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Evolution of brain development in amphibians
Abstract
Principal events in the early embryonic development of the nervous system, from neurulation to primary differentiation, are
considered in different amphibian species. Attention is paid to numerous interspecific differences in the structure of neuroepithelium
and the patterns of neurulation and embryonic brain segmentation. The data presented indicate that similarity in brain developmental
patterns is apparently explained by universality of morphogenetic mechanisms rather than by the common origin of particular
species. A hypothesis is proposed that similarity in the shape of the developing amphibian brain is determined by mechanisms
of coding positional information necessary for histogenetic differentiation.
... In human and chick embryos, a unique mechanism of junctional neurulation, which involves concerted elevation and folding combined with local cell ingression and accretion, provides for the morphological integrity of the anterior and posterior NT (Catala et al., 1995;Colas & Schoenwolf, 2001;Copp et al., 2003;Dady et al., 2014;Griffith et al., 1992;Sakai, 1989;Shimokita & Takahashi, 2011). In amphibians, the neurulation in the anterior region is primary (Davidson & Keller, 1999;Harrington et al., 2009;Jacobson & Gordon, 1976;Saveliev, 2009). The development of posterior axial structures is reviewed in Beck (2015). ...
The neural tube of amniotes is formed through different mechanisms that take place in the anterior and posterior regions and involve neural plate folding or mesenchymal condensation followed by its cavitation. Meanwhile, in teleost trunk region, the neural plate forms the neural keel, while the lumen develops later. However, the data on neurulation and other morphogenetic processes in the posterior body region in Teleostei remain fragmentary. We proposed that there could be variations in the morphogenetic processes, such as cell shape changes and cell rearrangements, in the posterior region compared to the anterior one at the different stages. Here, we performed morphological and histochemical analyses of morphogenetic processes with an emphasis on neurulation in the zebrafish tail bud and posterior region. To analyze the posterior expression of sox2 and tbxta we performed WMISH. We showed that the tail bud cells of variable shapes and orientation are tightly packed, and the neural and notochord primordia develop first. The shape of the neural primordium undergoes numerous changes as a result of cell rearrangements leading to the development of the neural rod. At the prim-6 stage, the cells of the neural primordium directly form the neural rod. The neuroepithelial cells undergo sequential shape changes. At the stage of the neural rod formation, the apical regions of triangular neuroepithelial cells of the floor plate are enriched in F-actin. The neurocoel development onset is above the apical poles of neuroepithelial cells. The expression domains of sox2 and tbxta become more restricted during the development.
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This review summarizes some major events in the evolution of body plans along the backbone of the arthropod tree, with a special focus on the origin of insects. The incompatibility among recent molecular phylogenies motivates a discussion about possible causes for failures: there is a worrisome lack of information in alignments, which can be visualized with spectra of split-supporting positions, and there are systematic errors occurring even when using correct models in maximum likelihood methods (Kück et al., this book). Currently, these problems cannot be avoided. Combining information from the fossil record and from extant arthropods, the morphology-based evolutionary scenario leads from worm-like stem-lineage arthropods via first euarthropods to the crown group of Mandibulata. The evolution of the mandibulate head is well documented in the Cambrian Orsten fossils. The evolution within crustaceans is also the evolution that leads to characters of the bauplan of myriapods and insects. It is argued that morphologicallymyriapods do not fit to the base of the mandibulatan tree and that this placement is also not plausible from a paleontological point of view. Available morphological evidencesuggests that myriapods are the sister-group to Hexapoda and that tracheates evolved from a marine ancestor that was similar in many ways to Remipedia. In the extant fauna, the Remipedia are the sister-group of Tracheata.
Phylogenetic analyses based on large molecular data sets are reviewed, including results of the ‘Deep Metazoan Phylogeny’ project. The phylogeny of Crustacea is still little understood and tree topologies based on molecular data are not congruent with many other morphological data especially for deeper nodes. Earlier analyses using DNA data were not mutually consistent, but more recent analyses have achieved some stability due to better taxon sampling, longer alignments and more sophisticated data selection and modeling. Orthology prediction and gene selection strongly influence results. The current phylogenies place Remipedia and not Branchiopoda close to insects, usually Malacostraca appear closer to Cirripedia and Copepoda, monophyletic Maxillopoda were never recovered.
