New permanent stem cell niche for development and regeneration in a chordate
Virginia VanniFederico CaicciAnna PeronatoGraziano MartelloDavide AsnicarFabio GaspariniLoriano BallarinLucia Manni
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Abstract Stem cell niches are defined as the microenvironments where stem cells home, receiving stimuli defining their fate. In vertebrates, stem cell niches are stable and physically confined compartments. Botryllus schlosseri is an invertebrate colonial chordate where temporary stem cell niches have been identified in adult individuals that are cyclically resorbed and replaced by a new generation of clonal zooids. B. schlosseri also displays remarkable regenerative abilities, being capable of whole-body regeneration, but the cellular source of these processes is still unknown. Here we identified by means of a high-resolution morphological characterization a new putative stem cell niche in the ampullae of the circulatory system acting as a stem cell source during asexual reproduction. Stem cells of the ampullae travel via the circulatory system and contribute to the development of several organs and could explain where stem cells contributing to whole-body regeneration are stored. The ampullae niches are stable during the life cycle and regeneration of B. schlosseri , while additional niches of the zooid are dynamically established and colonised by circulating stem cells. Our results reveal an unprecedented dynamicity of stem cell niches in highly regenerative invertebrates.Keywords:
Zooid
Chordate
Stem cell niche
Regenerative Medicine
Asexual reproduction
Abstract Phenotypic plasticity is the capability of a genotype to produce different phenotypes in different environments. Previous studies have indicated phenotypic variability in asexual, male, and female reproduction in Botryllus schlosseri , a hermaphroditic, colonial ascidian, but not explicitly tested for genotype by environment interactions that indicate genetic variation in plastic responses. Consequently, clones derived from an estuarine population were deployed at their native site and a warmer, higher productivity site 10km up‐river. Male reproduction was assayed by testis size, female reproduction by the number of eggs produced, and asexual reproduction by colony growth rate. To test for ontogenetic effects, data were collected from two different generations of zooids born in the field. Analyses of variance indicated plasticity in asexual and female reproduction during the first zooid generation and plasticity in all three traits during the third zooid generation. Reaction norms varied significantly among genotypes in direction and magnitude for asexual reproduction at both times, implying that selection on asexual reproduction is weak. Sperm production during the third zooid generation was significantly lower at the nonnative site, but there was no genotype by environment interaction. The reaction norms for female reproduction varied significantly among genotypes in direction and magnitude during the first zooid generation, but only varied in magnitude during the third generation, with egg production being higher in all genotypes at the nonnative site. Comparisons of weighted frequency distributions between sites demonstrated that differences in egg production in the third generation were due to increases in the proportion of reproductive zooids within a colony. The greater emphasis on female reproduction at a site associated with higher food availability and temperature, and the greater emphasis on male reproduction at a colder, food‐limited site, supports predictions from sex allocation theory. J. Exp. Zool. 297A:180–188, 2003. © 2003 Wiley‐Liss, Inc.
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Abstract. A new mechanism of asexual multiplication of colonies is described in a colonial ascidian of the genus Clavelina (Aplousobranchiata). The mechanism consisted of the production of star‐shaped buds that originate from a basal vessel that bends anteriorly and extends along the dorsal region of the zooids. Once they are well developed, the buds detached easily and were dispersed by water movement. Analysis of the fine structure of the buds revealed that they were a modification of the stolonic budding common in this genus. Time‐lapse video recordings showed that released buds required several days to develop, allowing for a potentially significant dispersal range. The buds underwent organogenesis during which the central part gave rise to a new blastozooid with a defined polarity; the arms of the star gave rise to stolons. A new species is defined based on the presence of this type of budding and on other morphological features. The significance of these findings, which adds to the known mechanisms of asexual reproduction in ascidians, is discussed in relation to the biology and distribution of the species.
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1. Metandrocarpa taylori Huntsman (1912) is an ovoviviparous colonial ascidian with separate zooids connected by a common basal tunic, which reproduces asexually by pallial budding.2. Specimens in collections from field populations show maximum periods of sexual reproduction during the summer months. Although approximately 80% of the 1961 summer samples were reproductively active during this period, sexual reproduction continued during the remainder of the year with no less than 30% of the population active at any time. Eggs and testes develop simultaneously within the individual zooids.3. Asexual reproduction was quantitatively studied in colonies cultured in the intertidal zone. Budding rates are lowest during the summer and continue at a high level during the remainder of the year. These rates are not dependent upon the size or age of the colony, but do derive from variations in rates at which successive bud generations follow one another and from the number of bud offspring produced by each zooid.4. Although the two modes of reproduction are not mutually exclusive, it is clear that one form predominates in activity during any single season.5. There is a general direct relationship between sexual reproductive activity and ocean temperature. There is little correlation of reproductive activity with food supply, since either phytoplankton or suspended organic detritus are abundant in Monterey Bay all year.
