GROWTH AND SEXUAL MATURATION OF LABORATORY-CULTURED MONTEREY<i>BOTRYLLUS SCHLOSSERI</i>

Boyd, Heather C.; Brown, Stephen K.; Harp, James A.; Weissman, Irving L.

doi:10.2307/1541383

Cited by 103 publications

(72 citation statements)

References 13 publications

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“…First, Sabbadin and Zaniolo demonstrated that progenitors are mobile, and can naturally transplant between parabiosed individuals resulting in long-term germline chimerism and parasitism (Sabbadin and Zaniolo, 1979). Second, adults in both natural and laboratory-reared populations cycle between fertile and infertile states, demonstrating that germline progenitors that can be quiescent exist within an individual (Boyd et al, 1986;Sabbadin, 1953). Finally, prospective isolation studies suggested that both germline and somatic progenitors could be enriched about 10 times based on ALDH activity (Laird et al, 2005).…”

Section: Discussionmentioning

confidence: 99%

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Early lineage specification of long-lived germline precursors in the colonial ascidianBotryllus schlosseri

et al. 2009

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DEVELOPMENT 3486bodies undergo apoptosis and are removed via phagocytic cells in the blood, the primary bud migrates into the newly vacated region of the colony, opening its siphons and becoming a zooid, the secondary bud becomes the primary bud, and a new secondary bud begins to develop. Thus, the life history of Botryllus consists of a constant succession of individual zooids, each with a three-week lifespan (Lauzon et al., 2002).Asexual development (blastogenesis) takes 14 days under laboratory conditions, and can be divided into seven distinct visual stages ( Fig. 1; stages A-1 through D) (Lauzon et al., 2002). A new generation starts as a secondary bud, first visible as a thickening of the peribranchial epithelium of a primary bud ( Fig. 1; stage A1), which evaginates and forms a closed vesicle ( Fig. 1; stage A-2 through B-2). Next, a series of epithelial invaginations and protrusions ( Fig. 1; stage C-1) differentiate into somatic tissues and organs ( Fig. 1; stage C-2). After seven days ( Fig. 1; stage D), the secondary bud transitions to a primary bud and continues to develop. At day 14, the siphons open and the primary bud becomes a filterfeeding adult zooid. Each zooid can generate multiple buds each week, so the colony will eventually expand asexually. While interconnected, the zooids and buds develop independently, and individuals can be separated from the colony without disturbing their growth (i.e. subcloning), thus multiple experiments can be done on a single genotype.Following metamorphosis, colonies undergo at least 8-12 developmental cycles prior to the first appearance of gametes (sexual maturity). In addition, populations show seasonal fertility, and in the lab cycle in and out of reproductive (fertile) and nonreproductive (infertile) states. However when the colony is fertile development of the gametes is synchronized with somatic development (Mukai, 1977;Mukai and Watanabe, 1976;Sabbadin and Zaniolo, 1979). The first appearance of gonads occurs in the secondary bud (stage B), when mobile progenitors in the blood migrate to a region between the inner epithelium and the epidermis and begin to proliferate. Concurrently, oocytes at various stages of development also appear (Fig. 1). Over the next 10 days, the medial region of the blastema will differentiate into the lobular testis, while the lateral region will become the ovary (Sabbadin and Zaniolo, 1979). For the latter, one or several oocytes will become fixed on the epithelia of the peribranchial chamber, and an oviduct will form from the outer follicular layer. Upon transition to the adult zooid, mature eggs will immediately ovulate into the peribranchial chamber, be fertilized by exogenous sperm, and develop in situ. Several hours to days later the testes will complete development, and sperm will be released into the peribranchial chamber and flushed into the water column, fertilizing neighboring colonies (Johnson and Yund, 2004). The time lag between ovulation and sperm release (protogyny) prevents self-fertilization.Given this plastici...

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Section: Discussionmentioning

confidence: 99%

“…Botryllus schlosseri colonies were raised, staged, crossed and screened at 18-20°C according to Boyd et al (Boyd et al, 1986). Embryos were isolated and prepared for in situ hybridization as previously described (Brown and Swalla, 2007).…”

Section: Animalsmentioning

confidence: 99%

Early lineage specification of long-lived germline precursors in the colonial ascidianBotryllus schlosseri

et al. 2009

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“…This unique developmental phenomenon, in which every week all functional soma go through an apoptotic process, remains an empirical and theoretical challenge. To date, only a limited number of methodologies have been found to successfully alter the blastogenic rhythm, including changes of water temperature regimen (Boyd et al, 1986;, use of allogeneic fusions (Rinkevich and Weissman, 1987a), or zooid/bud removals (Sabbadin, 1956a,b;Lauzon et al, 2002) or by employing ionization radiation (Rinkevich and Weissman, 1990). All the above protocols, however, had not revealed much of the nature of this unique phenomenon.…”

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confidence: 99%

Macrophage involvement for successful degeneration of apoptotic organs in the colonial urochordateBotryllus schlosseri