The theoretical reliability of Maximum Likelihood methods often fails in practice due to the finite size of data sets and because of peculiarities of the software, even when correct substitution models are used. In addition, systematic errors inherent to the method may occur.
To detect biases, we simulated star phylogenies. In the case of star-like divergences, an unbiased tree reconstruction method will choose a best resolved binary tree by chance. Concerning 4-taxon trees, each of the three possible topologies should be chosen with the same probability. Deviations from the expected equal frequency of occurrence of topologies indicate a bias of the method. Based on this assumption, we analysed the influence of topological bias on Maximum Likelihood tree reconstructions under a broad range of different branch length conditions, model parameter assumptions, and alignment lengths. Our analyses show that the Maximum Likelihood method can be influenced by topological bias at certain branch length differences even if model parameter assumptions have been chosen correctly. Furthermore, our analyses show that the topological bias obtained from tree reconstructions with correct model assumptions is more distinct for alignments with 100,000 base positions than for 10,000 base positions.
The quantitative approach based on the resolution of star-like trees seems to be a good starting point to test the influence of long branch attraction and chosen model assumptions. The artifactual attraction of strongly derived taxa found in our analyses due to oversimplified model assumptions confirms the commonly accepted assumption that an exclusion of among-site rate variation increases the probability of topological bias in Maximum Likelihood tree reconstructions when underlying data is heterogeneous. However, the occurrence of topological bias under correct model assumptions and the increased probability of grouping strongly derived taxa with increasing sequence lengths imply that this bias is a systematic error. A better adaption of model assumptions can only delay the occurrence of errors in Maximum Likelihood tree reconstructions for a certain range of branch length conditions.
Recent improvements of tools for inference of phylogenies from molecular data could not impede that tree topologies estimated from different data sets are often mutually incompatible (see e.g. recent discussions about placement of Porifera in the metazoan tree). There are obviously causes of error that remain undetected. Fundamental discrepancies between molecular phylogenies and morphological data (see e.g. Wägele and Kück, this book) nourish major doubts concerning the reliability of established methods.
A series of simulations with a 11-taxon setup designed to study conditions (branch length ratios, among site variation, alignment lengths) that are prone to long branch effects prove that three different classes of artefacts (Wägele and Mayer, 2007) can be discerned. Maximum likelihood inference is more successful if among site variation is considered with a mixed-distribution model, however reconstruction fails when differences in branch lengths are very large, especially in topologies with short stem-lineages. Long inner branches can lead to a systematic error with high support for the wrong tree caused by plesiomorphies even when long alignments and the correct model are used. Other errors are caused by signal erosion and by chance similarities. We present for a set of tree topologies the parameter ranges for which correct topologies can be obtained.
This review summarizes some major events in the evolution of body plans along the backbone of the arthropod tree, with a special focus on the origin of insects. The incompatibility among recent molecular phylogenies motivates a discussion about possible causes for failures: there is a worrisome lack of information in alignments, which can be visualized with spectra of split-supporting positions, and there are systematic errors occurring even when using correct models in maximum likelihood methods (Kück et al, this book). Currently, these problems cannot be avoided. Combining information from the fossil record and from extant arthropods, the morphology-based evolutionary scenario leads from worm-like stem-lineage arthropods via first euarthropods to the crown group of Mandibulata. The evolution of the mandibulate head is well documented in the Cambrian Orsten fossils. The evolution within crustaceans is also the evolution that leads to characters of the bauplan of myriapods and insects. It is argued that morphologically myriapods do not fit to the base of the mandibulatan tree and that this placement is also not plausible from a paleontological point of view. Available morphological evidence suggests that myriapods are the sistergroup to Hexapoda and that tracheates evolved from a marine ancestor that was similar in many ways to Remipedia. In the extant fauna, the Remipedia are the sistergroup of Tracheata.
