Expression of somite segmentation genes in amphioxus: a clock without a wavefront?

Beaster-Jones, Laura; Kaltenbach, Stacy L.; Koop, Demian; Yuan, Shaochun; Chastain, Roger A.; Holland, Linda Z.

doi:10.1007/s00427-008-0257-5

Cited by 46 publications

(63 citation statements)

References 56 publications

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“…Both genes are also expressed in the genital tubercle (GT), and whereas GT-specific inactivation of Fgf4 and Fgf8 shows that they are dispensable for GT outgrowth, this may be due to increased activity of other ligands (38). Furthermore, in all three systems, FGF activity is regulated by WNT signaling (38,39), and the coordinate WNT/FGF signaling system may have evolved in early chordates to link the somite clock to body axis extension (40). These data support speculations that programs controlling axis and tail extension have been co-opted over the course of evolution to control the outgrowth of multiple appendages (41,42).…”

Section: Discussionmentioning

confidence: 99%

FGF4 and FGF8 comprise the wavefront activity that controls somitogenesis

Naiche

Holder

Lewandoski

2011

Proc. Natl. Acad. Sci. U.S.A.

160

191

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Somites form along the embryonic axis by sequential segmentation from the presomitic mesoderm (PSM) and differentiate into the segmented vertebral column as well as other unsegmented tissues. Somites are thought to form via the intersection of two activities known as the clock and the wavefront. Previous work has suggested that fibroblast growth factor (FGF) activity may be the wavefront signal, which maintains the PSM in an undifferentiated state. However, it is unclear which (if any) of the FGFs expressed in the PSM comprise this activity, as removal of any one gene is insufficient to disrupt early somitogenesis. Here we show that when both Fgf4 and Fgf8 are deleted in the PSM, expression of most PSM genes is absent, including cycling genes, WNT pathway genes, and markers of undifferentiated PSM. Significantly, markers of nascent somite cell fate expand throughout the PSM, demonstrating the premature differentiation of this entire tissue, a highly unusual phenotype indicative of the loss of wavefront activity. When WNT signaling is restored in mutants, PSM progenitor markers are partially restored but premature differentiation of the PSM still occurs, demonstrating that FGF signaling operates independently of WNT signaling. This study provides genetic evidence that FGFs are the wavefront signal and identifies the specific FGF ligands that encode this activity. Furthermore, these data show that FGF action maintains WNT signaling, and that both signaling pathways are required in parallel to maintain PSM progenitor tissue.genetic redundancy | Spry | T-Cre | axis extension | paraxial mesoderm

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Section: Discussionmentioning

confidence: 99%

FGF4 and FGF8 comprise the wavefront activity that controls somitogenesis

Naiche

Holder

Lewandoski

2011

Proc. Natl. Acad. Sci. U.S.A.

160

191

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“…Beyond this ontological division, expression of several genes clearly functionally divides anterior from posterior somites. Engrailed, OligA, and Pbx (24) are specific gene markers of the anterior enterocoelic somites, and Axin, Lcx, and Paraxis specifically label the tailbud during posterior somitogenesis (24). However, several data suggest an additional division of the amphioxus somites, particularly within the anterior enterocoelic ones.…”

Section: Discussion Evolution Of the Fgf Gene Family Inmentioning

confidence: 99%

Amphioxus FGF signaling predicts the acquisition of vertebrate morphological traits

Bertrand

Camasses

Somorjai

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

102

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FGF signaling is one of the few cell-cell signaling pathways conserved among all metazoans. The diversity of FGF gene content among different phyla suggests that evolution of FGF signaling may have participated in generating the current variety of animal forms. Vertebrates possess the greatest number of FGF genes, the functional evolution of which may have been implicated in the acquisition of vertebrate-specific morphological traits. In this study, we have investigated the roles of the FGF signal during embryogenesis of the cephalochordate amphioxus, the best proxy for the chordate ancestor. We first isolate the full FGF gene complement and determine the evolutionary relationships between amphioxus and vertebrate FGFs via phylogenetic and synteny conservation analysis. Using pharmacological treatments, we inhibit the FGF signaling pathway in amphioxus embryos in different time windows. Our results show that the requirement for FGF signaling during gastrulation is a conserved character among chordates, whereas this signal is not necessary for neural induction in amphioxus, in contrast to what is known in vertebrates. We also show that FGF signal, acting through the MAPK pathway, is necessary for the formation of the most anterior somites in amphioxus, whereas more posterior somite formation is not FGF-dependent. This result leads us to propose that modification of the FGF signal function in the anterior paraxial mesoderm in an amphioxus-like vertebrate ancestor might have contributed to the loss of segmentation in the preotic paraxial mesoderm of the vertebrate head.O nly a few cell-cell signaling molecules are known to play a major role during metazoan embryonic development. Among them, the FGFs were discovered in the mid-1970s in vertebrates. FGFs are small proteins, generally secreted, characterized by a conserved functional domain and acting through binding to their transmembrane receptors [FGF receptors (FGFRs)], causing them to homodimerize. This leads to intracellular autophosphorylation and further activation of cytoplasmic signaling cascades, such as the MAPK and the PI3K pathways (1).Sequencing of several complete metazoan genomes has shown that FGF and FGFR genes were already present in the common ancestor of diploblastic and bilaterian animals (2). In vertebrates, at least 22 genes coding for FGFs and 4 coding for their FGFRs are known. In contrast, only 3 genes coding for FGFs and 2 coding for FGFRs have been described in Drosophila (2). In the urochordate Ciona intestinalis, a member of the sister group of vertebrates, only 6 FGF genes are present, for which some orthology relationships with vertebrate FGFs are still not resolved (3). This large number of FGFs and FGFRs in vertebrates raises the question of their implication in the evolution of vertebrate-specific morphological characteristics.In vertebrates, FGF signaling is involved in different developmental processes, among which are neural and mesoderm induction in the early embryo, and somitogenesis and limb bud formation at later stages (4)....

