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At least 19 recordsLinked to original sources
PubMed1991

Interpopulational allogeneic reactions in the colonial protochordate Botryllus schlosseri.

Botryllus schlosseri is a cosmopolitan encrusting colonial tunicate which undergoes a natural transplantation reaction. When the growing edges of two colonies come into direct contact by interaction between their extracorporeal blood vessel termini, the ampullae, they either reject each other or fuse. This phenomenon is controlled by a single gene locus (Fu/HC) with multiple codominantly expressed alleles. Rejecting colonies share no alleles. Here we analyze allogeneic responses of Monterey (Mon), California, versus Woods Hole (WH), Massachusetts, colonies. Of 42 Mon x WH pairs tested, allogeneic rejection reactions occurred in all. Necrotic lesions (points of rejection, PORs) were produced and developed only by Woods Hole ampullae, either within the Woods Hole tunic, in the borderline between the paired colonies, or within the Monterey tunic. Four types of PORs were characterized. All types involved reactions of blood cells and vessels, including infiltration, hemorrhage formation, retraction and ampullae amputation. These findings were observed in single WH x Mon pairs, in multiple subclones of WH x Mon from two parental colonies (seven independent colony pairs were assayed), and on multiple repeats of interactions from pairs that had already undergone a rejection reaction. In all cases, the range of reaction types, the location of PORs, and the timing of the responses could be found in primary as well as repeat reactions.

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PubMed2025

First chromosome-level genome assembly of the colonial chordate model Botryllus schlosseri (Tunicata).

BACKGROUND: Botryllus schlosseri (Tunicata) is a colonial, laboratory model tunicate recognized for its remarkable developmental diversity, its regenerative abilities, and its peculiar genetically determined allorecognition system governed by a polymorphic locus controlling chimerism and cell parasitism. RESULTS: We report the first chromosome-level genome assembly of B. schlosseri subclade A1. By integrating long and short reads with Hi-C scaffolding, we produced both a phased diploid genome assembly and a conventional collapsed consensus sequence of 533 Mb. Of this total length, 96% belonged to 16 chromosome-scale scaffolds, with a BUSCO completeness score of 91.4%. We then compared our assembly with other high-quality tunicate genomes, revealing some synteny conservation but also extensive genomic rearrangements and a general loss of colinearity. CONCLUSIONS: The chromosome-level resolution of this assembly enhances our understanding of genome organization in colonial modular organisms. Comparative analyses highlight the dynamic nature of tunicate genomes, with conserved macrosynteny yet extensive microsyntenic rearrangements and scrambling, underscoring their rapid evolutionary trajectory. This high-quality genome assembly provides a valuable resource for exploring the unique biological features of colonial chordates, including their exceptional regenerative abilities and complex allorecognition system.

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PubMed1976

T system in ascidian muscle: organization of the sarcotubular system in the caudal muscle cells of Botryllus schlosseri tadpole larvae.

The organization of the sarcotubular system has been examined in the caudal muscle cells of the ascidian. Botryllus schlosseri. At variance with striated muscle of other protochordates. Botryllus muscle cells are endowed with a well-developed T system, which has a peculiar laminar structure. The thin T laminae are in continuity with the plasma membrane and extend longitudinally in the intermyofibrillar spaces. At the level of the I-band the T laminae are focally associated with SR cisternae in dyad junctions similar to those observed in invertebrate muscles. These findings are discussed in relation to the origin of the sarcotubular system in vertebrate muscle.

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PubMed1990

Botryllus schlosseri (Tunicata) whole colony irradiation: do senescent zooid resorption and immunological resorption involve similar recognition events?