The chordate body plan is characterized by a central notochord, a pharynx perforated by gill pores, and a dorsal central nervous system. Despite progress in recent years, the evolutionary origin of each of theses characters remains controversial. In the case of the nervous system, two contradictory hypotheses exist. In the first, the chordate nervous system is derived directly from a diffuse nerve net; whereas, the second proposes that a centralized nervous system is found in hemichordates and, therefore, predates chordate evolution. Here, we document the ontogeny of the collar cord of the enteropneust Saccoglossus kowalevskii using transmission electron microscopy and 3D-reconstruction based on completely serially sectioned stages. We demonstrate that the collar cord develops from a middorsal neural plate that is closed in a posterior to anterior direction. Transversely oriented ependymal cells possessing myofilaments mediate this morphogenetic process and surround the remnants of the neural canal in juveniles. A mid-dorsal glandular complex is present in the collar. The collar cord in juveniles is clearly separated into a dorsal saddle-like region of somata and a ventral neuropil. We characterize two cell types in the somata region, giant neurons and ependymal cells. Giant neurons connect via a peculiar cell junction that seems to function in intercellular communication. Synaptic junctions containing different vesicle types are present in the neuropil. These findings support the hypotheses that the collar cord constitutes a centralized element of the nervous system and that the morphogenetic process in the ontogeny of the collar cord is homologous to neurulation in chordates. Moreover, we suggest that these similarities are indicative of a close phylogenetic relationship between enteropneusts and chordates.
The embryonic origins of the central nervous system (CNS) can be traced back to the fertilized egg, in which the information for establishing the basic pattern of the nervous system is encoded not only in the nucleus but also in the cytoplasm, as Wilhelm His1.2 first proposed in his book Unsere Körperform. His modified the 18th-century preformationism3 and proposed a more advanced theory of prelocalization of “organ-forming germ regions” in the egg cytoplasm and hence under control of the maternal genome. The problem of how much control of development is exerted by maternally derived determinants in the egg cytoplasm and how much the embryo’s own genome contributes to its development are central themes of books by Wilson4 and Davidson.5 These books, written 90 years apart, show how little progress had been made in thattime in understanding the control of development of morphological patterns.
Neuroepithelial cells transform from spindle-shaped to wedge-shaped within the median and paired dorsolateral hinge points of the bending neural plate, but the mechanisms underlying these localized changes are unclear. This study was designed to evaluate further the hypothesis that localized wedging of neuroepithelial cells during bending involves basal cellular expansion resulting from alteration of the cell-cycle. Neurulating chick embryos were treated with tritiated thymidine, and transverse sections through the midbrain were examined autoradiographically. Parameters of the cell-cycle as well as nuclear position and size were assessed in the median hinge point, which contains predominantly wedge-shaped cells, and in adjacent lateral areas of the neural plate, which contain predominantly spindle-shaped cells. Both the DNA-synthetic phase and non-DNA synthetic portion of the cell-cycle were significantly longer in the median hinge point than in lateral neuroepithelial areas, some nuclei in both regions were located basally during these phases, and virtually all basal nuclei in the median hinge point were large. Additionally, the mitotic phase was significantly shorter in the median hinge point than in lateral areas. We present a model to explain how alteration of the cell-cycle in the median hinge point could generate wedging of cells in this region.
In the salamander embryo, the morphogenetic movements of neurulation are correlated with two cell shape changes in the neural epithelium: elongation and apical constriction of the columnar neural plate cells. Cells first elongate to form the flat open neural plate and then constrict apically as the plate rolls up to form the neural tube. Evidence is presented that these cell shape changes are intrinsic to the cells themselves and that they play a causal role in the morphogenetic movements. Neural plate cells contain numerous microtubules oriented parallel to the axis of elongation. These microtubules are critical to the elongation process. Possible mechanisms for microtubule function in cell elongation are considered. During apical constriction the cells contain bundles of microfilaments which encircle the cell apex in purse-string fashion. Evidence is presented which suggests that microfilament bundles play an active role in apical constriction, and that this localized contraction is produced by filament sliding.
Each blastomere in the marginal zone of Xenopus laevis embryos at the 32-cell stage was stained with Nile blue sulphate. Only specimens with the typical arrangement of blastomeres of morulae of this species were used, and special care was taken to prevent the dye from spreading to neighbouring cells and to determine the extent of stained areas. The prospective fate of each blastomere was studied and a new fate-map of the 32-cell embryo was drawn by tracing the movement of stain during the course of further development.
