RESUMEN
Insects and other arthropods utilise external sensory structures for mechanosensory, olfactory, and gustatory reception. These sense organs have characteristic shapes related to their function, and in many cases are distributed in a fixed pattern so that they are identifiable individually. In Drosophila melanogaster, the identity of sense organs is regulated by specific combinations of transcription factors. In other arthropods, however, sense organ subtypes cannot be linked to the same code of gene expression. This raises the questions of how sense organ diversity has evolved and whether the principles underlying subtype identity in D. melanogaster are representative of other insects. Here, we provide evidence that such principles cannot be generalised, and suggest that sensory organ diversification followed the recruitment of sensory genes to distinct sensory organ specification mechanism. RESULTS: We analysed sense organ development in a nondipteran insect, the flour beetle Tribolium castaneum, by gene expression and RNA interference studies. We show that in contrast to D. melanogaster, T. castaneum sense organs cannot be categorised based on the expression or their requirement for individual or combinations of conserved sense organ transcription factors such as cut and pox neuro, or members of the Achaete-Scute (Tc ASH, Tc asense), Atonal (Tc atonal, Tc cato, Tc amos), and neurogenin families (Tc tap). Rather, our observations support an evolutionary scenario whereby these sensory genes are required for the specification of sense organ precursors and the development and differentiation of sensory cell types in diverse external sensilla which do not fall into specific morphological and functional classes. CONCLUSIONS: Based on our findings and past research, we present an evolutionary scenario suggesting that sense organ subtype identity has evolved by recruitment of a flexible sensory gene network to the different sense organ specification processes. A dominant role of these genes in subtype identity has evolved as a secondary effect of the function of these genes in individual or subsets of sense organs, probably modulated by positional cues.
Asunto(s)
Expresión Génica , Interferencia de ARN , Órganos de los Sentidos/crecimiento & desarrollo , Tribolium/crecimiento & desarrollo , Animales , Larva/genética , Larva/crecimiento & desarrollo , Tribolium/genéticaRESUMEN
Spiders are equipped with a large number of innervated cuticular specializations, which respond to various sensory stimuli. The physiological function of mechanosensory organs has been analysed in great detail in some model spider species (e.g. Cupiennius salei); however, much less is known about the distribution and function of chemosensory organs. Furthermore, our knowledge on how the sense organ pattern develops on the spider appendages is limited. Here we analyse the development of the pattern and distribution of six different external mechano- and chemosensory organs in all postembryonic stages and in adult male and female spiders of the species Parasteatoda tepidariorum. We show that except for small mechanosensory setae, external sense organs appear in fixed positions on the pedipalps and first walking legs, arranged in longitudinal rows along the proximal-distal axis or in invariable positions relative to morphological landmarks (joints, distal tarsal tip). A comparison to other Entelegynae spiders shows that these features are conserved. We hope that this study lays the foundation for future molecular analysis to address the question how this conserved pattern is generated.
Asunto(s)
Extremidades/crecimiento & desarrollo , Órganos de los Sentidos/crecimiento & desarrollo , Sensilos/anatomía & histología , Sensilos/crecimiento & desarrollo , Arañas/crecimiento & desarrollo , Animales , Extremidades/anatomía & histología , Femenino , Fémur/anatomía & histología , Fémur/crecimiento & desarrollo , Masculino , Metatarso/anatomía & histología , Metatarso/crecimiento & desarrollo , Microscopía Electrónica de Rastreo , Órganos de los Sentidos/anatomía & histología , Sensilos/ultraestructura , Arañas/anatomía & histología , Tibia/anatomía & histología , Tibia/crecimiento & desarrolloRESUMEN
Angelika Stollewerk is a Reader at Queen Mary University of London, where her lab uses a diverse range of species to study the evolution of the arthropod nervous system. Angelika spoke to us about social spiders, the future of evo-devo, and open peer review.
