RESUMEN
During the course of evolution, animals have become increasingly complex by the addition of novel cell types and regulatory mechanisms. A prime example is represented by the lateral neural border, known as the neural plate border in vertebrates, a region of the developing ectoderm where presumptive neural and non-neural tissue meet. This region has been intensively studied as the source of two important embryonic cell types unique to vertebrates-the neural crest and the ectodermal placodes-which contribute to diverse differentiated cell types including the peripheral nervous system, pigment cells, bone, and cartilage. How did these multipotent progenitors originate in animal evolution? What triggered the elaboration of the border during the course of chordate evolution? How is the lateral neural border patterned in various bilaterians and what is its fate? Here, we review and compare the development and fate of the lateral neural border in vertebrates and invertebrates and we speculate about its evolutionary origin. Taken together, the data suggest that the lateral neural border existed in bilaterian ancestors prior to the origin of vertebrates and became a developmental source of exquisite evolutionary change that frequently enabled the acquisition of new cell types.
Asunto(s)
Evolución Biológica , Invertebrados/embriología , Cresta Neural/citología , Vertebrados/embriología , Animales , Proteínas Morfogenéticas Óseas/metabolismo , Cordados no Vertebrados/embriología , Ectodermo/citología , Embrión no Mamífero/citología , Cresta Neural/metabolismo , Placa Neural/metabolismoRESUMEN
Many colonial marine animals care for embryos by brooding them on or in their bodies. For brooding to occur, features of the animals must allow it, and brooding must be at least as advantageous as releasing gametes or zygotes. Shared features of diverse colonial brooders are suspension feeding and a body composed of small modules that are indefinitely repeated and can function semi-autonomously, such as polyps or zooids. Suspension feeding permits capture of sperm for fertilization of ova that are retained by the parent. Distribution of broods among numerous small polyps, zooids, or other small modules facilitates supply of oxygen to embryos that are retained and protected by the parent. Brooding increases survival of offspring, controls dispersal, and can provide other developmental advantages. Colonial ascidians, pterobranch hemichordates, and entoprocts brood; most bryozoans and many colonial cnidarians brood. An unanswered question is why so many colonial anthozoans do not brood. Sponges share with colonies capacities for capturing sperm and separating numerous retained embryos yet many do not brood. Hypotheses for nonbrooding by colonies and sponges necessarily must apply to particular taxa. Few have been tested.
Asunto(s)
Invertebrados/embriología , Invertebrados/fisiología , Animales , Organismos Acuáticos/fisiología , Conducta Alimentaria , Invertebrados/anatomía & histología , Reproducción/fisiologíaRESUMEN
Immunoblotting analyses employing phospho-specific antibodies can help elucidate potential roles played by protein kinases as oocytes age and lose their ability to undergo normal fertilization. This chapter updates a previously published protocol for conducting immunoblotting analyses of oocyte maturation in marine nemertean worms by adding general methods for obtaining adult worms and for handling their gametes in experiments assessing oocyte aging.
Asunto(s)
Immunoblotting/métodos , Invertebrados/citología , Oocitos/citología , Animales , Senescencia Celular , Electroforesis/métodos , Femenino , Invertebrados/embriología , OogénesisRESUMEN
The development of multicellular organisms involves three main events: differentiation, growth, and morphogenesis. These processes need to be coordinated for a correct developmental program to work. Mechanisms of cell segregation and the formation of boundaries during development play essential roles in this coordination, allowing the generation and maintenance of distinct regions in an organism. These mechanisms are also at work in the nervous system. The process of regionalization involves first the patterning of the developing organism through gradients and the expression of transcription factors in specific regions. Once different tissues have been induced, segregation mechanisms may operate to avoid cell mixing between different compartments. Three mechanisms have been proposed to achieve segregation: (1) differential affinity, which mainly involves the expression of distinct pools of adhesion molecules such as members of the cadherin superfamily; (2) contact inhibition, which is largely mediated by Eph-ephrin signaling; and (3) cortical tension, which involves the actomyosin cytoskeleton. In many instances, these mechanisms collaborate in cell segregation. In the last three decades, there have been several advances in our understanding of how cell segregation and boundaries participate in the development of the nervous system. Interestingly, as in other aspects of development, the molecular players are remarkably similar between vertebrates and invertebrates. Here we summarize the main concepts of cell segregation and boundary formation, focusing on the nervous system and highlighting the similarities between vertebrate and invertebrate model organisms.