Horseradish peroxidase injected into individual blastomeres of 2- to 16-cell embryos ofXenopus laevis can later be identified in cells at larval stages 31 to 37. The label is confined to the progeny of the injected blastomeres and all such cells in the central nervous system retain the label. The space in the central nervous system occupied by the labeled cells originating from a single injected blastomere is termed a clonal domain, which has a characteristic size, shape, and position for each blastomere. Well-defined boundaries separate neighboring clonal domains with little or no mixing of cells belonging to different clonal domains.
Formation of wedge-shaped neuroepithelial cells, owing to the constriction of apical bands of microfilaments, is widely believed to play a major part in bending of the neural plate. Although cell "wedging" occurs during neurulation, its exact role in bending is unknown. Likewise, although microfilament bands occupy the apices of neuroepithelial cells, whether these structures are required for cell wedging is unknown. Finally, although it is known that cytochalasins interfere with neurulation, it is unknown whether they block shaping or furrowing of the neural plate, or elevation, convergence, or fusion of the neural folds. The purpose of this study was to reexamine the role of microfilaments in neurulation in the chick embryo. Embryos were treated with cytochalasin D (CD) to depolymerize microfilaments and were analyzed 4-24 hr later. CD did not prevent neural plate shaping, median neural plate furrowing, wedging of median neuroepithelial cells, or neural fold elevation. However, dorsolateral neural plate furrowing, wedging of dorsolateral neuroepithelial cells, and convergence of the neural folds were blocked frequently by CD. In addition, neural folds always failed to fuse across the midline in embryos treated with CD, and neural crest cell migration was prevented. These data indicate that only the later aspects of neurulation may require microfilaments, and that certain neuroepithelial cells, particularly those that normally wedge with median furrowing and elevation of the neural folds, become (and remain) wedge-shaped in the absence of apical microfilament bands. Thus, microfilament-mediated constriction of neuroepithelial cell apices is not the major force for median neuroepithelial cell wedging and elevation of the chick neural plate. Further studies are needed to localize the motor(s) for these processes.
It has been proposed that clonal restriction boundaries develop in Xenopus embryos between clones initiated at the 512-cell
stage, and that these boundaries result in formation of morphological compartments, each populated by progeny of a group of
ancestral cells. Although this hypothesis has gained some acceptance, it has also been criticized because the use of only
one cell lineage tracer was not a conclusive test of the hypothesis. However, the critical experiment, an assessment of the
extent of mingling between two labeled clones in the same embryo, has now been performed. A model of the proposed arrangement
of the ancestral cell groups in the 512-cell embryo predicted that the two clones would remain separate in 49% of cases and
intermingle in 51% of cases. In fact, there was a bimodal distribution, in which separation of the clones occurred in 46%
of embryos and extensive interclonal mingling was observed in 54%. These results are not compatible with hypotheses in which
a unimodal distribution of mingling would be predicted but are consistent with the compartment hypothesis.
A detailed fate map of all of the progeny derived from each of the blastomeres of the 32-cell-stage South African clawed frog embryo (Xenopus laevis), which were selected for stereotypic cleavages, is presented. Individual blastomeres were injected with horseradish peroxidase and all of their descendants in the late tailbud embryo (stages 32 to 34) were identified after histochemical processing of serial tissue sections and whole-mount preparations. The progeny of each blastomere were distributed characteristically, both in phenotype and location. Most organs were populated largely by the descendants of particular sets of blastomeres, the progeny of each often being restricted to defined spatial addresses. Thus, the descendants of any one blastomere were distinct and predictable when embryos were preselected for stereotypic cleavages. However, variations among embryos were common and the frequencies with which one may expect organs to contain progeny from any particular blastomere are reported. The differences in the fates of the 16-cell-stage blastomeres and their 32-cell-stage daughter blastomeres are outlined and can be grouped into three general categories. The two daughter cells may give rise to equal numbers of cells in a particular organ, one daughter cell may give rise to many more of the cells in an organ derived from the mother blastomere, or one daughter cell may give rise to all of the progeny in an organ derived from the mother blastomere. Thus, cell fates are segregated during cleavage stages in both symmetric and asymmetric manners, and the lineages exhibit a diversification mode (G. S. Stent, 1985, Philos. Trans R. Soc. London Ser. B 312, 3-19) of cell division.