The colonial tunicate Botryllus schlosseri undergoes cyclic blastogenesis where feeding zooids are senescened and resorbed and a new generation of zooids takes over the colony. When non-identical colonies come into direct contact, they either reject each other or fuse. Fusion is usually followed by the resorption of one of the partners in the chimera (immunological resorption). The striking morphological similarities between the two resorption phenomena suggest that both may involve tissue destruction following self-nonself recognition events. Here we attempt to modify these two events by whole colony gamma irradiation assays. Three sets of experiments were performed: 1) different doses of whole colony irradiation for determination of irradiation effects (110 colonies, up to 8,000 rads); 2) pairs of irradiated-nonirradiated isografts of clonal replicates for the potential of reconstruction of the irradiated partners (23 pairs); 3) chimeras of irradiated-nonirradiated partners for analysis of resorption hierarchy. Mortality increased with the irradiation dose. All colonies exposed to more than 5,000 rads died within 19 days, while no colony died below 2,000 rads. The average mortality periods, in days, for doses of 6,000-8,000, 5,000, and 2,500-4,000 rads were 14.4 +/- 3.1 (n = 24), 19.8 +/- 6.0 (n = 15), and 19.6 + 5.1 (n = 22), respectively. Younger colonies (3-6 months old) may survive radiation better than older ones (more than 13 months). Many morphological alterations were recorded in irradiated colonies: ampullar contraction and/or dilation, accumulation of pigment cells within ampullae, abnormal bleeding from blood vessels, sluggish blood circulation, necrotic zones, reduction in bud number, and irregularities in zooid and system structures. With doses of 3,000-4,000 rads and above, irradiation arrested the formation of new buds and interrupted normal takeover, turning the colony into a chaotic bulk of vessels, buds, and zooid segments. Death supervened after a period of up to 1 month of poor condition, which was also characterized by loss of organization in systems. In isografts of irradiated-nonirradiated parts, the normal subclone resorbed all zooids and buds of the irradiated one within less than 1 week, even if it was up to 13 times smaller, without showing any sign of harmful effects. Thus, the irradiated subclone is not reconstituted by sharing blood circulation with a syngeneic part. Under 2,000 rads some of the irradiated zooids within this type of union started to regenerate, and at 1,000 rads no resorption was recorded, even though the number of zooids decreased in the irradiated part.(ABSTRACT TRUNCATED AT 400 WORDS)

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PubMed1977

Fine structure of the intestinal epithelium of the colonial ascidian Botryllus schlosseri.

In the intestine of the filtering zooids of B. schlosseri three segments can be distinguished. In the intermediate segment the epithelium, which is encrusted by the ampullae of the pyloric gland, shows marked aspects of alteration. In the proximal and distal segments, ciliated mucous, vacuolated and endocrine-like cells are recognizable. Ciliated mucous cells, widely distributed along the intestine, possess the apical region filled with numerous mucous granules, which are extruded with merocrine modality. Variations in morphology of the granules are visible especially between cells of different regions. Vacuolated cells appear involved in absorptive function. They are characterized by developed microvilli, numerous apical small vesicles and great supranuclear vacuoles containing heterogeneous material. The vacuolated cells of the proximal segment resemble the gastric vacuolated cells of B. schlosseri. The vacuolated cells of the distal segment show many morphological similarities with protein absorbing cells of various animals for the presence of a giant vacuole and an apical network of vesicles and tubules with fuzzy coating on the luminal face. The intestinal endocrine-like cells are rare and characterized by strongly electron dense granules distributed in all the cytoplasm, but predominantly in the basal region.

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PubMed1975

Fine structure of the gastric epithelium of the ascidian Botryllus schlosseri. Mucous, endocrine and plicated cells.

The following five cell types have been recognized and defined on the basis of their fine structure in the gastric epithelium of B. schlosseri: vacuolated and zymogenic cells (described in a previous paper); ciliated mucous, endocrine and plicated cells. The ciliated mucous cells are distributed at the apex and the bottom of the gastric folds and along the dorsal groove. The mucus droplets appear to form from the Golgi complex as secretory granules of variable density and texture, which are released from the cell after fusion of their membranes with the apical plasma membrane. Holocrine or apocrine secretion has not been observed. The endocrine cells are scattered and are characterized by electron dense granules, especially numerous in the basal region of the cell. Finally, the plicated cells, present in the pyloric caecum, show rod-like microvilli, a well developed Golgi complex and abundant, deep infoldings of the basal plasma membrane, which are associated with numerous mitochondria. The possible role of the gastric cell types is discussed taking into account information concerning morphologically similar cells in other animals, as well as previously reported data on the biochemistry and physiology of digestion and excretion in ascidians.

