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The gastropod Lottia peitaihoensis as a model to study the body patterning of trochophore larvae.

The body patterning of trochophore larvae is important for understanding spiralian evolution and the origin of the bilateral body plan. However, considerable variations are observed among spiralian lineages, which have adopted varied strategies to develop trochophore larvae or even omit a trochophore stage. Some spiralians, such as patellogastropod mollusks, are suggested to exhibit ancestral traits by producing equal-cleaving fertilized eggs and possessing "typical" trochophore larvae. In recent years, we developed a potential model system using the patellogastropod Lottia peitaihoensis (= Lottia goshimai). Here, we introduce how the species were selected and establish sources and techniques, including gene knockdown, ectopic gene expression, and genome editing. Investigations on this species reveal essential aspects of trochophore body patterning, including organizer signaling, molecular and cellular processes connecting the various developmental functions of the organizer, the specification and behaviors of the endomesoderm and ectomesoderm, and the characteristic dorsoventral decoupling of Hox expression. These findings enrich the knowledge of trochophore body patterning and have important implications regarding the evolution of spiralians as well as bilateral body plans.

Animals↗

Reproductive behavior in the squid Sepioteuthis australis from South Australia: ethogram of reproductive body patterns.

Squids use a diverse range of body patterns for communication. Each pattern consists of a series of chromatic, postural, and locomotor components that are under neural control and can change within fractions of a second. Here we describe an ethogram of 48 body pattern components from in situ observations of reproductively active Sepioteuthis australis. In addition, we identify the total time and average duration that each component is shown, to a resolution of 1 s. Our results suggest that only a few components (e.g., "Golden epaulettes," "Stitchwork fins," and "Rigid arms") are temporally common, that is, shown for more than 80% of the time. In contrast to the component classification reported for other species of squid, for this species we suggest a classification system consisting of "short acute" (lasting for < 10 s); some of these same components were also classified as "medium acute" (11-60 s) or "chronic" (> 60 s). Several body patterning components were previously unreported, as were some of the combinations observed. The significance of these patterning components is discussed within the context of the associated behaviors of the squid on the spawning grounds.

Animal Communication↗

An ethogram of body patterning behavior in the biomedically and commercially valuable squid Loligo pealei off Cape Cod, Massachusetts.

Squids have a wide repertoire of body patterns; these patterns contain visual signals assembled from a highly diverse inventory of chromatic, postural, and locomotor components. The chromatic components reflect the activity of dermal chromatophore organs that, like the postural and locomotor muscles, are controlled directly from the central nervous system. Because a thorough knowledge of body patterns is fundamental to an understanding of squid behavior, we have compiled and described an ethogram (a catalog of body patterns and associated behaviors) for Loligo pealei. Observations of this species were made over a period of three years (> or = 440 h) and under a variety of behavioral circumstances. The natural behavior of the squid was filmed on spawning grounds off Cape Cod (northwestern Atlantic), and behavioral trials in the laboratory were run in large tanks. The body pattern components--34 chromatic (including 4 polarization components), 5 postural, and 12 locomotor--are each described in detail. Eleven of the most common body patterns are also described. Four of them are chronic, or long-lasting, patterns for crypsis; an example is Banded Bottom Sitting, which produces disruptive coloration against the substrate. The remaining seven patterns are acute; they are mostly used in intraspecific communication among spawning squids. Two of these acute patterns--Lateral Display and Mate Guarding Pattern--are used during agonistic bouts and mate guarding; they are visually bright and conspicuous, which may subject the squids to predation; but we hypothesize that schooling and diurnal activity may offset the disadvantage presented by increased visibility to predators. The rapid changeability and the diversity of body patterns used for crypsis and communication are discussed in the context of the behavioral ecology of this species.

Animal Communication↗

Role of activin and other peptide growth factors in body patterning in the early amphibian embryo.

The amphibian body plan is established as the result of a series of inductive interactions. During early cleavage stages cells in the vegetal hemisphere induce overlying animal hemisphere cells to form mesoderm. The interaction represents the first major body-patterning event and is mediated by peptide growth factors. Various peptide growth factors have been implicated in mesoderm development, including most notably members of the transforming growth factor-beta superfamily. Identification of the so-called "natural" inducer from among the several candidate peptide growth factors is being achieved by employing several experimental strategies, including the use of a tissue explant assay for testing potential inducers, cloning of marker genes as indices of early induction events, and microinjection of altered peptide growth factor receptors to disrupt normal embryonic inductions. Activin emerges as the most likely choice for assignment of the role of endogenous mesoderm inducer, because it currently best fulfills the rigorous set of criteria expected of such an important embryonic signaling molecule. Activin, however, may not act alone in mesoderm induction. Other peptide growth factors such as fibroblast growth factor might be involved, especially in the regional patterning of the mesoderm. In addition, several genes (e.g., Wnt and noggin), which are expressed after the mesoderm is initially induced, probably assist in further definition of the mesoderm pattern. Following mesoderm induction, the primary embryonic organizer tissue (first described in 1924 by Spemann) develops and contributes further to body patterning by its action as a neural inducer. Peptide growth factors such as activin may also be involved in the inductive event, either directly (by facilitating gene expression) or indirectly (by serving to constrain pathways).

