Insights into spawning behavior and development of the european amphioxus (<i>Branchiostoma lanceolatum</i>)

Fuentès, Michaël; Benito, Eva; Bertrand, Stéphanie; Paris, Mathilde; Mignardot, Aurelie; Godoy, Laura; Jiménez‐Delgado, Senda; Oliveri, Diana; Candiani, Simona; Hirsinger, Estelle; D’Aniello, Salvatore; Pascual-Anaya, Juan; Maeso, Ignacio; Pestarino, Mario; Vernier, Philippe; Nicolas, Jean-François; Schubert, Michael; Laudet, Vincent; Genevière, Anne Marie; Albalat, Ricard; Garcia‐Fernàndez, Jordi; Holland, Nicholas D.; Escrivà, Héctor

doi:10.1002/jez.b.21179

Cited by 106 publications

(142 citation statements)

References 17 publications

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“…Recently, however, progress has been made in the induction of spawning in captive animals, which should greatly facilitate the use of amphioxus as an experimental system (28). It will be fascinating to determine whether the ventral mesoderm of amphioxus larvae has any outgrowth potential, and, if so, to investigate the temporal window of this competence, similar to previous experiments, which show that an exogenous source of FGF applied to the chick flank can induce ectopic limb formation (13,14).…”

Section: Discussionmentioning

confidence: 73%

Tbx4/5 gene duplication and the origin of vertebrate paired appendages

Minguillón

Gibson‐Brown

Logan

2009

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

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Paired fins/limbs are one of the most successful vertebrate innovations, since they are used for numerous fundamental activities, including locomotion, feeding, and breeding. Gene duplication events generate new genes with the potential to acquire novel functions, and two rounds of genome duplication took place during vertebrate evolution. The cephalochordate amphioxus diverged from other chordates before these events and is widely used to deduce the functions of ancestral genes, present in single copy in amphioxus, compared to the functions of their duplicated vertebrate orthologues. The T-box genes Tbx5 and Tbx4 encode two closely related transcription factors that are the earliest factors required to initiate forelimb and hind limb outgrowth, respectively. Since the genetic components proposed to be responsible for acquiring a trait during evolution are likely to be involved in the formation of that same trait in living organisms, we investigated whether the duplication of an ancestral, single Tbx4/5 gene to give rise to distinct Tbx4 and Tbx5 genes has been instrumental in the acquisition of limbs during vertebrate evolution. We analyzed whether the amphioxus Tbx4/5 gene is able to initiate limb outgrowth, and assayed the amphioxus locus for the presence of limb-forming regulatory regions. We show that AmphiTbx4/5 is able to initiate limb outgrowth and, in contrast, that the genomic locus lacks the regulatory modules required for expression that would result in limb formation. We propose that changes at the level of Tbx5 and Tbx4 expression, rather than the generation of novel protein function, have been necessary for the acquisition of paired appendages during vertebrate evolution.S ince Ohno's visionary hypothesis concerning the origin of vertebrate innovations by genome duplication (1), numerous reports have been published supporting this concept (reviewed in ref.2). The cephalochordate amphioxus, a limbless extant invertebrate relative of the vertebrates (3), has been extensively used to study the ancestral functions of genes, present in single copy in amphioxus, that have been duplicated in the vertebrate lineage. Amphioxus exhibits many basal chordate characteristics, including the presence of a dorsal nerve cord, a notochord, and segmented paraxial mesoderm, but lacks many vertebrate characteristics such as migratory neural crest cells, a cranium, or an endoskeleton (4). We sought to investigate the origin of one of the most successful vertebrate innovations, paired appendages, which include the pectoral and pelvic fins of fish and their derived homologues, the forelimbs and hind limbs of tetrapods.The T-box genes Tbx4 and Tbx5 are paralogous genes that arose by duplication of a single, ancestral Tbx4/5 gene. Extant amphioxus possesses a single Tbx4/5 gene (AmphiTbx4/5) (5) and lacks paired appendages, whereas all jawed vertebrates with two pairs of paired appendages have distinct, postduplication Tbx4 and Tbx5 genes. In vertebrates, Tbx5 is expressed in the lateral plate mesoderm (LPM) of the presump...

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Section: Discussionmentioning

confidence: 73%

Tbx4/5 gene duplication and the origin of vertebrate paired appendages

Minguillón

Gibson‐Brown

Logan

2009

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

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“…Gametes were obtained as previously described (34), and embryos were fixed and processed for whole-mount in situ hybridization as described (35). The accession numbers of the sequences used for probe synthesis are provided in SI Materials and Methods.…”

Section: Methodsmentioning

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.

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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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“…lanceolatum adult animals were collected in Argeles-sur-Mer (France) and preserved in the lab in a day/night cycle of 14h/10h until spawning, which was induced by a shift in temperature (Fuentes et al, 2007). Staging of all collected embryos was performed according to Hirakow and Kajita (1994).…”

Section: Animal Collectionmentioning

confidence: 99%

The opsin repertoire of the European lancelet: a window into light detection in a basal chordate

Pantzartzi

Pergner²,

Kozmiková³

et al. 2017

Int. J. Dev. Biol.

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Light detection in animals is predominantly based on the photopigment composed of a protein moiety, the opsin, and the chromophore retinal. Animal opsins originated very early in metazoan evolution from within the G-Protein Coupled Receptor (GPCR) gene superfamily and diversified into several distinct branches prior to the cnidarian-bilaterian split. The origin of opsin diversity, opsin classification and interfamily relationships have been the matter of long-standing debate. Comparative studies of opsins from various Metazoa provide key insight into the evolutionary history of opsins and the visual perception in animals. Here, we have analyzed the genome assembly of the cephalochordate Branchiostoma lanceolatum, applying BLAST, gene prediction tools and manual curation in order to predict de novo its complete opsin repertoire. We investigated the structure of predicted opsin genes, encoded proteins, their phylogenetic placement, and expression. We identified a total of 22 opsin genes in B. lanceolatum, of which 21 are expressed and the remaining one appears to be a pseudogene. According to our phylogenetic analysis, representatives from the three major opsin groups, namely C-type, the R-type and the Group 4, can be identified in B. lanceolatum. Most of the B. lanceolatum opsins exhibit a stage-specific, but not a tissue-specific, expression pattern. The large number of opsins detected in B. lanceolatum, the observed similarities and differences in terms of sequence characteristics and expression patterns lead us to conclude that there may be a fine tuning in opsin utilization in order to facilitate visually-guided behavior of European amphioxus under various environmental settings.

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Insights into spawning behavior and development of the european amphioxus (Branchiostoma lanceolatum)

Cited by 106 publications

References 17 publications

Tbx4/5 gene duplication and the origin of vertebrate paired appendages

Tbx4/5 gene duplication and the origin of vertebrate paired appendages

Amphioxus FGF signaling predicts the acquisition of vertebrate morphological traits

The opsin repertoire of the European lancelet: a window into light detection in a basal chordate

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