Development Genes and Evolution

Vlaskalin, Tatjana; Wong, Christine J.; Tsilfidis, Catherine

doi: 10.1007/s00427-004-0417-1pmid: 15322877

Many of the genes involved in the initial development of the limb in higher vertebrates are also expressed during regeneration of the limb in urodeles such as Notophthalmus viridescens. These similarities have led researchers to conclude that the regeneration process is a recapitulation of development, and that patterning of the regenerate mimics pattern formation in development. However, the developing limb and the regenerating limb do not look similar. In developing urodele forelimbs, digits appear sequentially as outgrowths from the limb palette. In regeneration, all the digits appear at once. In this work, we address the issue of whether regeneration and development are similar by examining growth and apoptosis patterns. In contrast to higher vertebrates, forelimb development in the newt, N. viridescens, does not use interdigital apoptosis as the method of digit separation. During adult forelimb regeneration, apoptosis seems to play an important role in wound healing and again during cartilage to bone turnover in the advanced digits and radius/ulna. However, similar to forelimb development, demarcation of the digits in adult forelimb regeneration does not involve interdigital apoptosis. Outgrowth, rather than regression of the interdigital mesenchyme, leads to the individualization of forelimb digits in both newt development and regeneration.

Stafford, D.; Hornbruch, A.; Mueller, P. R.; Prince, V. E.

doi: 10.1007/s00427-004-0420-6pmid: 15322880

Retinoic acid (RA) signaling plays critical roles in the regionalization of the central nervous system and mesoderm of all vertebrates that have been examined. However, to date, a role for RA in pancreas and liver development has only been demonstrated for the teleost zebrafish. Here, we demonstrate that RA signaling is required for development of the pancreas but not the liver in the amphibian Xenopus laevis and the avian quail. We disrupted RA signaling in Xenopus tadpoles, using both a pharmacological and a dominant-negative strategy. RA-deficient quail embryos were obtained from hens with a dietary deficiency in vitamin A. In both species we found that pancreas development was dependent on RA signaling. Furthermore, treatment of Xenopus tadpoles with exogenous RA led to an expansion of the pancreatic field. By contrast, liver development was not perturbed by manipulation of RA signaling. Taken together with our previous finding that RA signaling is necessary and sufficient for zebrafish pancreas development, these data support the hypothesis that a critical role for RA signaling in pancreas development is a conserved feature of the vertebrates.

Orgogozo, Virginie; Schweisguth, François

doi: 10.1007/s00427-004-0422-4pmid: 15293048

A key challenge in evolutionary biology is to identify developmental events responsible for morphological changes. To determine the cellular basis that underlies changes in the larval peripheral nervous system (PNS) of flies, we first described the PNS pattern of the abdominal segments A1–A7 in late embryos of several fly species using antibody staining. In contrast to the many variations reported previously for the adult PNS pattern, we found that the larval PNS pattern has remained very stable during evolution. Indeed, our observation that most of the analysed Drosophilinae species exhibit exactly the same pattern as Drosophila melanogaster reveals that the pattern observed in D. melanogaster embryos has remained constant for at least 40 million years. Furthermore, we observed that the PNS pattern in more distantly related flies (Calliphoridae and Phoridae) is only slightly different from the one in D. melanogaster. A single difference relative to D. melanogaster was identified in the PNS pattern of the Drosophilinae fly D. busckii, the absence of a specific external sensory organ. Our analysis of sensory organ development in D. busckii suggests that this specific loss resulted from a transformation in cell lineage, from a multidendritic-neuron-external-sensory-organ lineage to a multidendritic-neuron-solo lineage.

Apitz, Holger; Kambacheld, Melanie; Höhne, Martin; Ramos, Ricardo G. P.; Straube, Angela; Fischbach, Karl-Friedrich

doi: 10.1007/s00427-004-0423-3pmid: 15278452

Roughest (Rst) is a cell adhesion molecule of the immunoglobulin superfamily with pleiotropic functions during the development of Drosophila melanogaster. It has been shown to be involved in cell sorting before apoptosis in the developing compound eye, in fusion processes of embryonic muscle development and in axonal pathfinding. In accordance with its multiple functions, the rst gene shows a dynamic expression pattern throughout the development of Drosophila. In order to understand the transcriptional regulation of rst expression we have identified rst cis regulatory sequences in an enhancer detection screen. By dissection of the identified rst cis regulatory sequences we identified several distinct rst regulatory modules. Among others these include elements for expression in interommatidial cells of the pupal eye disc at a time when apoptotic decisions are made in these cells and elements for expression in the embryonic mesoderm. The expression of rst in the embryonic mesoderm is regulated by at least two separate modules.

Utsumi, Nanami; Shimojima, Yasuhiro; Saiga, Hidetoshi

doi: 10.1007/s00427-004-0425-1pmid: 15338306

The ascidian larva is often regarded as an organism close to the ancestral form of chordates, while it is generally accepted that the Spemann’s organizer is absent from ascidian embryos. Not is one of the genes expressed in the organizer to execute functions in vertebrate embryos. To address the extent of conservation of Not gene expression among ascidians and vertebrates, we examined the structure and developmental expression of Not of the two distantly related ascidian species, Halocynthia and Ciona. Putative ascidian Not proteins were noted by the absence of one of the two motifs conserved among Not proteins of sea urchin and vertebrates. Analysis by in situ hybridization revealed that Not gene expression of ascidians could be categorized into three types: expression likely to be conserved between ascidians and vertebrates, that probably unique to ascidians, and that specific to ascidian species. Expression of ascidian Not in the posterior end of the tail as well as the notochord and a small part of the anterior neural tube at the tailbud stage is reminiscent of the expression of the vertebrate counterparts in the tailbud, which is regarded as a continuation of the organizer and the pineal gland, respectively. The expression of Not in the epidermis precursors during cleavage stage may be unique to ascidians. In the light of the present findings, evolutionary aspects of Not genes are discussed.

Freitas, Renata; Cohn, Martin J.

doi: 10.1007/s00427-004-0426-0pmid: 15300436

The Eph family is the largest known group of structurally related receptor tyrosine kinases (RTKs). Each Eph receptor has a specific Ephrin ligand, and these function to define spatial boundaries during development. Analyses of EphA4 in mouse, chick, frog and zebrafish embryos have implicated this gene in a number of developmental processes, including maintenance of segmental boundaries, axon guidance, limb development, neural crest migration and patterning of the ear. In order to determine which components of EphA4 function may be primitive for gnathostomes, we cloned EphA4 from the lesser spotted catshark (Scyliorhinus canicula) and examined its expression pattern during shark embryonic development. Consistent with the patterns reported for bony fish and tetrapods, we observed segmental expression of EphA4 in the developing hindbrain and later in the pharyngeal arches of shark embryos. EphA4 was also detected during sensory organogenesis, in the developing ear, eye, nasal pits and lateral line. A dynamic pattern of EphA4 expression occurs during shark fin development, suggesting an early role in outgrowth and patterning of the fin buds and a later role in tissue differentiation. We also observed several novel domains of EphA4 expression that have not been reported in other vertebrates, including external gill buds, dermal denticles, median fins and claspers. While some of these domains may reflect co-option of EphA4 expression to novel sites for development of shark-specific characters, others are more likely to be ancestral patterns of expression that were lost in other vertebrate lineages.