Activins↗

Drosophila virilis oskar transgenes direct body patterning but not pole cell formation or maintenance of mRNA localization in D. melanogaster.

The Drosophila melanogaster gene oskar is required for both posterior body patterning and germline formation in the early embryo; precisely how oskar functions is unknown. The oskar transcript is localized to the posterior pole of the developing oocyte, and oskar mRNA and protein are maintained at the pole through early embryogenesis. The posterior maintenance of oskar mRNA is dependent upon the presence of oskar protein. We have cloned and characterized the Drosophila virilis oskar homologue, virosk, and examined its activity as a transgene in Drosophila melanogaster flies. We find that the cis-acting mRNA localization signals are conserved, although the virosk transcript also transiently accumulates at novel intermediate sites. The virosk protein, however, shows substantial differences from oskar: while virosk is able to rescue body patterning in a D. melanogaster oskar- background, it is impaired in both mRNA maintenance and pole cell formation. Furthermore, virosk induces a dominant maternal-effect lethality when introduced into a wild-type background, and interferes with the posterior maintenance of the endogenous oskar transcript in early embryogenesis. Our data suggest that virosk protein is unable to anchor at the posterior pole of the early embryo; this defect could account for all of the characteristics of virosk mentioned above. Our observations support a model in which oskar protein functions both by nucleating the factors necessary for the activation of the posterior body patterning determinant and the germ cell determinant, and by anchoring these factors to the posterior pole of the embryo. While the posterior body patterning determinant need not be correctly localized to provide body patterning activity, the germ cell determinant may need to be highly concentrated adjacent to the cortex in order to direct pole cell formation.

Amino Acid Sequence↗

In vitro control of organogenesis and body patterning by activin during early amphibian development.

In the process of amphibian development, an embryonic body plan is established through cell division, sequential gene expression, morphogenesis and cell differentiation. The mechanism of body patterning is complex and includes multiple induction events. Activin, a TGF-beta family protein, can induce several kinds of mesodermal and endodermal tissues in animal cap explants in a dose-dependent manner. In a recent study of the role of activin in organogenesis, we succeeded in raising a beating heart by treating animal caps with a high concentration of activin. Activin also participates in kidney organogenesis in combination with retinoic acid. An embryonic kidney induced by activin and retinoic acid in vitro can function in vivo when it is transplanted into a larva in which pronephros rudiments have already been removed. Further, the activin-treated animal caps clearly show organizer actions that are closely related to body patterning along the anteroposterior axis. These experiments will help to serve as a model system for understanding organogenesis and body patterning at the cellular and molecular levels.

Activins↗

An oncogenic form of human raf can specify terminal body pattern in Drosophila.

Terminal portions of the Drosophila body pattern are specified by an extracellular ligand generated at each end of the early syncytial embryo. This ligand triggers the localized transcription of two gap segmentation genes, tailles (tll) and huckebein (hkb) through a signal transduction cascade involving the receptor tyrosine kinase torso (tor) and homologues of ras, raf, and mek (map kinae kinase). In contrast to the ligand, these signal transducing components are expressed ubiquitously. Here, we show that a constitutively active form of human raf1 protein can trigger tll and hkb transcription in Drosophila embryos and specify elements of the terminal body pattern. This result indicates a strong functional conservation between Drosophila and mammalian raf proteins and argues that the localized activity of Drosophila raf (D-raf) normally carries spatial information specifying the end portions of the body.

Animals↗

Novel genetic screen for genes involved in posterior body patterning in Drosophila.