Voskoboynik

Rinkevich

Weiss

et al. 2004

Journal of Experimental Biology

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SUMMARY Apoptosis is an important tool for shaping developing organs and for maintaining cellular homeostasis. In the colonial urochordate Botryllus schlosseri, apoptosis is also the hallmark end point in blastogenesis, a cyclical and weekly developmental phenomenon. Then the entire old generation of zooids are eliminated (resorbed) by a process that lasts 24–36 h. Administration of the antioxidant butylated hydroxytoluene (BHT) resulted in resorption being arrested by 1–8 days on average. At high doses(2.5–15.0 mg BHT l-1) resorption was completed only after removal of BHT. Colonies that were not removed in time, died. In treated colonies, although DNA fragmentation was high, tissues and organs that would normally have died, survived, and the general oxidative levels of lipids were reduced. Blood vessels were widened, containing aggregates of blood cells with a significantly increased proportion of empty macrophage-like cells without inclusion. In colonies rescued from BHT treatment, resorption of zooids started immediately and was completed within a few days. We propose three possible mechanisms as to how BHT may affect macrophage activity: (1) by interrupting signals that further promote apoptosis; (2) through the respiratory burst initiated following a phagocytic stimulus; and (3) by reducing lipid oxidation and changing cell surface markers of target cells. Our results point, for the first time, to the role of phagocytic cells in the coordination of death and clearance signals in blastogenesis.

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“…The colonial ascidians B. schlosseri and B. leachi can be readily cultured on glass slides in the laboratory (generation time 2-3 months) (Boyd et al, 1986). These animals, which produce few embryos, are particularly adapted to the study of blastogenesis and regeneration.…”

Section: Experimental Techniques In Tunicatesmentioning

confidence: 99%

“…The breeding of C. intestinalis and C. savignyi in the laboratory (Hendrickson et al, 2004;Joly et al, 2007) has also permitted the development of germ-line transgenesis by electroporation (Matsuoka et al, 2005), a technique that has been subsequently improved by the use of the Minos transposon, which opens the way to insertional mutagenesis and enhancer-trap assays . Finally, powerful computational methods and infrastructures have been developed for solitary ascidians, in particular C. intestinalis, which facilitate genomic data analysis and the integration of molecular and anatomical data into virtual representations of embryogenesis (Tassy et al, 2010;Endo et al, 2010).The colonial ascidians B. schlosseri and B. leachi can be readily cultured on glass slides in the laboratory (generation time 2-3 months) (Boyd et al, 1986). These animals, which produce few embryos, are particularly adapted to the study of blastogenesis and regeneration.…”

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confidence: 99%

Evolutionary crossroads in developmental biology: the tunicates

2011

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The tunicates, or urochordates, constitute a large group of marine animals whose recent common ancestry with vertebrates is reflected in the tadpole-like larvae of most tunicates. Their diversity and key phylogenetic position are enhanced, from a research viewpoint, by anatomically simple and transparent embryos, compact rapidly evolving genomes, and the availability of powerful experimental and computational tools with which to study these organisms. Tunicates are thus a powerful system for exploring chordate evolution and how extreme variation in genome sequence and gene regulatory network architecture is compatible with the preservation of an ancestral chordate body plan. Key words: Chordates, Tunicates, Asexual development, Budding, Embryogenesis, EvolutionIntroduction Cephalochordates (including Amphioxus; see Glossary, Box 1), tunicates (or urochordates, see Glossary, Box 1) and vertebrates constitute the chordate phylum, which is characterized by a tadpolelike body plan at the end of embryogenesis. The rigidity of the tail of these tadpoles is ensured by a unique structure, the notochord, which gave its name to the phylum. Fossil evidence, although sometimes controversial, suggests that ancestral chordates roamed Cambrian oceans more than 550 million years ago (Morris, 1999;Shu et al., 1996).It is now thought that cephalochordates are the most basal chordates. Tunicates and vertebrates are sister taxa (see Glossary, Box 1), which diverged more recently (Delsuc et al., 2006;Bourlat et al., 2006;Putnam et al., 2008). This molecular classification is supported at the anatomical level by the presence in tunicate larvae, but not in those of cephalochordates or of any other invertebrate, of cells similar to vertebrate migratory neural crest cells (Jeffery, 2007).The tunicates constitute a diverse group of animals that are united by the cellulose-containing tunic that covers their body (Nakashima et al., 2004). They are traditionally split into three major classes: the ascidians, thaliaceans and appendicularians, whose phylogenetic relationships are depicted in Fig. 1 (Tsagkogeorga et al., 2009;Govindarajan et al., 2010). Ascidians, also called sea squirts, are the most diverse tunicate group and include several developmental models such as Ciona intestinalis, Halocynthia roretzi and Botryllus schlosseri. These vase-like benthic filter feeders (see Glossary, Box 1) ('ascidian' derives from Development 138, 2143Development 138, -2152Development 138, (2011 Filter feeder. Organisms that feed on particulate food suspended in water. In tunicates, water enters the body via the oral siphon, is filtered on the branchial basket and expelled through an atrial siphon (in appendicularians, water is expelled through gill slits).Hybridization. The production of offspring by interbreeding between two individuals of different species. Kernel. A small region of a gene regulatory network that is evolutionarily highly conserved, the retention of which might underlie the conservation of body plans and the development of major ...

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GROWTH AND SEXUAL MATURATION OF LABORATORY-CULTURED MONTEREYBOTRYLLUS SCHLOSSERI

Cited by 103 publications

References 13 publications

Early lineage specification of long-lived germline precursors in the colonial ascidianBotryllus schlosseri

Early lineage specification of long-lived germline precursors in the colonial ascidianBotryllus schlosseri

Macrophage involvement for successful degeneration of apoptotic organs in the colonial urochordateBotryllus schlosseri

Evolutionary crossroads in developmental biology: the tunicates

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