Repression of zygotic gene expression in the<i>Xenopus</i>germline

Venkatarama, Thiagarajan; Lai, Fangfang; Luo, Xueting; Yi, Zili; Newman, K M; King, Mary Lou

doi:10.1242/dev.038554

Cited by 67 publications

(108 citation statements)

References 75 publications

(89 reference statements)

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“…3 B-N and Fig. S5 A-C), as reported (21,22). The germ plasm was identified by its enrichment in mitochondria, besides the localization of vegt transcripts and protein (Fig.…”

Section: Resultssupporting

confidence: 69%

Transcription factors Mix1 and VegT, relocalization of vegt mRNA, and conserved endoderm and dorsal specification in frogs

Sudou

Garcés-Vásconez

López-Latorre

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Protein expression of the transcription factor genes mix1 and vegt characterized the presumptive endoderm in embryos of the frogs Engystomops randi, Epipedobates machalilla, Gastrotheca riobambae, and Eleutherodactylus coqui, as in Xenopus laevis embryos. Protein VegT was detected in the animal hemisphere of the early blastula in all frogs, and only the animal pole was VegT-negative. This finding stimulated a vegt mRNA analysis in X. laevis eggs and embryos. vegt mRNA was detected in the animal region of X. laevis eggs and early embryos, in agreement with the VegT localization observed in the analyzed frogs. Moreover, a dorso-animal relocalization of vegt mRNA occurred in the egg at fertilization. Thus, the comparative analysis indicated that vegt may participate in dorsal development besides its known roles in endoderm development, and germlayer specification. Zygotic vegt (zvegt) mRNA was detected as a minor isoform besides the major maternal (mvegt) isoform of the X. laevis egg. In addition, α-amanitin-insensitive vegt transcripts were detected around vegetal nuclei of the blastula. Thus, accumulation of vegt mRNA around vegetal nuclei was caused by relocalization rather than new mRNA synthesis. The localization of vegt mRNA around vegetal nuclei may contribute to the identity of vegetal blastomeres. These and previously reportedly localization features of vegt mRNA and protein derive from the master role of vegt in the development of frogs. The comparative analysis indicated that the strategies for endoderm, and dorsal specification, involving vegt and mix1, have been evolutionary conserved in frogs.mvegt | zvegt | germ plasm | blastula | gastrula

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“…3 B-N and Fig. S5 A-C), as reported (21,22). The germ plasm was identified by its enrichment in mitochondria, besides the localization of vegt transcripts and protein (Fig.…”

Section: Resultssupporting

confidence: 69%

Transcription factors Mix1 and VegT, relocalization of vegt mRNA, and conserved endoderm and dorsal specification in frogs

Sudou

Garcés-Vásconez

López-Latorre

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…Using isolated PGCs as a point of entry, Venkatarama et al (2010) showed that transcriptional activity in Xenopus PGCs is repressed, relative to somatic cells, from mid-blastula through neurula stages, coinciding with the interval during which somatic germ layers are specified. Consequently, as in Caenorhabditis elegans and Drosophila, transcriptional repression prevents specification of the nascent germ line to a somatic fate.…”

Section: Preformationmentioning

confidence: 99%

“…As a result, the PGC progenitors must repress the cell-autonomous effects of maternally encoded transcription factors, in addition to repressing the response to external stimuli. For example, in Xenopus embryos, germ plasm counters the potential effects of VegT, which is an endodermal determinant whose RNA is also localized to the vegetal hemisphere and inherited by the PGCs (Venkatarama et al 2010). However, VegT is not localized in oocytes of axolotls (Nath & Elinson 2007), or even basal species of fish (H Chen, M Loose and A D Johnson, unpublished observations), raising the possibility that the evolution of germ plasm, generally, is a precondition for the evolution of a mosaic distribution of somatic determinants.…”

Section: Preformationmentioning

confidence: 99%

“…Though it is not conserved, the germ plasm of vertebrates and invertebrates accomplishes the same task; it inhibits the transcriptional apparatus of nascent germ cells, rendering them transcriptionally unresponsive to somatic inducing signals (Nakamura & Seydoux 2008, Venkatarama et al 2010. Transcription is inhibited during the period in which lineage specification is underway, and as a consequence, nascent germ cells avoid being diverted to a somatic fate.…”

Section: Introductionmentioning

confidence: 99%

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Evolution of the germ line–soma relationship in vertebrate embryos

