest that ancient genomic functional associations are far more common than previously thought-involving~12% of the ancestral bilaterian genome-and that cis-regulatory constraints are crucial in determining metazoan genome architecture.

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Section: Experimental Evidence For Grbs In Vertebrate Developmentmentioning

confidence: 99%

Extensive conservation of ancient microsynteny across metazoans due to cis-regulatory constraints

et al. 2012

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“…In vertebrates, Otx and Gbx mutually repress one another and have been shown to position the MHB; they likely do so as well in amphioxus. Similarly, in vertebrates, the domains of Fezf and Irx, which mutually repress each other, abut at the ISO and in amphioxus abut about the midpoint of the diencephalon (Irimia et al, 2010). In S. kowalevskii, Otx, Gbx, Fezf and Irx are not expressed as they are in chordates (Pani et al, 2012) (Fig.…”

Section: Reviewmentioning

confidence: 99%

Evolution of basal deuterostome nervous systems

Holland

2015

Journal of Experimental Biology

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Understanding the evolution of deuterostome nervous systems has been complicated by the ambiguous phylogenetic position of the Xenocoelomorpha (Xenoturbellids, acoel flat worms, nemertodermatids), which has been placed either as basal bilaterians, basal deuterostomes or as a sister group to the hemichordate/ echinoderm clade (Ambulacraria), which is a sister group of the Chordata. None of these groups has a single longitudinal nerve cord and a brain. A further complication is that echinoderm nerve cords are not likely to be evolutionarily related to the chordate central nervous system. For hemichordates, opinion is divided as to whether either one or none of the two nerve cords is homologous to the chordate nerve cord. In chordates, opposition by two secreted signaling proteins, bone morphogenetic protein (BMP) and Nodal, regulates partitioning of the ectoderm into central and peripheral nervous systems. Similarly, in echinoderm larvae, opposition between BMP and Nodal positions the ciliary band and regulates its extent. The apparent loss of this opposition in hemichordates is, therefore, compatible with the scenario, suggested by Dawydoff over 65 years ago, that a true centralized nervous system was lost in hemichordates. KEY WORDS: Cephalochordate, Deuterostomes, Echinoderm, Hemichordate, Nervous system evolution IntroductionDeuterostomes include at least the Chordata (vertebrates, tunicates and cephalochordates) and the Ambulacraria (echinoderms and hemichordates). The enigmatic Xenoturbellida has been placed either basally in the deuterostomes or together with acoel flatworms as the Xenocoelomorpha -the sister group of the Ambulacraria. Alternatively, the Xenocoelomorpha have been placed basal to the bilateria (reviewed in Achatz et al., 2013). Xenoturbella has a very simple body plan with a nerve net and is thought to have lost a number of ancestral features (Philippe et al., 2011). Therefore, it is unclear whether it is at all relevant to the evolution of deuterostome nervous systems. However, there is no question that echinoderms and hemichordates are deuterostomes. In most phylogenetic analyses, Ambulacraria are the sister group of the chordates (Blair and Hedges, 2005; Delsuc et al., 2008; Edgecombe et al., 2011). However, a recent analysis based on 586 nuclear genes places cephalochordates as the sister group of the Ambulacraria with high bootstrap support and cephalochordates plus Ambulacraria as the sister group of tunicates plus vertebrates (Moroz et al., 2014). Because the nervous systems of echinoderms, hemichordates and chordates are so very different, it has been controversial whether the ancestral deuterostome had a longitudinal nerve cord or a nerve net or a combination of both.Several schemes for the evolution of deuterostome nervous systems have focused on the possible contribution of the larval REVIEW Marine Biology Research Division, Scripps Institution of Oceanography, University of California San Diego, La Jolla, CA 92093-0202, USA.*Author for correspondence (lzholland@ucsd.edu)...

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“…These data have been used to support the plausible hypothesis that most vertebrate brain signaling centers were sequentially assembled during chordate evolution. In this scenario, the recruitment of signaling ligands to these centers was the final step achieved in stem vertebrates (Holland, 2009;Irimia et al, 2010). However, ectodermal signaling centers that might be homologous to three of those found in vertebrate brains have now been described in S. kowalevskii (Pani et al, 2012), suggesting that these developmental programs predate chordate origins and were first assembled independently of the vertebrate brain.…”

Section: Basic Body Plan Comparisons Anteroposterior Patterningmentioning

confidence: 99%

“…In all vertebrates, local signaling centers in the neural plate, characterized by expression of secreted ligands in predictable AP positions within a conserved transcriptional map, act to divide the brain into discrete regions (Wurst and Bally-Cuif, 2001;Echevarria et al, 2003;Wilson and Houart, 2004;Kiecker and Lumsden, 2005). Although some of the transcriptional signatures associated with vertebrate signaling centers are present in invertebrate chordates (Holland, 2009;Irimia et al, 2010), in most instances the signaling ligands that define the organizing abilities of these centers in vertebrates are not expressed in the corresponding AP positions in the amphioxus and ascidian nervous systems or general ectoderm. These data have been used to support the plausible hypothesis that most vertebrate brain signaling centers were sequentially assembled during chordate evolution.…”

Section: Basic Body Plan Comparisons Anteroposterior Patterningmentioning

confidence: 99%

Evolutionary crossroads in developmental biology: hemichordates

Röttinger

Lowe

2012

Development

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Hemichordates are a deuterostome phylum, the sister group to echinoderms, and closely related to chordates. They have thus been used to gain insights into the origins of deuterostome and chordate body plans. Developmental studies of this group have a long and distinguished history. Recent improvements in animal husbandry, functional tool development and genomic resources have resulted in novel developmental data from several species in this group. In this Primer, we introduce representative hemichordate species with contrasting modes of development and summarize recent findings that are beginning to yield important insights into deuterostome developmental mechanisms.

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Conserved developmental expression of Fezf in chordates and Drosophila and the origin of the Zona Limitans Intrathalamica (ZLI) brain organizer

Cited by 56 publications

References 57 publications

Extensive conservation of ancient microsynteny across metazoans due to cis-regulatory constraints

Extensive conservation of ancient microsynteny across metazoans due to cis-regulatory constraints

Evolution of basal deuterostome nervous systems

Evolutionary crossroads in developmental biology: hemichordates

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