The fate of each of the blastomeres in the 16-cell stage Xenopus embryo which had been carefully selected for stereotypic cleavages was determined by intracellularly marking a single blastomere with horseradish peroxidase and identifying the labeled progeny in the tailbud embryo by histochemistry. Each blastomere populated all three primary germ layers. The progeny of each blastomere were distributed characteristically both in phenotype and in location. For example, most organs were populated by the descendants of particular sets of blastomeres. Furthermore, within an organ the progeny of a single blastomere were restricted to defined spatial addresses. This study describes the fates of identified 16-cell stage blastomeres and demonstrates that they are distinct and predictable if embryos are preselected for stereotypic cleavages.
During urodele neurulation, presumptive neural cells elongate to form the neural plate and then constrict apically as the plate rolls up to form the neural tube. During the same period, epidermal cells gradually flatten. Electron microscopy of these cells has been carried out in an attempt to understand the mechanism of morphogenetic cell shape changes. In elongating neural plate cells, microtubules are oriented parallel to the long axis. Counts of numbers of these “paraxial” microtubules per cell do not differ significantly at three apicobasal levels of the cells; therefore, it is practical to consider the paraxial microtubules as a single population of full-cell-length microtubules. The number of paraxial microtubules per cell decreases significantly as the cell elongates, but the degree of elongation of a cell at a given stage is not closely related to the number of paraxial microtubules it contains. Several observations suggest that microtubules contribute to cell elongation by some form of transport mechanism. During the apical constriction of neural ectoderm cells, there is marked increase in thickness of a circumferential bundle of microfilaments which encircles the cell apex. The inverse relationship between increase in bundle thickness and decrease in circumference of the cell apex suggests that these processes result from increased overlap and interdigitation of the original complement of apical filaments. Flattening epidermal cells display randomly oriented microtubules and bundles of thicker filaments (70–100 Å in diameter) which are reminiscent of “tonofibrils” and appear to span the cell from desmosome to desmosome.
It is a matter of general knowledge that neurulation, as it occurs in most chordate embryos, proceeds by longitudinal in-folding of the neural plate. Løvtrup (1965) ably described such morphogenetic movements as they occur in several neurulating amphibians. The mechanical causes of these movements are not clearly understood, however. In his review of the prominent theories of neurulation, Curtis (1967) points to their various inadequacies and concludes that ‘possibly the solution of this problem is to search for contractile movements in the cells involved in neurulation’ (p. 310).
The present paper seeks to identify the causal mechanisms of neurulation in the African clawed toad Xenopus laevis. The study was originally undertaken specifically to test Cloney's (1966) prediction that the presumed contractility of neural plate cells is associated with the morphological presence of fine cytoplasmic filaments which actually constitute the molecular agents of contraction and cellular shape-changes.
Defect embryos of 24 series were prepared by removing increasing numbers of blastomeres from an 8-cell embryo of Xenopus laevis. They were cultured and their development was examined macroscopically when controls reached a tailbud stage or later. Results show that most of defect embryos of 12 series develop normally, and some of them become normal frogs. Each of these defect embryos contain at least two animal blastomeres, one dorsal, and one ventral blastomere of the vegetal hemisphere. This suggests that a set of these four blastomeres of the three types is essential for complete pattern regulation.
Xenopus embryos at the 2-cell stage were cut into right and left halves, those at the 4-cell stage into dorsal and ventral halves or individual blastomeres, and those at the 8-cell stage into lateral, animal and vegetal halves. Defect embryos, that is, 8-cell embryos from which a particular pair of blastomeres had been removed, were also prepared. These halves, blastomeres and defect embryos were cultured in 50% Leibovitz (L-15) medium supplemented with 10% foetal calf serum and then in 10% Steinberg solution. Their development was determined from their macroscopic appearance when controls reached stage 26 (early tailbud stage) or later.
The only halves that could develop into normal larvae or frogs were lateral ones of 2- and 8-cell embryos. An interesting finding was that these halves of 2-cell embryos developed into only half-embryos when cultured in the above Leibovitz medium beyond the beginning of gastrulation. On the other hand, most or all the dorsal and ventral halves at the 4-cell stage and the animal and vegetal quartets at the 8-cell stage did not form normally proportioned embryos. Defect embryos lacking any two blastomeres of the animal half gave rise to nearly normal embryos, whereas those lacking two dorsal or two ventral blastomeres of the vegetal half did not.