Asunto(s)
Evolución Biológica , Encéfalo/anatomía & histología , Biología Evolutiva/historia , Animales , Historia del Siglo XXI , Revisión de la Investigación por ParesRESUMEN
Arthropods have numerous sense organs, which are adapted to their habitat. While some sense organs are similar in structure and function in all arthropod groups, structural differences in functionally related sense organs have been described, as well as the absence of particular sense organ subtypes in individual arthropod groups. Here we address the question of how the diverse structures of arthropod sense organs have evolved by analysing the underlying molecular developmental processes in a crustacean, an arthropod group that has been neglected so far. We have investigated the development of four types of chemo- and mechanosensory sense organs in the branchiopod Daphnia magna (Cladocera) that either cannot be found in arthropods other than crustaceans or represent adaptations to an aquatic environment. The formation of the sensory organ precursors shows greater similarity to the arthropod taxa Chelicerata and Myriapoda than to the more closely related insects. All analysed sense organ types co-express the proneural genes ASH and atonal regardless of their structure and function. In contrast, in Drosophila melanogaster, ASH and atonal expression does not overlap and the genes confer different sense organ subtype identities. We performed experimental co-expression studies in D. melanogaster and found that the combinatorial expression of ato and ASH can change the external structure of sense organs. Our results indicate a central role for ASH and Atonal family members in the emergence of structural variations in arthropod sense organs.
Asunto(s)
Evolución Biológica , Daphnia/embriología , Daphnia/genética , Regulación del Desarrollo de la Expresión Génica , Neuronas/metabolismo , Órganos de los Sentidos/embriología , Órganos de los Sentidos/metabolismo , Animales , Drosophila melanogaster/genética , Drosophila melanogaster/ultraestructura , Embrión no Mamífero/metabolismo , Embrión no Mamífero/ultraestructura , Larva/ultraestructura , Órganos de los Sentidos/ultraestructura , Alas de Animales/metabolismo , Alas de Animales/ultraestructuraRESUMEN
BACKGROUND: The duplication of genes can occur through various mechanisms and is thought to make a major contribution to the evolutionary diversification of organisms. There is increasing evidence for a large-scale duplication of genes in some chelicerate lineages including two rounds of whole genome duplication (WGD) in horseshoe crabs. To investigate this further, we sequenced and analyzed the genome of the common house spider Parasteatoda tepidariorum. RESULTS: We found pervasive duplication of both coding and non-coding genes in this spider, including two clusters of Hox genes. Analysis of synteny conservation across the P. tepidariorum genome suggests that there has been an ancient WGD in spiders. Comparison with the genomes of other chelicerates, including that of the newly sequenced bark scorpion Centruroides sculpturatus, suggests that this event occurred in the common ancestor of spiders and scorpions, and is probably independent of the WGDs in horseshoe crabs. Furthermore, characterization of the sequence and expression of the Hox paralogs in P. tepidariorum suggests that many have been subject to neo-functionalization and/or sub-functionalization since their duplication. CONCLUSIONS: Our results reveal that spiders and scorpions are likely the descendants of a polyploid ancestor that lived more than 450 MYA. Given the extensive morphological diversity and ecological adaptations found among these animals, rivaling those of vertebrates, our study of the ancient WGD event in Arachnopulmonata provides a new comparative platform to explore common and divergent evolutionary outcomes of polyploidization events across eukaryotes.