Much of our current understanding of how cytoplasmic determinants are localized and activated stems from genetic analyses in Drosophila. Characterization of mutants defective in establishing the initial embryonic body pattern has revealed the importance of mRNA localization and translational control and identified several factors required for these processes. Nevertheless, many additional genes are likely to be involved. Here, we describe a novel genetic screen designed to identify genes that participate in posterior body patterning, an elaborate process involving the sequential use of two localized cytoplasmic determinants, the products of the oskar and nanos genes. From the screen, we recovered new alleles of genes known to be required for posterior body patterning, demonstrating the validity of the approach. In addition, we isolated numerous other mutants. Further characterization of one mutant, P58, revealed that it is a novel allele of bullwinkle. We find that in bullwinkle mutants, oskar mRNA localization is not maintained in the embryo and oskar protein accumulates ectopically and to abnormally high levels. These defects are distinct from previously described perturbations in oskar activity and provide new insights into the regulation of oskar.

Animals↗

Early experience and postembryonic maturation of body patterns in cuttlefish (Sepia officinalis).

This study investigates effects of the environment on the maturation of body patterns in cuttlefish (Sepia officinalis). Cuttlefish were reared either individually on a uniform background, which the authors have termed uniform-solitary conditions (Group A), or grouped on variegated backgrounds, which the authors have termed varied-social conditions (Group B). At Days 1, 15, 30, and 60, juveniles were placed individually in perceptually different testing conditions, either on small, variegated stones or on a uniform pale gray background. During development in both testing conditions, juveniles from Group B concealed themselves differently from those from Group A. Thus, it appears that the response to the background is subject to individual experience. Some hypotheses are discussed relating to the effect of early experience on the maturation of body patterns.

Animals↗

Morphogen gradients and the control of body pattern in insect embryos.

The basic body plan of insects is set up in response to determinants initially localized at the anterior and posterior poles of the egg. Early in development, these determinants give rise to a series of morphogen gradients which in turn trigger a cascade of molecular signals determining the body pattern. This signalling process is outlined and recent experiments testing the roles of these gradient systems in determining anterior and posterior pattern are described. The results of these experiments suggest that anterior pattern is controlled by a single instructive gradient, whereas posterior pattern depends on the overlap of several gradients, each providing only one or a few distinct responses.

Animals↗

Body patterning.

Early patterning of the body during animal development is a fundamental process to subsequent events including cell differentiation, tissue and organ formation, and correct function of the adult body. We focused on two major topics: body segmentation and brain patterning, both of which are essential for conferring a functional complexity to the body, repetition of skeletal elements and complex neural network, respectively.

Animals↗

Dynamics of the control of body pattern in the development of Xenopus laevis. IV. Timing and pattern in the development of twinned bodies after reorientation of eggs in gravity.

The mesendodermal anatomy of twinned larval axes is described in relation to the normal single pattern, when twinning has been caused by experimental tilting of eggs before first cleavage. The formation of two origins for gastrulation movements (dorsal lips) and their relatively rapid spread and coalescence to give a circular blastopore, is a predictor of twin formation in individual embryos after treatment. The anatomy of twins where development has been disturbed from the outset in this way is appreciably different from that induced by the later operation of second dorsal lip implantation. It is also variable in a systematic way. The total sizes of cellular allocations to individual notochords and prechordal head patterns are enhanced above normal if they arise relatively close together in the tissue, but significantly reduced if they arise far apart. These and other features of twinned patterns due to precleavage disturbance are discussed in terms of what they might indicate about the physicochemical nature of the body positional system. The results confirm that by a variety of rather simple, nonsurgical manipulations the relative amounts of territory in the egg devoted to different parts of the body can be greatly influenced.

Animals↗

Reconstitution of the organizer is both sufficient and required to re-establish a fully patterned body plan in avian embryos.

Lateral blastoderm isolates (LBIs) at the late gastrula/early neurula stage (i.e., stage 3d/4) that lack Hensen's node (organizer) and primitive streak can reconstitute a functional organizer and primitive streak within 10-12 hours in culture. We used LBIs to study the initiation and regionalization of the body plan. A complete body plan forms in each LBI by 36 hours in culture, and normal craniocaudal, dorsoventral, and mediolateral axes are re-established. Thus, reconstitution of the organizer is sufficient to re-establish a fully patterned body plan. LBIs can be modified so that reconstitution of the organizer does not occur. In such modified LBIs, tissue-type specific differentiation (with the exception of heart differentiation) and reconstitution of the body plan fail to occur. Thus, the reconstitution of the organizer is not only sufficient to re-establish a fully patterned body plan, it is also required. Finally, our results show that formation and patterning of the heart is under the control of the organizer, and that such control is exerted during the early to mid-gastrula stages (i.e., stages 2-3a), prior to formation of the fully elongated primitive streak.

Animals↗

In vitro induction systems for analyses of amphibian organogenesis and body patterning.