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“…We examined mesoPrx (mPrx), a homolog of prx1 and prx2 (Cserjesi et al, 1992;de Jong and Meijlink, 1993;Leussink et al, 1995;Norris et al, 2000;Jones et al, 2001;Doufexi and Mina, 2008); mesp, a paralog to the vertebrate mesp and mesogenin (Saga et al, 1996;Saga et al, 1997;Sawada et al, 2000;Satou et al, 2004;Imai et al, 2006;Saga and Takahashi, 2008); six1 (Kozmik et al, 2007;Beaster-Jones et al, 2008;Gillis et al, 2012); and snail (Hammerschmidt and Nüsslein-Volhard, 1993;Erives et al, 1998;Fujiwara et al, 1998;Langeland et al, 1998;Cano et al, 2000;Wu and McClay, 2007;Rahimi et al, 2009). We did not detect expression of any of these genes in blastula-stage embryos (Fig.…”

Section: Mesoderm Is Specified During Gastrulationmentioning

confidence: 99%

FGF signaling induces mesoderm in the hemichordate Saccoglossus kowalevskii

et al. 2013

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SUMMARYFGFs act in vertebrate mesoderm induction and also play key roles in early mesoderm formation in ascidians and amphioxus. However, in sea urchins initial characterizations of FGF function do not support a role in early mesoderm induction, making the ancestral roles of FGF signaling and mechanisms of mesoderm specification in deuterostomes unclear. In order to better characterize the evolution of mesoderm formation, we have examined the role of FGF signaling during mesoderm development in Saccoglossus kowalevskii, an experimentally tractable representative of hemichordates. We report the expression of an FGF ligand, fgf8/17/18, in ectoderm overlying sites of mesoderm specification within the archenteron endomesoderm. Embryological experiments demonstrate that mesoderm induction in the archenteron requires contact with ectoderm, and loss-of-function experiments indicate that both FGF ligand and receptor are necessary for mesoderm specification. fgf8/17/18 gain-of-function experiments establish that FGF8/17/18 is sufficient to induce mesoderm in adjacent endomesoderm. These experiments suggest that FGF signaling is necessary from the earliest stages of mesoderm specification and is required for all mesoderm development. Furthermore, they suggest that the archenteron is competent to form mesoderm or endoderm, and that FGF signaling from the ectoderm defines the location and amount of mesoderm. When considered in a comparative context, these data support a phylogenetically broad requirement for FGF8/17/18 signaling in mesoderm specification and suggest that FGF signaling played an ancestral role in deuterostome mesoderm formation. RESEARCH ARTICLEFGFs and hemichordate mesoderm from five pouches that evaginate from the archenteron in a process called enterocoely (Bateson, 1884); this trait is shared with echinoderms and amphioxus (Conklin, 1932) and is suggested to be primitive for deuterostomes (Remane, 1963;Valentine, 2004). These morphogenetic similarities with echinoderms and basal chordates, and close similarities with chordates in early body plan patterning, suggest that analysis of mesoderm specification in enteropneusts could help reconstruct ancestral deuterostome developmental mechanisms for mesoderm induction.To investigate a potentially conserved role of FGF signaling in deuterostome mesoderm induction, we examined the role of FGF signaling during early development of the direct-developing hemichordate Saccoglossus kowalevskii (Bateson, 1884;Bateson, 1886;Colwin and Colwin, 1953;Lowe et al., 2004;Gerhart et al., 2005;Röttinger and Lowe, 2012). We tested the function of the FGF ligand FGF8/17/18 and the FGF receptor FGFR-B (Rebscher et al., 2009) in hemichordate mesoderm formation, and our work demonstrates that FGF8/17/18 signals from ectoderm to the underlying archenteron to induce mesoderm. These findings suggest that an ortholog of the fgf8/17/18 subfamily was essential for mesoderm induction in the deuterostome common ancestor and have important implications for the evolution of mesoderm induct...

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Expression of somite segmentation genes in amphioxus: a clock without a wavefront?

Cited by 46 publications

References 56 publications

FGF4 and FGF8 comprise the wavefront activity that controls somitogenesis

FGF4 and FGF8 comprise the wavefront activity that controls somitogenesis

Amphioxus FGF signaling predicts the acquisition of vertebrate morphological traits

FGF signaling induces mesoderm in the hemichordate Saccoglossus kowalevskii

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