Asunto(s)
Evolución Molecular , Duplicación de Gen , Genoma , Arañas/genética , Animales , Femenino , Masculino , SinteníaRESUMEN
Insects are ideally suited for gaining insight into the evolutionary developmental mechanisms that have led to adaptive changes of the nervous system since the specific structure of the nervous system can be directly linked to the neural stem cell (neuroblast) lineages, which in turn can be traced back to the last common ancestor of insects. The recent comparative analysis of the Drosophila melanogaster and Tribolium castaneum neuroblast maps revealed substantial differences in the expression profiles of neuroblasts. Here we show that despite the overall conservation of the dorso-ventral expression domains of muscle segment homeobox, intermediate neuroblasts defective and ventral nervous system defective, the expression of these genes relative to the neuroblasts in the respective domains has changed considerably during insect evolution. Furthermore, functional studies show evolutionary changes in the requirement of ventral nervous system defective in the formation of neuroblast 1-1 and the correct differentiation of its presumptive progeny, the pioneer neurons aCC and pCC. The inclusion of the expression data of the dorso-ventral genes into the recently established T. castaneum neuroblast map further increases the differences in the neuroblast expression profiles between D. melanogaster and T. castaneum. Despite these molecular variations, the Even-skipped positive pioneer neurons show an invariant arrangement, except for an additional Even-skipped positive cluster that we discovered in T. castaneum. Given the importance of these pioneer neurons in establishing the intersegmental nerves and the longitudinal tracts, which are part of the conserved axonal scaffold of arthropods, we discuss internal buffering mechanisms that might ensure that neuroblast lineages invariantly generate pioneer neurons over a wide range of molecular variations.
Asunto(s)
Evolución Biológica , Tipificación del Cuerpo/fisiología , Regulación del Desarrollo de la Expresión Génica/fisiología , Proteínas de Homeodominio/metabolismo , Sistema Nervioso/embriología , Neuronas/metabolismo , Tribolium/embriología , Animales , Tipificación del Cuerpo/genética , Clonación Molecular , Cartilla de ADN/genética , Proteínas de Drosophila/metabolismo , Regulación del Desarrollo de la Expresión Génica/genética , Hibridación in Situ , Células-Madre Neurales/metabolismo , Reacción en Cadena de la Polimerasa , Especificidad de la Especie , Factores de Transcripción/metabolismoRESUMEN
One of the major questions in evolutionary developmental neurobiology is how neuronal networks have been adapted to different morphologies and behaviour during evolution. Analyses of neurogenesis in representatives of all arthropod species have revealed evolutionary modifications of various developmental mechanisms. Among others, variations can be seen in mechanisms that are associated with changes in neural progenitor identity, which in turn determines the neuronal subtype of their progeny. Comparative analyses of the molecular processes that underlie the generation of neuronal identity might therefore uncover the steps of evolutionary changes that eventually resulted in modifications in neuronal networks. Here we address this question in the flour beetle Tribolium castaneum by analyzing and comparing the development and expression profile of neural stem cells (neuroblasts) to the published neuroblast map of the fruit fly Drosophila melanogaster. We show that substantial changes in the identity of neuroblasts have occurred during insect evolution. In almost all neuroblasts the relative positions in the ventral hemi-neuromeres are conserved; however, in over half of the neuroblasts the time of formation as well as the gene expression profile has changed. The neuroblast map presented here can be used for future comparative studies on individual neuroblast lineages in D. melanogaster and T. castaneum and additional markers and information on lineages can be added. Our data suggest that evolutionary changes in the expression profile of individual neuroblasts might have contributed to the evolution of neural diversity and subsequently to changes in neuronal networks in arthropod.
Asunto(s)
Drosophila melanogaster/genética , Regulación del Desarrollo de la Expresión Génica , Células-Madre Neurales/citología , Animales , Linaje de la Célula , Mapeo Cromosómico , Proteínas de Drosophila/genética , Proteínas de Drosophila/metabolismo , Drosophila melanogaster/embriología , Evolución Molecular , Perfilación de la Expresión Génica , Marcadores Genéticos/genética , Hibridación in Situ , Hibridación Fluorescente in Situ , Insectos , Red Nerviosa/fisiología , Sistema Nervioso/embriología , Neuronas/fisiología , Reacción en Cadena de la Polimerasa , Especificidad de la Especie , Factores de Tiempo , Tribolium/genéticaRESUMEN
Evolutionary developmental biology (evo-devo) has undergone dramatic transformations since its emergence as a distinct discipline. This paper aims to highlight the scope, power, and future promise of evo-devo to transform and unify diverse aspects of biology. We articulate key questions at the core of eleven biological disciplines-from Evolution, Development, Paleontology, and Neurobiology to Cellular and Molecular Biology, Quantitative Genetics, Human Diseases, Ecology, Agriculture and Science Education, and lastly, Evolutionary Developmental Biology itself-and discuss why evo-devo is uniquely situated to substantially improve our ability to find meaningful answers to these fundamental questions. We posit that the tools, concepts, and ways of thinking developed by evo-devo have profound potential to advance, integrate, and unify biological sciences as well as inform policy decisions and illuminate science education. We look to the next generation of evolutionary developmental biologists to help shape this process as we confront the scientific challenges of the 21st century.