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PubMed1988

Chimeras and histocompatibility in the colonial ascidian Botryllus schlosseri.

Chimeras of B. schlosseri were prepared by pairwise combination of colonies sharing one allele at the fusibility gene locus (AD = AC chimeras). A frequent resorption of one of the partners was observed and the resorption time was shown to be significantly correlated with the relative size, the resorbing partner being usually the larger. Both in the whole chimeras, AD = AC, and in the separated partners, (AD)AC, the fusibility of AC was frequently altered. In AD = AC the fusion did not prevent entirely AC fusion with BC. The fusion frequency with BC was significantly higher than with BD and significantly higher in (AD)AC than in AD = AC. Repeated rejections with BC or both BC and BD, repeated fusions with BD, simultaneous or successive fusions and rejections especially with BD, over a period of several months, indicated a long lasting competitive interaction of AD and AC in (AD)AC chimeras. The persistence in these chimeras of the AD cell population was also confirmed by the chimeric electrophoretic pattern of PGI in most of them.

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PubMed2026

Intra-colony divergence and global allele sharing reflect purifying selection and recombination at the Botryllus histocompatibility factor locus.

Urochordates, the closest relatives of vertebrates, lack adaptive immunity. However, some taxa, such as the colonial species Botryllus schlosseri, provide a unique model for studying innate self/non-self recognition through natural allogeneic transplantation responses. In this species, interactions between colonies are controlled by a highly polymorphic locus, with the Botryllus histocompatibility factor (BHF) being the only gene known to predict tissue fusion or rejection outcomes with complete accuracy. Here, we analyzed full-length BHF alleles from 19 laboratory-born and wild colonies and found that highly divergent alleles tend to coexist within individuals, whereas identical alleles can be shared across continental-scale distances. Despite extensive length variation, evidence of intragenic recombination, and pronounced nucleotide diversity, BHF exhibits limited protein divergence, with 33 alleles encoding only 17 distinct protein variants. Contrary to expectations for polymorphic recognition genes, no evidence of balancing or directional selection was detected. Instead, signatures of purifying selection were observed. We propose that this contrast between nucleotide and protein diversity arises from the combined effects of recombination, human-mediated gene flow, and linkage to nearby loci under balancing selection, while functional constraints maintain protein stability. These findings suggest that extensive protein diversification may not be a universal driver of allorecognition gene evolution.

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PubMed1990

Structural similarity between a primitive chordate membrane heterodimer and lymphocyte antigen receptors.

Botryllus schlosseri is a colonial tunicate that shared a common ancestor with the lineage leading to mammals about 450 million years ago, and flourishes today along the California coast. Prior studies of Botryllus populations have demonstrated the presence of a co-dominantly expressed, highly polymorphic histocompatibility locus (Fu/HC) controlling the acceptance (fusion) or rejection of new individuals into a parabiotic colony. Intercolonial blood cell contact, and recognition of self/not self, precedes both fusion and rejection reactions. Efforts to understand the evolution of the immune system necessitate study of cell surface molecules involved in cell-cell recognition events in primitive species. In mammals, birds, amphibians, and fishes clonally distributed lymphocyte surface molecules that are responsible for antigen recognition (B cell immunoglobulins and T cell receptors) can be distinguished by the disulfide linkage that pairs two or more polypeptides containing constant and variable regions. We have identified a disulfide-linked, heterodimeric (alpha beta) cell surface molecule in Botryllus with biochemical resemblance to mammalian lymphocyte antigen receptors. Observed charge variants of constituent chains of the tunicate protein described here do not correlate with Fu/HC allelic diversity. Both chains of this heterodimer can be resolved into several isoforms which are not based upon post-translational carbohydrate or phosphate additions. Comparisons of iodinated tryptic peptides from two beta chain isomorphs reveal one distinct and several common peptides.

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PubMed2026

Coating materials enhance urochordate primary cell culture adherence.

