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: 9.81). 09/1999; 96(16):9148-53. DOI: 10.1073/pnas.96.16.9148
Source: PubMed

ABSTRACT 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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    • "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.
    genesis 09/2014; 53(1). DOI:10.1002/dvg.22820 · 2.04 Impact Factor
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    • "Botrillinae ascidians have the ability to fuse and to form chimeras under the influence of an allorecognition locus (Stoner and Weissman, 1996). Germline stem cells of 'winner' genotypes have been documented to parasitize all gonads of two partner chimeras, even though somatic zooids of both 'winner' and 'loser' genotypes may propagate indefinitely (Grosberg and Quinn, 1986; Sabbadin and Zaniolo, 1979; Stoner et al., 1999). We have also shown germline parasitism of colonies that do not yet contain mature gonads, thus providing evidence for an early specification of long-lived germline precursors in Botryllus schlosseri (Brown et al., 2009b). "
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    ABSTRACT: The evolution of budding in metazoans is not well understood on a mechanistic level, but is an important developmental process. We examine the evolution of coloniality in ascidians, contrasting the life histories of solitary and colonial forms with a focus on the cellular and developmental basis of the evolution of budding. Tunicates are an excellent group to study colonial transitions, as all solitary larvae develop with determinant and invariant cleavage patterns, but colonial species show robust developmental flexibility during larval development. We propose that acquiring new stem cell lineages in the larvae may be a preadaptation necessary for the evolution of budding. Brooding in colonial ascidians allows increased egg size, which in turn allows greater flexibility in the specification of cells and cell numbers in late embryonic and pre-metamorphic larval stages. We review hypotheses for changes in stem cell lineages in colonial species, describe what the current data suggest about the evolution of budding, and discuss where we believe further studies will be most fruitful.
    Developmental Biology 06/2012; 369(2):151-62. DOI:10.1016/j.ydbio.2012.05.038 · 3.64 Impact Factor
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    • "Fusion of the vascular systems of colonies in ascidian B. schlosseri can lead to the replacement of germ and somatic cells in one colony with those from another one (Pancer et al., 1995; Stoner & Weissman, 1996; Stoner et al., 1999; Weissman, 2000; Laird et al., 2005). It remains unclear if the germline and somatic lineages are segregated or they descend from the same initial stem cell population in botryllids (Stoner et al., 1999). Pluripotent embryonic stem cells of mammals have capability to differentiate in vitro into female and male germ cells (Hübner et al., 2003; Geijsen et al., 2003; Toyooka et al., 2003; Clark et al., 2004; Daley, 2007; Kerkis et al., 2007). "
    Embryonic Stem Cells - Basic Biology to Bioengineering, 09/2011; , ISBN: 978-953-307-278-4
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