Asunto(s)
Evolución Biológica , Biología Evolutiva , Genética , Animales , Biología Evolutiva/educación , Biología Evolutiva/tendencias , Redes Reguladoras de Genes , Genética/educación , Genética/tendencias , HumanosRESUMEN
Ten years ago we showed for the first time that Notch signalling is required in segmentation in spiders, indicating the existence of similar mechanisms in arthropod and vertebrate segmentation. However, conflicting results in various arthropod groups hampered our understanding of the ancestral function of Notch in arthropod segmentation. Here we fill a crucial data gap in arthropods and analyse segmentation in a crustacean embryo. We analyse the expression of homologues of the Drosophila and vertebrate segmentation genes and show that members of the Notch signalling pathway are expressed at the same time as the pair-rule genes. Furthermore, inactivation of Notch signalling results in irregular boundaries of the odd-skipped-like expression domains and affects the formation of segments. In severe cases embryos appear unsegmented. We suggest two scenarios for the function of Notch signalling in segmentation. The first scenario agrees with a segmentation clock involving Notch signalling, while the second scenario discusses an alternative mechanism of Notch function which is integrated into a hierarchical segmentation cascade.
Asunto(s)
Tipificación del Cuerpo , Daphnia/embriología , Daphnia/metabolismo , Receptores Notch/metabolismo , Transducción de Señal , Animales , Tipificación del Cuerpo/genética , Drosophila melanogaster/embriología , Embrión no Mamífero/metabolismo , Regulación del Desarrollo de la Expresión Génica , Modelos Biológicos , Receptores Notch/genética , Homología de Secuencia de Aminoácido , Transducción de Señal/genética , Análisis Espacio-TemporalRESUMEN
The genetic regulatory networks controlling major developmental processes seem to be conserved in bilaterians regardless of an independent or a common origin of the structures. This has been explained by the employment of a genetic toolkit that was repeatedly used during bilaterian evolution to build the various forms and body plans. However, it is not clear how genetic networks were incorporated into the formation of novel structures and how homologous genes can regulate the disparate morphological processes. Here we address this question by analysing the role of Notch signalling, which is part of the bilaterian toolkit, in neural stem cell evolution in arthropods. Within arthropods neural stem cells have evolved in the last common ancestor of insects and crustaceans (Tetraconata). We analyse here for the first time the role of Notch signalling in a crustacean, the branchiopod Daphnia magna, and show that it is required in neural stem cells for regulating the time of neural precursor production and for binary cell fate decisions in the ventral neuroectoderm. The function of Notch signalling has diverged in the ventral neuroectoderm of insects and crustaceans accompanied by changes in the morphogenetic processes. In the crustacean, Notch controlled mechanisms of neuroblast regulation have evolved that are surprisingly similar to vertebrates and thus present a remarkable case of parallel evolution. These new data on a representative of crustaceans complete the arthropod data set on Notch signalling in the nervous system and allow for reconstructing how the Notch signalling pathway has been co-opted from pre-existing structures to the development of the evolving neural stem cells in the Tetraconata ancestor.