Asunto(s)
Efrinas , Sistema Nervioso/embriología , Organogénesis , Actomiosina , Animales , Invertebrados/embriología , Vertebrados/embriologíaRESUMEN
The organization and development of the nervous system are traditionally used for phylogenetic analysis and may be useful for clarification of evolution and phylogeny of some poor studied groups. One of these groups is brachiopods: most data on their nervous system organization were obtained in 19th century. In this research, antibody staining and confocal laser scanning microscopy were used to study the nervous system of early ontogenetic stages of the brachiopod Novocrania anomala. Although N. anomala adults are thought to lack a supraenteric ganglion, a large supraenteric ganglion exists in N. anomala juveniles with either a trocholophe or a schizolophe. During ontogenesis, the supraenteric ganglion in the juvenile changes its shape: the commissure between the two lobes of the ganglion extends. This commissure possibly gives rise to the main brachial nerve in adults. The supraenteric ganglion gives rise to the cross (transversal) nerves that extend to the accessory brachial nerve, which gives rise to the tentacular nerves. In juveniles with a trocholophe, the accessory brachial nerve gives rise to the frontal and intertentacular nerves of tentacles that form a single row. When the trocholophe transforms into the schizolophe, the second row of tentacles appears and the innervation of the tentacles changes. The intertentacular nerves disappear and the second accessory nerve forms and gives rise to the laterofrontal tentacular nerves of the inner and outer tentacles and to the abfrontal nerves of the inner tentacles. The so-called subenteric ganglion, which was described as a ganglion in N. anomala adults, is represented by a large circumvisceral nerve in N. anomala juveniles.The results suggest that 'phoronid-like' non-specialized tentacles may be regarded as the ancestral type of tentacles for brachiopods and probably for all lophophorates. The presence of intertentacular nerves is the ancestral feature of all lophophorates. The transformation of the juvenile supraenteric ganglion into the main brachial nerve of N. anomala adults suggests that research is needed on the development and organization of the supraenteric ganglion and the main brachial nerve in other brachiopods, whose adults have a prominent supraenteric ganglion.
Asunto(s)
Plexo Braquial/embriología , Invertebrados/anatomía & histología , Invertebrados/embriología , Tejido Nervioso/embriología , Fenómenos Fisiológicos del Sistema Nervioso , Animales , Evolución Biológica , Invertebrados/fisiología , Fenómenos Fisiológicos MusculoesqueléticosRESUMEN
The Sp-family genes encode important transcription factors in animal development. Here we investigate the embryonic expression patterns of the complete set of Sp-genes in the velvet worm Euperipatoides kanangrensis (Onychophora), with a special focus on the Sp6-9 ortholog. In arthropods, Sp6-9, the ortholog of the Drosophila melanogaster D-Sp1 gene plays a conserved role in appendage development. Our data show that the expression of Sp6-9 during the development of the velvet worm is conserved, suggesting that the key function of the Sp6-9 gene dates back to at least the last common ancestor of arthropods and onychophorans and thus likely the last common ancestor of Panarthropoda.
Asunto(s)
Tipificación del Cuerpo/genética , Invertebrados/embriología , Invertebrados/genética , Factores de Transcripción Sp/genética , Factores de Transcripción Sp/metabolismo , Secuencia de Aminoácidos , Animales , Embrión no Mamífero/metabolismo , Desarrollo Embrionario/genética , Regulación del Desarrollo de la Expresión Génica , Filogenia , Dedos de ZincRESUMEN
In eukaryotic cells, a spindle assembly checkpoint (SAC) ensures accurate chromosome segregation, by monitoring proper attachment of chromosomes to spindle microtubules and delaying mitotic progression if connections are erroneous or absent. The SAC is thought to be relaxed during early embryonic development. Here, we evaluate the checkpoint response to lack of kinetochore-spindle microtubule interactions in early embryos of diverse animal species. Our analysis shows that there are two classes of embryos, either proficient or deficient for SAC activation during cleavage. Sea urchins, mussels, and jellyfish embryos show a prolonged delay in mitotic progression in the absence of spindle microtubules from the first cleavage division, while ascidian and amphioxus embryos, like those of Xenopus and zebrafish, continue mitotic cycling without delay. SAC competence during early development shows no correlation with cell size, chromosome number, or kinetochore to cell volume ratio. We show that SAC proteins Mad1, Mad2, and Mps1 lack the ability to recognize unattached kinetochores in ascidian embryos, indicating that SAC signaling is not diluted but rather actively silenced during early chordate development.