Johnson¹,

Richardson²,

Bachvarova³

et al. 2011

Reproduction

111

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The germ line and soma together maintain genetic lineages from generation to generation: the germ line passes genetic information between generations; the soma is the vehicle for germ line transmission, and is shaped by natural selection. The germ line and somatic lineages arise simultaneously in early embryos, but how their development is related depends on how primordial germ cells (PGC) are specified. PGCs are specified by one of two means. Epigenesis describes the induction of PGCs from pluripotent cells by signals from surrounding somatic tissues. In contrast, PGCs in many species are specified cell-autonomously by maternally derived molecules, known as germ plasm, and this is called preformation. Germ plasm inhibits signaling to PGCs; thus, they are specified cell-autonomously. Germ plasm evolved independently in many animal lineages, suggesting convergent evolution, and therefore it would be expected to convey a selective advantage. But, what this is remains unknown. We propose that the selective advantage that drives the emergence of germ plasm in vertebrates is the disengagement of germ line specification from somatic influences. This liberates the evolution of gene regulatory networks (GRNs) that govern somatic development, and thereby enhances species evolvability, a well-recognized selective advantage. We cite recent evidence showing that frog embryos, which contain germ plasm, have modified GRNs that are not conserved in axolotls, which represent more basal amphibians and employ epigenesis. We also present the correlation of preformation with enhanced species radiations, and we discuss the mutually exclusive trajectories influenced by germ plasm or pluripotency, which shaped chordate evolution.

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“…Stable integration frequencies were improved 20-fold by incorporation of an attB site in the transgene plasmid and expression of ϕC31 integrase to promote chromosomal integration (8). The apparently low frequencies of stable integration may be due to transcriptional repression of the integrated transgenes by the genome-wide epigenetic modifications present in the PGCs of many organisms (9)(10)(11)(12).…”

mentioning

confidence: 99%

Efficient genetic modification and germ-line transmission of primordial germ cells using piggyBac and Tol2 transposons

Macdonald

Taylor

Sherman

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

154

127

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The derivation of germ-line competent avian primordial germ cells establishes a cell-based model system for the investigation of germ cell differentiation and the production of genetically modified animals. Current methods to modify primordial germ cells using DNA or retroviral vectors are inefficient and prone to epigenetic silencing. Here, we validate the use of transposable elements for the genetic manipulation of primordial germ cells. We demonstrate that chicken primordial germ cells can be modified in vitro using transposable elements. Both piggyBac and Tol2 transposons efficiently transpose primordial germ cells. Tol2 transposon integration sites were spread throughout both the macro-and microchromosomes of the chicken genome and were more prevalent in gene transcriptional units and intronic regions, consistent with transposon integrations observed in other species. We determined that the presence of insulator elements was not required for reporter gene expression from the integrated transposon. We further demonstrate that a gene-trap cassette carried in the Tol2 transposon can trap and mutate endogenous transcripts in primordial germ cells. Finally, we observed that modified primordial germ cells form functional gametes as demonstrated by the generation of transgenic offspring that correctly expressed a reporter gene carried in the transposon. Transposable elements are therefore efficient vectors for the genetic manipulation of primordial germ cells and the chicken genome.poultry | transgenesis | transposition P rimordial germ cells (PGCs) are specified in the early embryo and are the lineage-restricted stem cells for the germ cell population. In the chicken, segregation of PGCs from somatic cells occurs during the early stages of blastoderm formation (1-3). These cells accumulate in the germinal crescent region anterior to the forming head at day 1 of incubation [stage 4 Hamburger and Hamilton (HH)] and subsequently migrate via the circulatory system to the forming gonads on day 3 of incubation (stage 15 HH) (4). Chicken PGCs can be isolated from embryonic blood at this developmental stage and propagated indefinitely in culture (5). When returned to the circulatory system of an equivalent stage host embryo, the cultured PGCs migrated to and populated the forming embryonic gonad. Breeding from the resulting germline chimeras demonstrated that the cultured PGCs formed functional gametes by production of offspring derived from these cells. Germ-line transmission of cultured PGCs has now been demonstrated for three different chicken breeds (5-7).This in vitro system for the long-term propagation of chicken PGCs is the basis of a unique stem cell model for both the investigation of germ cell differentiation and the generation of genetically modified chickens. Thus far, chicken PGCs have proved highly resistant to genetic modification. Stable transfection of PGCs has been achieved by electroporation of plasmid DNA, at a frequency of ∼1 in 10 6 , but expression from integrated reporter constructs depended on t...

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Repression of zygotic gene expression in theXenopusgermline

Cited by 67 publications

References 75 publications

Transcription factors Mix1 and VegT, relocalization of vegt mRNA, and conserved endoderm and dorsal specification in frogs

Transcription factors Mix1 and VegT, relocalization of vegt mRNA, and conserved endoderm and dorsal specification in frogs

Evolution of the germ line–soma relationship in vertebrate embryos

Efficient genetic modification and germ-line transmission of primordial germ cells using piggyBac and Tol2 transposons

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