Asunto(s)
Daphnia/embriología , Células-Madre Neurales/citología , Receptores Notch/metabolismo , Transducción de Señal , Animales , Daphnia/genética , Daphnia/metabolismo , Embrión no Mamífero/metabolismo , Evolución Molecular , Regulación del Desarrollo de la Expresión Génica , Datos de Secuencia Molecular , Células-Madre Neurales/metabolismo , Receptores Notch/genéticaRESUMEN
In insects and crustaceans, ventral midline cells are present that subdivide the CNS into bilateral symmetric halves. In both arthropod groups unpaired midline neurons and glial cells have been identified that contribute to the embryonic patterning mechanisms. In the fruitfly Drosophila melanogaster, for example, the midline cells are involved in neural cell fate specification along the dorso-ventral axis but also in axonal pathfinding and organisation of the axonal scaffold. Both in insects and malacostracan crustaceans, the bHLH-PAS transcription factor single-minded is the master regulator of ventral midline development and homology has been suggested for individual midline precursors in these groups. The conserved arrangement of the axonal scaffold as well as the regular pattern of neural precursors in all euarthropod groups raises the question whether the ventral midline system is conserved in this phylum. In the remaining euarthropod groups, the chelicerates and myriapods, a single-minded homologue has been identified in the spider Achaearanea tepidariorum (chelicerate), however, the gene is not expressed in the ventral midline but in the median area of the ventral neuroectoderm. Here we show that At-sim is not required for ventral midline development. Furthermore, we identify sim homologues in representatives of arthropods that have not yet been analysed: the myriapod Strigamia maritima and a representative of an outgroup to the euarthropods, the onychophoran Euperipatoides kanangrensis. We compare the expression patterns to the A. tepidariorum sim homologue expression and furthermore analyse the nature of the arthropod midline cells. Our data suggest that in arthropods unpaired midline precursors evolved from the bilateral median domain of the ventral neuroectoderm in the last common ancestor of Mandibulata (insects, crustaceans, myriapods). We hypothesize that sim was expressed in this domain and recruited to ventral midline development. Subsequently, sim function has evolved in parallel to the evolution of midline cell function in the individual Mandibulata lineages.
Asunto(s)
Artrópodos/embriología , Evolución Biológica , Animales , Artrópodos/citología , Artrópodos/genética , Linaje de la Célula , Embrión no Mamífero/citología , Femenino , Regulación del Desarrollo de la Expresión GénicaRESUMEN
One of the controversial debates on euarthropod relationships centers on the question as to whether insects, crustaceans, and myriapods (Mandibulata) share a common ancestor or whether myriapods group with the chelicerates (Myriochelata). The debate was stimulated recently by studies in chelicerates and myriapods that show that neural precursor groups (NPGs) segregate from the neuroectoderm generating the nervous system, whereas in insects and crustaceans the nervous tissue is produced by stem cells. Do the shared neural characters of myriapods and chelicerates represent derived characters that support the Myriochelata grouping? Or do they rather reflect the ancestral pattern? Analyses of neurogenesis in a group closely related to euarthropods, the onychophorans, show that, similar to insects and crustaceans, single neural precursors are formed in the neuroectoderm, potentially supporting the Myriochelata hypothesis. Here we show that the nature and the selection of onychophoran neural precursors are distinct from euarthropods. The onychophoran nervous system is generated by the massive irregular segregation of single neural precursors, contrasting with the limited number and stereotyped arrangement of NPGs/stem cells in euarthropods. Furthermore, neural genes do not show the spatiotemporal pattern that sets up the precise position of neural precursors as in euarthropods. We conclude that neurogenesis in onychophorans largely does not reflect the ancestral pattern of euarthropod neurogenesis, but shows a mixture of derived characters and ancestral characters that have been modified in the euarthropod lineage. Based on these data and additional evidence, we suggest an evolutionary sequence of arthropod neurogenesis that is in line with the Mandibulata hypothesis.