Asunto(s)
Invertebrados/embriología , Puntos de Control de la Fase M del Ciclo Celular/fisiología , Huso Acromático/metabolismo , Animales , Puntos de Control del Ciclo Celular/fisiología , Proteínas de Ciclo Celular/metabolismo , Segregación Cromosómica/fisiología , Embrión no Mamífero/metabolismo , Cinetocoros/metabolismo , Microtúbulos/metabolismo , Mitosis/fisiología , Nocodazol/farmacología , Transducción de Señal/fisiologíaRESUMEN
In embryos of distantly related bilaterian phyla, their lateral neural borders give rise to the peripheral nervous system elements, including various mechanosensory cells derived from migratory precursors, such as hair cells and dorsal root ganglion (DRG) neurons in vertebrates, bipolar tail neuron (BTN) in Ciona, chordotonal organ in Drosophila, and AVM/PVM in Caenorhabditis elegans. Developmental genetics studies had revealed a couple of transcription factors (TFs) regulating differentiation of mechanosensory cells shared by vertebrates and arthropods. However, unbiased systematic profiling of regulators is needed to demonstrate conservation of differentiation gene batteries for mechanosensory cells across bilaterians. At first, we observed that in both C. elegans Q neuroblasts and Drosophila lateral neuroectoderm, conserved NPB specifier Msx/vab-15 regulates Atoh1/lin-32, supporting the homology of mechanosensory neuron development in lateral neural border lineage of Ecdysozia. So we used C. elegans as a protostomia model. Single-cell resolution expression profiling of TFs and genetic analysis revealed a differentiation gene battery (Atonh1/lin-32, Drg11/alr-1, Gfi1/pag-3, Lhx5/mec-3, and Pou4/unc-86) for AVM/PVM mechanosensory neurons. The worm-gene battery significantly overlaps with both that of placode-derived Atonh1/lin-32-dependent hair cells and that of NPB-derived Neurogenin-dependent DRG neurons in vertebrates, supporting the homology of molecular mechanisms underlying the differentiation of neural border-derived mechanosensory cells between protostome and deuterostome. At last, Ciona BTN, the homolog of vertebrate DRG, also expresses Atonh1/lin-32, further supporting the homology notion and indicating a common origin of hair cells and DRG in vertebrate lineage.
Asunto(s)
Evolución Molecular , Regulación del Desarrollo de la Expresión Génica , Invertebrados/genética , Neuronas/fisiología , Vertebrados/genética , Animales , Diferenciación Celular , Invertebrados/embriología , Invertebrados/crecimiento & desarrollo , Mecanotransducción Celular , Vertebrados/embriología , Vertebrados/crecimiento & desarrolloRESUMEN
Snails, earthworms and flatworms are remarkably different animals, but they all exhibit a very similar mode of early embryogenesis: spiral cleavage. This is one of the most widespread developmental programs in animals, probably ancestral to almost half of the animal phyla, and therefore its study is essential for understanding animal development and evolution. However, our knowledge of spiral cleavage is still in its infancy. Recent technical and conceptual advances, such as the establishment of genome editing and improved phylogenetic resolution, are paving the way for a fresher and deeper look into this fascinating early cleavage mode.
Asunto(s)
Evolución Biológica , Tipificación del Cuerpo , Eucariontes/crecimiento & desarrollo , Animales , Linaje de la Célula , Desarrollo Embrionario , Invertebrados/embriología , FilogeniaRESUMEN
Maturation of neuronal circuits requires selective elimination of synaptic connections. Although neuron-intrinsic mechanisms are important in this process, it is increasingly recognized that glial cells also play a critical role. Without proper functioning of these cells, the number, morphology, and function of synaptic contacts are profoundly altered, resulting in abnormal connectivity and behavioral abnormalities. In addition to their role in synaptic refinement, glial cells have also been implicated in pathological synapse loss and dysfunction following injury or nervous system degeneration in adults. Although mechanisms regulating glia-mediated synaptic elimination are still being uncovered, it is clear this complex process involves many cues that promote and inhibit the removal of specific synaptic connections. Gaining a greater understanding of these signals and the contribution of different cell types will not only provide insight into this critical biological event but also be instrumental in advancing knowledge of brain development and neural disease.
