Heritable germ and somatic cell linage competitions in chimeric colonial protochordates

Department of Developmental Biology , Stanford University, Palo Alto, California, United States
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 09/1999; 96(16):9148-53. DOI: 10.1073/pnas.96.16.9148
Source: PubMed


Theories of evolution that state natural selection acts on individuals have been modified to include multiple levels of selection. Here we demonstrate in chimeric protochordates that primitive germ cell (pgc) and somatic cell (psc) lineages have traits that also make them likely units of natural selection. Specifically, by using microsatellites to determine the genetic identity of various somatic and gametic tissues within vascularly fused Botryllus schlosseri chimeras, we show that genetically distinct pgc and psc can compete for access to developing gonads and somatic organs, and that this competition is hierarchical, reproducible, and heritable. Given that a single, highly polymorphic locus (Fu/HC) controls whether two contacting colonies fuse or reject, our findings also support a leading hypothesis for why the highly polymorphic histocompatibility loci common to many metazoa may have arisen or been maintained: to limit supercompetitor lineages to histocompatible kin.

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Available from: Baruch Rinkevich, Jun 10, 2014
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    • "In addition, following fusion one genotype may contribute disproportionately to new germline development, enabling one genotype to dominate the gametic output of the fused bud (Sabbadin & Zaniolo 1979; Pancer et al. 1995, Stoner & Weissman 1996). This process, called germ cell parasitism (GCP), is a repeatable and heritable trait (Stoner et al. 1999), with winner and loser genotypes in both lab-reared and field colonies. These parasitic abilities are autonomous to the cells themselves, retaining their parasitic phenotype upon transplantation (Laird et al. 2005; Brown et al. 2009), and allowing an experimental analysis of the cell properties responsible for regeneration (Brown et al. 2009). "
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    ABSTRACT: What mechanisms underlie aging? One theory, the wear-and-tear model, attributes aging to progressive deterioration in the molecular and cellular machinery which eventually lead to death through the disruption of physiological homeostasis. The second suggests that life span is genetically programmed, and aging may be derived from intrinsic processes which enforce a non-random, terminal time interval for the survivability of the organism. We are studying an organism that demonstrates both properties: the colonial ascidian, Botryllus schlosseri. Botryllus is a member of the Tunicata, the sister group to the vertebrates, and has a number of life history traits which make it an excellent model for studies on aging. First, Botryllus has a colonial life history, and grows by a process of asexual reproduction during which entire bodies, including all somatic and germline lineages, regenerate every week, resulting in a colony of genetically identical individuals. Second, previous studies of lifespan in genetically distinct Botryllus lineages suggest that a direct, heritable basis underlying mortality exists that is unlinked to reproductive effort and other life history traits. Here we will review recent efforts to take advantage of the unique life history traits of B. schlosseri and develop it into a robust model for aging research.
    Full-text · Article · Jan 2015 · Invertebrate Reproduction and Development
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    • "This phenomenon, known as parasitism, can be replicated by manually transplanting a FACS-isolated population of cells high in aldehyde dehydrogenase activity, a biomarker for stem cells in vertebrates (Kastan et al., 1990; Laird et al., 2005). Winner and loser phenotypes are hierarchical and heritable, suggesting that the ability of one colony to successfully parasitize another is likely to be genetically encoded (Stoner et al., 1999). The properties of parasitism and allorecognition make B. schlosseri an excellent model for addressing questions in the fields of immunology, stem cell biology, regeneration, and evolutionary biology. "
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    ABSTRACT: Botryllus schlosseri is a colonial ascidian with characteristics that make it an attractive model for studying immunology, stem cell biology, evolutionary biology, and regeneration. Transcriptome sequencing and the recent completion of a draft genome sequence for B. schlosseri have revealed a large number of genes, both with and without vertebrate homologs, but analyzing the spatial and temporal expression of these genes in situ has remained a challenge. Here we report a robust protocol for in situ hybridization that enables the simultaneous detection of multiple transcripts in whole adult B. schlosseri using Tyramide Signal Amplification in conjunction with digoxigenin- and dinitrophenol-labeled RNA probes. Using this protocol we have identified a number of genes that can serve as markers for developing and mature structures in B. schlosseri, permitting analysis of phenotypes induced in loss-of-function experiments. © 2014 Wiley Periodicals, Inc.
    Full-text · Article · Sep 2014 · genesis
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    • "Conversely, easy access to an ontology illustrating asexual reproduction and valorised by a well-characterized description of the anatomy and development of budding will be an important resource for the study of the nature of the asexual reproduction in B. schlosseri. B. schlosseri has the recognized potential to facilitate basic research on stem cells [11], [13], [24], [25], [30], [32], and can provide insights on the evolution, and loss, of regenerative abilities in vertebrates. At the moment, migrating cells belonging to ventral cell islands represent a good candidate to explore these hypothesis [11], [13], [25], [30]. "
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    ABSTRACT: Ontologies provide an important resource to integrate information. For developmental biology and comparative anatomy studies, ontologies of a species are used to formalize and annotate data that are related to anatomical structures, their lineage and timing of development. Here, we have constructed the first ontology for anatomy and asexual development (blastogenesis) of a bilaterian, the colonial tunicate Botryllus schlosseri. Tunicates, like Botryllus schlosseri, are non-vertebrates and the only chordate taxon species that reproduce both sexually and asexually. Their tadpole larval stage possesses structures characteristic of all chordates, i.e. a notochord, a dorsal neural tube, and gill slits. Larvae settle and metamorphose into individuals that are either solitary or colonial. The latter reproduce both sexually and asexually and these two reproductive modes lead to essentially the same adult body plan. The Botryllus schlosseri Ontology of Development and Anatomy (BODA) will facilitate the comparison between both types of development. BODA uses the rules defined by the Open Biomedical Ontologies Foundry. It is based on studies that investigate the anatomy, blastogenesis and regeneration of this organism. BODA features allow the users to easily search and identify anatomical structures in the colony, to define the developmental stage, and to follow the morphogenetic events of a tissue and/or organ of interest throughout asexual development. We invite the scientific community to use this resource as a reference for the anatomy and developmental ontology of B. schlosseri and encourage recommendations for updates and improvements.
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