Asunto(s)
Artrópodos/genética , Perfilación de la Expresión Génica , Regulación del Desarrollo de la Expresión Génica , Sistema Nervioso/metabolismo , Secuencia de Aminoácidos , Animales , Artrópodos/clasificación , Artrópodos/embriología , Embrión no Mamífero/citología , Embrión no Mamífero/embriología , Embrión no Mamífero/metabolismo , Evolución Molecular , Biblioteca de Genes , Variación Genética , Microscopía Confocal , Datos de Secuencia Molecular , Sistema Nervioso/citología , Sistema Nervioso/embriología , Neurogénesis , Filogenia , Análisis de Secuencia de ADN , Homología de Secuencia de Aminoácido , Especificidad de la EspecieRESUMEN
Netrins are well known for their function as long-range chemotropic guidance cues, in particular in the ventral midline of vertebrates and invertebrates. Over the past years, publications are accumulating that support an additional short-range function for Netrins in diverse developmental processes such as axonal pathfinding and cell adhesion. We describe here the formation of the axonal scaffold in the spiders Cupiennius salei and Achaearanea tepidariorum and show that axonal tract formation seems to follow the same sequence as in insects and crustaceans in both species. First, segmental neuropiles are established which then become connected by the longitudinal fascicles. Interestingly, the commissures are established at the same time as the longitudinal tracts despite the large gap between the corresponding hemi-neuromeres which results from the lateral movement of the germband halves during spider embryogenesis. We show that Netrin has a conserved function in the ventral midline in commissural axon guidance. This function is retained by an adaptation of the expression pattern to the specific morphology of the spider embryo. Furthermore, we demonstrate a novel function of netrin in the formation of glial sheath cells that has an impact on neural precursor differentiation. Loss of Netrin function leads to the absence of glial sheath cells which in turn results in premature segregation of neural precursors and overexpression of the early motor- and interneuronal marker islet. We suggest that Netrin is required in the differentiated sheath cells for establishing and maintaining the interaction between NPGs and sheath cells. This short-range adhesive interaction ensures that the neural precursors maintain their epithelial character and remain attached to the NPGs. Both the conserved and novel functions of Netrin seem to be required for the proper formation of the axonal scaffold.
Asunto(s)
Axones/fisiología , Proteínas del Tejido Nervioso/fisiología , Neuroglía/fisiología , Arañas/embriología , Animales , Comunicación Celular , Diferenciación Celular , Femenino , Morfogénesis , Proteínas del Tejido Nervioso/análisis , Células-Madre Neurales/citologíaRESUMEN
Within euarthropods, the morphological and molecular mechanisms of early nervous system development have been analysed in insects and several representatives of chelicerates and myriapods, while data on crustaceans are fragmentary. Neural stem cells (neuroblasts) generate the nervous system in insects and in higher crustaceans (malacostracans); in the remaining euarthropod groups, the chelicerates (e.g. spiders) and myriapods (e.g. millipedes), neuroblasts are missing. In the latter taxa, groups of neural precursors segregate from the neuroectoderm and directly differentiate into neurons and glial cells. In all euarthropod groups, achaete-scute homologues are required for neuroblast/neural precursor group formation. In the insects Drosophila melanogaster and Tribolium castaneum achaete-scute homologues are initially expressed in clusters of cells (proneural clusters) in the neuroepithelium but expression becomes restricted to the future neuroblast. Subsequently genes such as snail and prospero are expressed in the neuroblasts which are required for asymmetric division and differentiation. In contrast to insects, malacostracan neuroblasts do not segregate into the embryo but remain in the outer neuroepithelium, similar to vertebrate neural stem cells. It has been suggested that neuroblasts are present in another crustacean group, the branchiopods, and that they also remain in the neuroepithelium. This raises the questions how the molecular mechanisms of neuroblast selection have been modified during crustacean and insect evolution and if the segregation or the maintenance of neuroblasts in the neuroepithelium represents the ancestral state. Here we take advantage of the recently published Daphnia pulex (branchiopod) genome and identify genes in Daphnia magna that are known to be required for the selection and asymmetric division of neuroblasts in the fruit fly D. melanogaster. We unambiguously identify neuroblasts in D. magna by molecular marker gene expression and division pattern. We show for the first time that branchiopod neuroblasts divide in the same pattern as insect and malacostracan neuroblasts. Furthermore, in contrast to D. melanogaster, neuroblasts are not selected from proneural clusters in the branchiopod. Snail rather than ASH is the first gene to be expressed in the nascent neuroblasts suggesting that ASH is not required for the selection of neuroblasts as in D. melanogaster. The prolonged expression of ASH in D. magna furthermore suggests that it is involved in the maintenance of the neuroblasts in the neuroepithelium. Based on these and additional data from various representatives of arthropods we conclude that the selection of neural precursors from proneural clusters as well as the segregation of neural precursors represents the ancestral state of neurogenesis in arthropods. We discuss that the derived characters of malacostracans and branchiopods - the absence of neuroblast segregation and proneural clusters - might be used to support or reject the possible groupings of paraphyletic crustaceans.