Asunto(s)
Sistema Nervioso Central/embriología , Degeneración Nerviosa/fisiopatología , Enfermedades del Sistema Nervioso/fisiopatología , Neuroglía/fisiología , Neuronas/fisiología , Sistema Nervioso Periférico/embriología , Sinapsis/fisiología , Animales , Astrocitos/fisiología , Evolución Biológica , Sistema Nervioso Central/crecimiento & desarrollo , Señales (Psicología) , Exosomas/fisiología , Humanos , Invertebrados/embriología , Microglía/fisiología , Morfogénesis , Vaina de Mielina/fisiología , Unión Neuromuscular/embriología , Sistema Nervioso Periférico/crecimiento & desarrollo , Sinapsis/patologíaRESUMEN
Posterior elongation of the developing embryo is a common feature of animal development. One group of genes that is involved in posterior elongation is represented by the Wnt genes, secreted glycoprotein ligands that signal to specific receptors on neighbouring cells and thereby establish cell-to-cell communication. In segmented animals such as annelids and arthropods, Wnt signalling is also likely involved in segment border formation and regionalisation of the segments. Priapulids represent unsegmented worms that are distantly related to arthropods. Despite their interesting phylogenetic position and their importance for the understanding of ecdysozoan evolution, priapulids still represent a highly underinvestigated group of animals. Here, we study the embryonic expression patterns of the complete sets of Wnt genes in the priapulids Priapulus caudatus and Halicryptus spinulosus. We find that both priapulids possess a complete set of 12 Wnt genes. At least in Priapulus, most of these genes are expressed in and around the posterior-located blastopore and thus likely play a role in posterior elongation. Together with previous work on the expression of other genetic factors such as caudal and even-skipped, this suggests that posterior elongation in priapulids is under control of the same (or very similar) conserved gene regulatory network as in arthropods.
Asunto(s)
Invertebrados/embriología , Proteínas Wnt/genética , Animales , Artrópodos/genética , Desarrollo Embrionario , Redes Reguladoras de Genes , Filogenia , Transducción de SeñalRESUMEN
Numerous aquatic invertebrates survive harsh environments by displaying dormancy as encysted embryos. This study aimed at determining whether metabolomics could provide molecular insight to explain the "dormancy syndrome" by highlighting functional pathways and metabolites, hence offering a novel comprehensive molecular view of dormancy. We compared the metabolome of morphologically distinct dormant encysted embryos (resting eggs) and non-dormant embryos (amictic eggs) of a rotifer (Brachionus plicatilis). Metabolome profiling revealed ~5,000 features, 1,079 of which were annotated. Most of the features were represented at significantly higher levels in non-dormant than dormant embryos. A large number of features was assigned to putative functional pathways indicating novel differences between dormant and non-dormant states. These include features associated with glycolysis, the TCA and urea cycles, amino acid, purine and pyrimidine metabolism. Interestingly, ATP, nucleobases, cyclic nucleotides, thymidine and uracil, were not detected in dormant resting eggs, suggesting an impairment of response to environmental and internal cues, cessation of DNA synthesis, transcription and plausibly translation in the dormant embryos. The levels of trehalose or its analogues, with a role in survival under desiccation conditions, were higher in resting eggs. In conclusion, the current study highlights metabolomics as a major analytical tool to functionally compare dormancy across species.