The discovery that some well-known growth factors have inducing activity in embryogenesis has accelerated our understanding of embryonic induction. Relevant receptors, signal transduction pathways and patterns of gene expression have been characterized over the past decade. Amphibian embryos have provided an excellent model for analysis of embryonic induction because they are easily surgically manipulated and cultured in vitro, and with the addition of treatment with various inducing factors we have been able to control organogenesis and body patterning during early development in vitro. Activin A, a TGF-beta family protein, has a potent mesoderm-inducing activity on the isolated ectoderm called the animal cap. Activin induces animal caps to differentiate into various mesodermal and endodermal tissues, including beating hearts, in a dose-dependent fashion. Activin, in combination with retinoic acid, also induces the formation of the pronephros, a primitive embryonic kidney. The in vitro induced kidney was confirmed to function in vivo in a transplantation experiment. Furthermore, the activin-induced animal caps organize heads or trunk-and-tails in exactly the same manner as the organizer. The potential use of in vitro induction systems to further our understanding of vertebrate organogenesis and body patterning will be discussed.

Activins↗

Similarities between trunk and spätzle, putative extracellular ligands specifying body pattern in Drosophila.

The basic body plan of Drosophila is specified by four determinant systems that organize pattern along the anteroposterior and dorsoventral axes. Two of these systems (anterior and posterior) depend on localized mRNAs. In contrast, the other two (ventral and terminal) require locally generated extracellular ligands that are transduced, respectively, by the transmembrane receptors Toll and torso (tor). The ligand for the Toll receptor is thought to be spätzle (spz), a secreted protein that is activated by proteolytic cleavage. Here we report that trunk (trk), a gene required for activity of the tor receptor, encodes a protein that resembles spz in several respects. In particular, the sequence suggests that trk is a secreted protein and that it contains an internal site for proteolytic cleavage. Furthermore, the carboxy-terminal domain of trk has a similar arrangement of cysteines to that of spz. We propose that trk encodes an extracellular ligand involved in specifying terminal body pattern and suggest by analogy with spz that a cleaved form of trk constitutes the ligand for the tor receptor.

Alleles↗

Congenital abnormalities of body patterning: embryology revisited.

Many of the developmental mechanisms and molecular pathways that underlie fundamental features of body patterning are shared by all vertebrates, and some have even been conserved across evolution from invertebrates to vertebrates. Defects in such processes are a common cause of congenital malformation syndromes, and rapid progress is being made in elucidating their embryological and genetic basis. Here, I focus on three examples, each of which has been the subject of recent advances, and which together illustrate many of the most interesting and important aspects of these disorders. The first example is the development of the pharyngeal apparatus and its perturbation in DiGeorge's syndrome; the second is the induction and differentiation of the forebrain and its perturbation in holoprosencephaly; and the third is the role played by the human HOX genes in congenital malformations.

Body Patterning↗

Signaling to the enemy? Body pattern expression and its response to external cues during hunting in the cuttlefish Sepia officinalis (Cephalopoda).

Cuttlefish can rapidly alter their appearance by using neurally controlled chromatophore organs. This ability may provide a window into their cognitive capacity. We test whether the changes in body pattern that occur during hunting depend on context. If they do, then it may be possible to use these changes to study cephalopod cognition while the animal is engaged in ecologically relevant tasks. We found consistent individual differences in the tendency of cuttlefish to hunt with the first two arms raised. We also found that cuttlefish usually darken their skin after they seize a prey item. This darkening is observed regardless of the identity of the prey (fish, crab, or shrimp), prey context (buried in sand, in a bare tank, or on top of a rock pile), or the presence of a sudden stimulus. The sudden stimulus was created by presenting an overhead model bird to the cuttlefish. The model induced components of the Deimatic Display, which is a form of antipredator behavior, suggesting that the model was perceived as a potential threat. Passing Cloud displays and the Darkening of the arms were significantly reduced after exposure to the model bird. The effect of a potential predator on body pattern expression during hunting suggests it may be possible to use these changes as a sensitive indicator of ecologically relevant learning.

Animal Communication↗

Differing strategies for organizing anterior and posterior body pattern in Drosophila embryos.

Opposing anterior and posterior morphogen systems specify the segmented body pattern of Drosophila. The anterior morphogen, bicoid, exerts a direct, instructive influence on head and thoracic pattern by triggering different outcomes according to changes in its concentration along the body. In contrast, the posterior morphogen, nanos, simply defines where abdominal patterning can occur by eliminating an otherwise ubiquitous repressor, hunchback protein, from the posterior half of the embryo. Within this hunchback-free domain the pattern of abdominal segments must be specified by other morphogens, possibly by shorter range gradients of the products of zygotic gap genes Kruppel, knirps and tailless.

Animals↗