Asunto(s)
Daphnia/genética , Regulación del Desarrollo de la Expresión Génica , Neurogénesis/genética , Neuronas/citología , Animales , Diferenciación Celular , Cladóceros/genética , Daphnia/embriología , Embrión no Mamífero/metabolismo , Insectos/genética , Células-Madre Neurales/citología , FilogeniaRESUMEN
Arthropods are common in marine, freshwater, terrestrial, and even aerial environments. The arthropod nervous systems must be adjusted to the highly diverse behaviour and requirements of the individual arthropod species. This raises the question of how the underlying patterning mechanisms have changed during arthropod evolution to produce the characteristic axonal scaffold on the one hand and allow for variations in neuronal networks on the other hand. Here we show that the overall number of the neural precursor groups/neuroblasts as well as their spatial arrangement in rows and columns is similar in all four arthropod groups indicating a common origin of this pattern. Furthermore, we demonstrate differences in the expression pattern of the columnar gene muscle segment homeobox and both differences in the expression and regulation of the neural subtype specific genes even-skipped and islet. This variation may underlie the evolutionary variations in neural identity in the individual arthropod groups. Furthermore, we discuss to what extent the stereotyped pattern of neural precursors is required for the conserved axonal scaffold and thus might have been constrained along with the underlying patterning mechanisms.
Asunto(s)
Artrópodos/genética , Regulación del Desarrollo de la Expresión Génica , Proteínas de Homeodominio/genética , Arañas/genética , Animales , Artrópodos/clasificación , Artrópodos/embriología , Tipificación del Cuerpo/genética , Clonación Molecular , ADN Complementario/química , ADN Complementario/genética , Embrión no Mamífero/embriología , Embrión no Mamífero/metabolismo , Evolución Molecular , Femenino , Variación Genética , Proteínas de Homeodominio/metabolismo , Inmunohistoquímica , Hibridación in Situ , Masculino , Músculos/embriología , Músculos/inervación , Músculos/metabolismo , Sistema Nervioso/embriología , Sistema Nervioso/metabolismo , Neurogénesis/genética , Interferencia de ARN , Reacción en Cadena de la Polimerasa de Transcriptasa Inversa , Análisis de Secuencia de ADN , Especificidad de la Especie , Arañas/embriologíaRESUMEN
BACKGROUND: An increasing number of publications demonstrate conservation of function of cis-regulatory elements without sequence similarity. In invertebrates such functional conservation has only been shown for closely related species. Here we demonstrate the existence of an ancient arthropod regulatory element that functions during the selection of neural precursors. The activity of genes of the achaete-scute (ac-sc) family endows cells with neural potential. An essential, conserved characteristic of proneural genes is their ability to restrict their own activity to single or a small number of progenitor cells from their initially broad domains of expression. This is achieved through a process called lateral inhibition. A regulatory element, the sensory organ precursor enhancer (SOPE), is required for this process. First identified in Drosophila, the SOPE contains discrete binding sites for four regulatory factors. The SOPE of the Drosophila asense gene is situated in the 5' UTR. RESULTS: Through a manual comparison of consensus binding site sequences we have been able to identify a SOPE in UTR sequences of asense-like genes in species belonging to all four arthropod groups (Crustacea, Myriapoda, Chelicerata and Insecta). The SOPEs of the spider Cupiennius salei and the insect Tribolium castaneum are shown to be functional in transgenic Drosophila. This would place the origin of this regulatory sequence as far back as the last common ancestor of the Arthropoda, that is, in the Cambrian, 550 million years ago. CONCLUSIONS: The SOPE is not detectable by inter-specific sequence comparison, raising the possibility that other ancient regulatory modules in invertebrates might have escaped detection.