Asunto(s)
Embrión no Mamífero , Hidrobiología , Invertebrados/embriología , Metabolómica , AnimalesRESUMEN
Computer-assisted 4D manual cell tracking has been a valuable method for understanding spatial-temporal dynamics of embryogenesis (e.g., Stach & Anselmi BMC Biol, 13(113), 1-11 2015; Vellutini et al. BMC Biol, 15(33), 1-28 2017; Wolff et al. eLife, 7, e34410 2018) since the method was introduced in the late 1990s. Since two decades SIMI® BioCell (Schnabel et al. Dev Biol, 184, 234-265 1997), a software which initially was developed for analyzing data coming from the, at that time new technique of 4D microscopy, is in use. Many laboratories around the world use SIMI BioCell for the manual tracing of cells in embryonic development of various species to reconstruct cell genealogies with high precision. However, the software has several disadvantages: limits in handling very large data sets, the virtually no maintenance over the last 10 years (bound to older Windows versions), the difficulty to access the created cell lineage data for analyses outside SIMI BioCell, and the high cost of the program. Recently, bioinformatics, in close collaboration with biologists, developed new lineaging tools that are freely available through the open source image processing platform Fiji. Here we introduce a software tool that allows conversion of SIMI BioCell lineage data to a format that is compatible with the Fiji plugin MaMuT (Wolff et al. eLife, 7, e34410 2018). Hereby we intend to maintain the usability of SIMI BioCell created cell lineage data for the future and, for investigators who wish to do so, facilitate the transition from this software to a more convenient program.
Asunto(s)
Invertebrados/citología , Programas Informáticos , Animales , Linaje de la Célula , Desarrollo Embrionario , Invertebrados/clasificación , Invertebrados/embriología , Masculino , MitosisRESUMEN
Gene regulatory networks account for the ability of the genome to program development in complex multi-cellular organisms. Such networks are based on principles of gene regulation by combinations of transcription factors that bind to specific cis-regulatory DNA sites to activate transcription. These cis-regulatory regions mediate logic processing at each network node, enabling progressive increases in organismal complexity with development. Gene regulatory network explanations of development have been shown to account for patterning and cell type diversification in fly and sea urchin embryonic systems, where networks are characterized by fast coupling between transcriptional inputs and changes in target gene transcription rates, and crucial cis-regulatory elements are concentrated relatively close to the protein coding sequences of the target genes, thus facilitating their identification. Stem cell-based development in post-embryonic mammalian systems also depends on gene networks, but differs from the fly and sea urchin systems. First, the number of regulatory elements per gene and the distances between regulatory elements and the genes they control are considerably larger, forcing searches via genome-wide transcription factor binding surveys rather than functional assays. Second, the intrinsic timing of network state transitions can be slowed considerably by the need to undo stem-cell chromatin configurations, which presumably add stability to stem-cell states but retard responses to transcription factor changes during differentiation. The dispersed, partially redundant cis-regulatory systems controlling gene expression and the slow state transition kinetics in these systems already reveal new insights and opportunities to extend understanding of the repertoire of gene networks and regulatory system logic.
Asunto(s)
Organismos Acuáticos/genética , Regulación del Desarrollo de la Expresión Génica , Redes Reguladoras de Genes , Genoma , Invertebrados/genética , Vertebrados/genética , Animales , Organismos Acuáticos/crecimiento & desarrollo , Genómica , Invertebrados/embriología , Invertebrados/crecimiento & desarrollo , Vertebrados/embriología , Vertebrados/crecimiento & desarrolloRESUMEN
Gene expression can vary with the organisms' life stage. It is known that embryos can be more sensitive to toxicant exposure, as previously demonstrated for Enchytraeus crypticus (Oligochaeta) exposed to cadmium (Cd), known to cause embryotoxicity and hatching delay. It was shown that Ca enters embryos via the L-type Ca channels in the cocoon membrane, this being affected in Cd exposed embryos (Cd-Ca competition is well-known). In the present study, the embryotoxic mechanisms of Cd were studied via high-throughput gene expression for E. crypticus. Cocoons (1-2 days old), instead of the adult organism, were exposed in Cd spiked LUFA 2.2 soil during 1 day. Results showed that Cd affected Ca homeostasis which is implicated in several other molecular processes. Several of the major modulators of Cd toxicity (e.g., impaired gene expression, cell cycle arrest, DNA and mitochondrial damage) were identified in the embryos showing its relevancy as a model in ecotoxicogenomics. The draft Adverse Outcome Pathway was improved. Previously was hypothesized that gene regulation mechanisms were activated to synthesize more Ca channel proteins - this was confirmed here. Further, novel evidences were that, besides the extracellular competition, Cd competes intracellularly which causes a reduction in Ca efflux, and potentiates Cd embryotoxicity.