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The relative numbers of sexually and asexually recruited colonies and the proportion of brooding zooids were determined in 26 species of cheilostome bryozoans of Late Cretaceous and Early Tertiary ages. Asexual reproduction seems to be much more widespread than previously realized, although its relative importance is related to growth habit. Arborescent species of these fossil assemblages reproduce mainly asexually via fragmentation; encrusting species reproduce sexually via motile larvae. Free-living species use both methods; some reproduce sexually, whereas other species have enhanced the ability to break and reproduce predominantly asexually. Mode of reproduction was stable over a period of 3 m.y. in all species except the vinelike Columnotheca cribrosa. In this species both the proportion of asexual recruits and brooding zooids varied in accord with environmental parameters. In all cases populations dominated by asexual propagation had a significantly lower proportion of brooding zooids than populations dominated by sexual propagation.
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Hydrocoryne iemanja sp. nov. was found in an aquarium, growing on rhodoliths of coralline algae collected on the south-eastern coast of Brazil (20°40′S 40°2′W). The colonies were reared through maturity in the laboratory. Each colony had up to 7 sessile, long and thin monomorphic zooids, very extensible and flexible, arising from a chitinous, hard dark-brown plate with minute spines. Medusae budded from near the basal part of hydrocaulus, and were released in immature condition, acquiring fully developed interradial gonads 5–7 days after release. Asexual reproduction by longitudinal fission was observed on the hydrocaulus of the polyps, both for those in normal condition and those with injuries. Fission started at the oral region, extending aborally, with a new hard plate formed in the basal part of hydrocaulus. When fission reached the new hard plate, the new polyp detached, becoming free and sinking to the bottom, starting a new colony. Detached polyps were morphologically indistinguishable from other polyps, being able to produce medusae. Mother and daughter polyps undertook subsequent fissions. This mode of longitudinal fission is distinct from other modes of longitudinal fission, a process known for a few species of cnidarians. Further studies of this process may shed light on the understanding of the evolutionary pathways in Cnidaria and animals. Hydrocoryne iemanja sp. nov. is distinguishable from its two congeners by the distinct marginal tentacles of the medusae—short and with a median nematocyst knob—an unambiguous character useful even for the identification of newly liberated medusae.
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ABSTRACT Embryogenesis and asexual reproduction are commonly considered to be coordinated developmental processes, which depend on accurate progression through a defined sequence of developmental stages. Here we report a peculiar developmental scenario in a simple chordate, Botryllus schlossenri, wherein a normal colony of individuals (zooids and buds) is regenerated from the vasculature (vascular budding) through a sequence of morphologically abnormal developmental stages. Vascular budding was induced by surgically removing buds and zooids from B. schlossenri colonies, leaving only the vasculature and the tunic that connects them. In vivo imaging and histological sections showed that the timing and morphology of developing structures during vascular budding deviated significantly from other asexual reproduction modes (the regular asexual reproduction mode in this organism and vascular budding in other botryllid species). Subsequent asexual reproduction cycles exhibited gradual regaining of normal developmental patterns, eventually leading to regeneration of a normal colony. The conversion into a normal body form suggests the activation of an alternative pathway of asexual reproduction, which involves gradual regaining of normal positional information. It presents a powerful model for studying the specification of the same body plan by different developmental programs.—Voskoboynik A., Simon‐Blecher, N., Soen, Y., Rinkevich, B., De Tomaso A. W., Ishizuka, K. J., Weissman I. L., Striving for normality: whole body regeneration through a series of abnormal generations. FASEB J. 21, 1335–1344 (2007)
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The neoblast distribution in the prepharyngeal portion of the body remains unchanged during the asexual reproduction of planaria. During the first few days after fission, the number of neoblasts decreases in the portion of the body immediately adjoining the site of daughter zooid detachment and considerably increases in the regenerative bud. Starting with the fourth day after division, there is an increase in the number of neoblasts in the region of future fission, which can be regarded as one preparatory mechanism for the next fission. The mitosis distribution pattern is just the reverse: the regions of the body with the highest neoblast density are characterized by a low mitotic index or no dividing cells at all. The neoblast and mitosis distributions in the daughter zooid during its asexual reproduction cycle duplicate those observed in the maternal zooid.
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Planaria
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