Asunto(s)
Region del Complejo Génico Achaete-Scute/genética , Artrópodos/genética , Factores de Transcripción con Motivo Hélice-Asa-Hélice Básico/genética , Evolución Biológica , Regulación del Desarrollo de la Expresión Génica/genética , Sistema Nervioso/crecimiento & desarrollo , Elementos Reguladores de la Transcripción/genética , Secuencia de Aminoácidos , Animales , Artrópodos/fisiología , Secuencia de Bases , Sitios de Unión/genética , Secuencia Conservada/genética , Duplicación de Gen/genética , Regulación del Desarrollo de la Expresión Génica/fisiología , Datos de Secuencia Molecular , Sistema Nervioso/metabolismo , Placa Neural/metabolismo , Filogenia , Alineación de Secuencia , Especificidad de la EspecieRESUMEN
In the spider Cupiennius salei the mechanosensory organs of the legs are generated from epithelial sensory precursor groups which are specified by elevated levels of the achaete-scute homologues CsASH1 and CsASH2. Neural precursors delaminate from the groups and occupy positions basal and proximal to the accessory cells which remain in the epithelium. Here we analyse the role of Notch signalling and numb function in the development of the mechanosensory organs of the spider. We show that Notch signalling is required for several processes: the selection of the sensory precursor groups, the maintenance of undifferentiated sensory precursors, the binary cell fate decision between accessory and neural fate and the differentiation of sensory neurons. Our data suggest that Numb antagonises Notch signalling in the neural precursors, which results in activation of the neural cell fate determinant Prospero and delamination of the neural precursors from the epithelium. Prospero is expressed de novo in sensory neural precursors and we assume that the expression of the gene is regulated by the Notch to Numb ratio within the sensory precursors. Interestingly, the spider numb RNAi phenotype resembles the numb/numblike loss of function phenotypes in the mammalian nervous system, indicating that the interaction between Notch signalling and Numb might play a similar role in both systems.
Asunto(s)
Péptidos y Proteínas de Señalización Intracelular/fisiología , Proteínas del Tejido Nervioso/fisiología , Neurogénesis , Receptores Notch/fisiología , Células Receptoras Sensoriales/citología , Transducción de Señal , Animales , Diferenciación Celular , Mecanotransducción Celular , Arañas , Células Madre/citologíaRESUMEN
We describe here for the first time the development of mechanosensory organs in a chelicerate, the spider Cupiennius salei. It has been shown previously that the number of external sense organs increases with each moult. While stage 1 larvae do not have any external sensory structures, stage 2 larvae show a stereotyped pattern of touch sensitive 'tactile hairs' on their legs. We show that these mechanosensory organs develop during embryogenesis. In contrast to insects, groups of sensory precursors are recruited from the leg epithelium, rather than single sensory organ progenitors. The groups increase by proliferation, and neural cells delaminate from the cluster, which migrate away to occupy a position proximal to the accessory cells of the sense organ. In addition, we describe the development of putative internal sense organs, which do not differentiate until larval stage 2. We show by RNA interference that, similar to Drosophila, proneural genes are responsible for the formation and subtype identity of sensory organs. Furthermore, we demonstrate an additional function for proneural genes in the coordinated invagination and migration of neural cells during sensory organ formation in the spider.