Asunto(s)
Cadmio/toxicidad , Expresión Génica , Oligoquetos/embriología , Animales , Calcio/metabolismo , Invertebrados/embriología , Invertebrados/genética , Oligoquetos/genética , Oligoquetos/fisiología , Suelo/química , Contaminantes del Suelo/toxicidadRESUMEN
All animal oocytes are surrounded by a glycoproteinaceous egg coat, a specialized extracellular matrix that serves both structural and species-specific roles during fertilization. Egg coat glycoproteins polymerize into the extracellular matrix of the egg coat using a conserved protein-protein interaction module-the zona pellucida (ZP) domain-common to both vertebrates and invertebrates, suggesting that the basic structural features of egg coats have been conserved across hundreds of millions of years of evolution. Egg coat proteins, as with other proteins involved in reproduction, are frequently found to be rapidly evolving. Given that gamete compatibility must be maintained for the fitness of sexually reproducing organisms, this finding is somewhat paradoxical and suggests a role for adaptive diversification in reproductive protein evolution. Here we review the structure and function of metazoan egg coat proteins, with an emphasis on the potential role their evolution has played in the creation and maintenance of species boundaries.
Asunto(s)
Evolución Biológica , Proteínas del Huevo/química , Proteínas del Huevo/metabolismo , Glicoproteínas de la Zona Pelúcida/química , Glicoproteínas de la Zona Pelúcida/metabolismo , Animales , Proteínas del Huevo/fisiología , Femenino , Humanos , Invertebrados/química , Invertebrados/embriología , Invertebrados/metabolismo , Dominios Proteicos , Multimerización de Proteína/fisiología , Vertebrados/embriología , Vertebrados/metabolismo , Zona Pelúcida/química , Zona Pelúcida/metabolismo , Glicoproteínas de la Zona Pelúcida/fisiologíaRESUMEN
It has been hypothesized that a condensed nervous system with a medial ventral nerve cord is an ancestral character of Bilateria. The presence of similar dorsoventral molecular patterns along the nerve cords of vertebrates, flies, and an annelid has been interpreted as support for this scenario. Whether these similarities are generally found across the diversity of bilaterian neuroanatomies is unclear, and thus the evolutionary history of the nervous system is still contentious. Here we study representatives of Xenacoelomorpha, Rotifera, Nemertea, Brachiopoda, and Annelida to assess the conservation of the dorsoventral nerve cord patterning. None of the studied species show a conserved dorsoventral molecular regionalization of their nerve cords, not even the annelid Owenia fusiformis, whose trunk neuroanatomy parallels that of vertebrates and flies. Our findings restrict the use of molecular patterns to explain nervous system evolution, and suggest that the similarities in dorsoventral patterning and trunk neuroanatomies evolved independently in Bilateria.
Asunto(s)
Evolución Biológica , Sistema Nervioso Central/anatomía & histología , Sistema Nervioso Central/embriología , Red Nerviosa/anatomía & histología , Red Nerviosa/embriología , Animales , Anélidos/anatomía & histología , Anélidos/embriología , Tipificación del Cuerpo , Invertebrados/anatomía & histología , Invertebrados/embriología , Placa Neural/anatomía & histología , Placa Neural/embriología , Filogenia , Rotíferos/anatomía & histología , Rotíferos/embriologíaRESUMEN
Spiralians, including molluscs, annelids and platyhelminths, share a unique development process that includes the typical geometry of early cleavage and early segregation of cell fate in blastomeres along the animal-vegetal axis. However, the molecular mechanisms underlying this early cell fate segregation are largely unknown. Here, we report spiralian-specific expansion of the three-amino-acid loop extension (TALE) class of homeobox genes. During early development, some of these TALE genes are expressed in staggered domains along the animal-vegetal axis in the limpet Nipponacmea fuscoviridis and the polychaete Spirobranchus kraussii. Inhibition or overexpression of these genes alters the developmental fate of blastomeres, as predicted by the gene expression patterns. These results suggest that the expansion of novel TALE genes plays a critical role in the establishment of a novel cell fate segregation mechanism in spiralians.