Marine invertebrate cell cultures are a potential source for diverse biotechnological applications, given the wide range of bioactive compounds they synthesize and accumulate. Yet, the number of established marine invertebrate cell culture systems remains limited compared with those of insects and vertebrates, particularly with respect to adherent cell cultures. Here we studied the in vitro adherence of circulating blood cells from the colonial ascidian Botryllus schlosseri. Two experimental approaches were employed, seeding blood cells either alone (setup 1) or in combination with tissue fragments (setup 2), using three basal media (DMEM, DMEM/F-12, RPMI) on culture plates coated with either Poly-L/D-lysine, gelatin, collagen, or laminin. Each experiment lasted for up to 3 d. Setup 1 results reveal that Botryllus cells remain viable and can adhere to coated surfaces in all tested media. Collagen- and laminin-coated plates supported longer-term cultures, whereas Poly-D (or L)-lysine coatings were more suitable for short-term studies. Among the basal media, RPMI and DMEM/F12 most effectively supported cell attachment. Setup 2 plates consistently showed higher cell adherence compared to setup 1, suggesting that tissue-derived factors may enhance attachment. Overall, circulating Botryllus cells demonstrate the capacity for substrate adhesion in vitro, offering a foundation for the development of adherent cell cultures.

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PubMed1992

A cyclical, developmentally-regulated death phenomenon in a colonial urochordate.

Botryllus schlosseri is a colonial ascidian whose asexually derived, clonally modular systems of zooids exhibit developmental synchrony. The blastogenic cycle culminates in a phase of programmed cell and zooid death called takeover, in which all functional zooids die over a 30 hr period, and are replaced by a new generation of individuals. Because of the weekly recurrence and magnitude of visceral death in this model organism, we have begun to characterize the mechanisms that govern takeover. Here we describe a monoclonal antibody (B3F12.9) that recognizes a novel 57 Kd polypeptide (under reducing conditions) localized to the perivisceral extracellular matrix (PVEM) of buds and zooids, as well as blood cells of Botryllus by immunofluorescence and immunogold labeling of tissue sections. During their active feeding phase, zooids exhibited a uniform labeling pattern of PVEM along their anteroposterior (A-P) axis. At the onset of takeover (T = 3 hr), B3F12.9 immunostaining became diffuse or absent at the anterior end, which paralleled the axis of contraction of the dying zooid, whereas the posterior end retained its labeling integrity. During mid (T = 15 hr) to late (T = 28 hr) takeover, issue damage was extensive, large blood macrophages and other B3F12.9 immunoreactive blood cells invaded the peribranchial cavity, whereas PVEM labeling gradually disappeared along the entire A-P axis. These findings indicate that takeover is a dynamic process in which extracellular matrix breakdown proceeds in a polarized fashion, beginning at the anterior end of each zooid and gradually propagating toward the posterior end.

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PubMed1992

Incidents of rejection and indifference in Fu/HC incompatible protochordate colonies.

We test here for the existence of specific alloimmune memory in the rejection responses of the colonial tunicate Botryllus schlosseri. Colony specificity in these organisms is controlled by the Fu/HC locus. Rejection occurs only between colonies that do not share any allelic determinant at this locus. Two sets of experiments were conducted: 1) Forty-nine pairs of nonfusible oozooids were interacted naturally along a period of several months. They rejected, disconnected, and in 20% of the cases, interacted again. 2) Repeated colony allorecognition assays were done on 15 pairs of interacting subclones (up to 5 consecutive tests/pair). Major results indicate: 1) Not all ampulla-ampulla interactions resulted in necrotic areas, points of rejection (PORs). 2) A full repertoire of PORs was attained within the first 10 days. Thereafter, no more PORs were added. 3) The outcome of indifference (cases where ampulla-ampulla contacts did not result in rejection) was repeatedly recorded in multiple tests, and its frequency increased in the secondary and tertiary tests along a set of 5 consecutive tests. It is concluded that allospecific memory, as measured by an accelerated production of PORs and amplification in their number, was not characteristic of the Botryllus rejection phenomenon, which, however, reveals the qualities of a low responder. These results are discussed in the light of some aspects of tolerance in the mammalian system.