From the present results and those of studies now in progress, it is concluded that development of blastomeres and halves from these early embryos, except lateral halves from 2- and 8-cell embryos, is not regulative as expected earlier, and that a certain combination of blastomeres is essential for complete pattern regulation.
Results of experiments with biomechanical interactions of neuroepithelial cells from growing brain in various vertebrate taxa are analyzed. It is shown that neuroepithelium fulfills a number of mechanical functions at the stages of blastula, gastrula, neurula, and nerve tube. The cells develop mechanical tensions differing by their form, strength and duration. Tensions and compressions are resulted from local or global changes in the form of the cells possessing mechanical sensitiveness. Regular distribution of mechanical tensions and compression is related topologically to various zones of neurons differentiations. This allows to suppose mechanical dependence of processes of determination of the nerve system development at its earlier stages. The place of biomechanical interactions in the brain formation is considered in the framework of the evolution of structural organization of the vertebrate neuroepithelium.
The mechanisms of early embryonal shaping of the brain in man and animals were studied. Analysis of the biomechanical properties of development of nervous tissue and embryological experiments demonstrated that tangential neuroepithelial intention is the major source of positional information. Experimental changes in the neuroepithelial intention system resulted in various types of embryonal anomalies of the nervous system. Mechanism-dependent ion channels that have marked periods of sensitivity and determine the histogenetic direction of neuroblast cell differentiation were found to underlie the mechanosensitivity of the neuroepithelium. Experimental findings were compared with unique autopsy data on early development of the human brain. Human embryos were examined from neurulation to week 6 of development. Different types of human embryonal brain anomalies were shown to occur with 3 types of neurulation disorders: 1) an open preneuropore is responsible for anomalies of the forebrain and ethmoidal area; 2) arrested neurulation in the postneuropore leads to anomalies of the diencephalon, midbrain, and occipital region; 3) impaired neurulation in the caudal region is a cause of spinal cord anomalies. The above anomalies resulted from local compensatory responses of the neuroepithelium due to the lack of intentions that are characteristic of normal development of the neural tube.
Über Entwicklungsgeschichte der Thiere, Beo-bachtung und Reflexion
- K E Baer
Baer, K.E., Über Entwicklungsgeschichte der Thiere, Beo-bachtung und Reflexion, Konigsberg, 1837, vol. 2. Burnside, A., Microtubules and Microfilaments in Newt Neurulation, Dev. Biol., 1971, vol. 26, pp. 416–441.
Embrional'naya patologiya nervnoi sistemy (Embryonic Pathology of the Nervous System) Moscow: VEDI The Influ-ence of Morphogenetic Processes on the Timing of Gene Expression during Spanish Newt Ontogeny
- S V Saveliev
- S V Saveliev
- N V Besova
- L I Korochkin
Saveliev, S.V., Embrional'naya patologiya nervnoi sistemy (Embryonic Pathology of the Nervous System), Moscow: VEDI, 2007. Saveliev, S.V., Besova, N.V., and Korochkin, L.I., The Influ-ence of Morphogenetic Processes on the Timing of Gene Expression during Spanish Newt Ontogeny, Dokl. Akad. Nauk SSSR, 1989, vol. 305, no. 1, pp. 215–218.
Formoobrazovanie mozga pozvonochnykh (Morphogenesis of the Vertebrate Brain), Moscow: Mosk
- S V Saveliev
The Influence of Morphogenetic Processes on the Timing of Gene Expression during Spanish Newt Ontogeny
- S V Saveliev
- N V Besova
- L I Korochkin
- S.V. Saveliev
A Comparative Analysis of Neurulation in Urodeles and Anurans, Morfologiya
- Yu S Krivova
- S V Saveliev
Über die Morphogenese des Gehirns von Hynobius nebulosus, Folia Anat
- R Sumi
The Epigenetic Nature of Early Chordate Development
- P O Nieuwkoop
- A G Johneu
- B Albers
- P.O. Nieuwkoop
Formoobrazovanie mozga pozvonochnykh (Morphogenesis of the Vertebrate Brain)
- S V Saveliev
- S.V. Saveliev
Mechanism of Positional Information Coding in Embryonic Morphogenesis of the Vertebrate Brain
- S V Saveliev
Über die Morphogenese des Gehirns von Hynobius nebulosus
- R Sumi
- R. Sumi