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PubMed1990

Failure to find alloimmune memory in the resorption phenomenon of Botryllus cytomictical chimera.

It has been previously shown that mixed-cell chimeras may be established between different colonies of the compound tunicate Botryllus schlosseri given that they share one allele in common on the fusibility locus. However, one of the partners in each chimera is often resorbed. Here we tested for the existence of a memory component to this response, as measured by the accelerated interval to resorption of a second set of semiallogeneic colonies. Eight genetically unrelated colonies gave rise to eighteen chimeras. After a complete resorption of the "inferior" partners in these chimeras, secondary and tertiary sets of chimeras were established with some of them by fusion of the "superior" with naive subclones of the "inferior" partners. It is shown here that (a) when multiple chimeras are prepared using the same pair of colonies, subclones of only one of the partners are resorbed; (b) high variation in the time for resorption is recorded when several chimeras are prepared from any specific pair of colonies, and (c) the time for resorption is not related to the number of vessels connecting between the partners in the chimera, nor to their relative body sizes. Allospecific memory is not documented here and reasons for its absence are discussed.

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PubMed1977

Comparative studies on the structure of reproductive organs of four botryllid ascidians.

Reproductive organs of four botryllid ascidians, Botryllus primigenus, Botryllus schlosseri, Botrylloides violaceus and Botrylloides leachi, were studied histologically. In every species, the egg follicle consisting of an egg and its inner and outer follicles, is attached to the follicle stalk, the vesicle being composed of a flat epithelium, which in its turn is connected to the atrial epithelium or to the brood pouch specialized from it. In B. schlosseri, the egg is ovulated into the atrial cavity and remains there held by the brood cup, of which the inner epithelium is derived from the follicle stalk and the outer one from the atrial epithelium. In B. primigenus, the brood pouch develops as a diverticulum of the atrial cavity, around the entrance of which a fold differentiates from the atrial epithelium and closes the pouch during embryogenesis. In both species of Botrylloides, the brood pouch is formed by the outgrowth of the thickened atrial epithelium into the blood space, the entrance of which is closed during embryogenesis. The discarded outer follicle completely disintegrates soon after ovulation in B. schlosseri, but part of it remains throughout embryogenesis in the blood space in B. primigenus or projecting into the interior of the brood pouch in Botrylloides. In primigenus, the testis, when it accompanies the egg follicle, is placed at the bottom of the brood pouch and the sperm is shed through the pouch prior to ovulation. In B. schlosseri and the Botrylloides species, the testis is located independently from the egg follicle and the sperm matures after ovulation.

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PubMedDate not supplied

Allogeneic resorption in colonial protochordates: consequences of nonself recognition.

Colonial tunicates (protochordates of the subfamily Botryllinae) have the property of forming natural chimeras in the wild or in the laboratory with other members of the same species if both individuals share at least one allele at a single highly polymorphic locus, termed the fusibility/histocompatibility (Fu/HC) locus. Laboratory studies revealed that after the establishment of a common blood circulatory system between a fusible pair one of the colonies in the chimera is usually resorbed, a phenomenon that occurs after an interval of 1 week or extends to up to 8 months. In the present article, we review this allogeneic resorption in Botryllus schlosseri, a cosmopolitan protochordate. The studies on allogeneic resorption in B. schlosseri revealed 13 typical characteristics. However, several processes interrupt successful resorption, such as the retreat growth phenomenon, chimeric death, and others. It was also found that allogeneic resorption is not only genetically controlled but is also controlled by a polymorphic hierarchial phenomenon, including the Fu/HC locus and additional unrelated loci. One basic rule for this genetic system is that colonies heterozygotic on the resorption elements will resorb more homozygotic partners. This colony resorption, expressed by a morphological elimination of one partner, is probably manifested by cellular elements circulating in the tunicate blood system. However, it was also shown that some blood-borne cells of the inferior partner, such as the stem cells, may escape resorption, a phenomenon that raises the threat of germ/somatic cell parasitism.

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