Deficient induction response in a Xenopus nucleocytoplasmic hybrid.

Incompatibilities between the nucleus and the cytoplasm of sufficiently distant species result in developmental arrest of hybrid and nucleocytoplasmic hybrid (cybrid) embryos. Several hypotheses have been proposed to explain their lethality, including problems in embryonic genome activation (EGA) an...

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Autores principales:	Patrick Narbonne, David E Simpson, John B Gurdon
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2011
Materias:	Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/0d3a4e9484934e51af03556f98f329a0
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spelling	oai:doaj.org-article:0d3a4e9484934e51af03556f98f329a02021-11-18T05:36:53ZDeficient induction response in a Xenopus nucleocytoplasmic hybrid.1544-91731545-788510.1371/journal.pbio.1001197https://doaj.org/article/0d3a4e9484934e51af03556f98f329a02011-11-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/22131902/?tool=EBIhttps://doaj.org/toc/1544-9173https://doaj.org/toc/1545-7885Incompatibilities between the nucleus and the cytoplasm of sufficiently distant species result in developmental arrest of hybrid and nucleocytoplasmic hybrid (cybrid) embryos. Several hypotheses have been proposed to explain their lethality, including problems in embryonic genome activation (EGA) and/or nucleo-mitochondrial interactions. However, conclusive identification of the causes underlying developmental defects of cybrid embryos is still lacking. We show here that while over 80% of both Xenopus laevis and Xenopus (Silurana) tropicalis same-species androgenetic haploids develop to the swimming tadpole stage, the androgenetic cybrids formed by the combination of X. laevis egg cytoplasm and X. tropicalis sperm nucleus invariably fail to gastrulate properly and never reach the swimming tadpole stage. In spite of this arrest, these cybrids show quantitatively normal EGA and energy levels at the stage where their initial gastrulation defects are manifested. The nucleocytoplasmic incompatibility between these two species instead results from a combination of factors, including a reduced emission of induction signal from the vegetal half, a decreased sensitivity of animal cells to induction signals, and differences in a key embryonic protein (Xbra) concentration between the two species, together leading to inefficient induction and defective convergence-extension during gastrulation. Indeed, increased exposure to induction signals and/or Xbra signalling partially rescues the induction response in animal explants and whole cybrid embryos. Altogether, our study demonstrates that the egg cytoplasm of one species may not support the development promoted by the nucleus of another species, even if this nucleus does not interfere with the cytoplasmic/maternal functions of the egg, while the egg cytoplasm is also capable of activating the genome of that nucleus. Instead, our results provide evidence that inefficient signalling and differences in the concentrations of key proteins between species lead to developmental defects in cybrids. Finally, they show that the incompatibilities of cybrids can be corrected by appropriate treatments.Patrick NarbonneDavid E SimpsonJohn B GurdonPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Biology, Vol 9, Iss 11, p e1001197 (2011)
institution	DOAJ
collection	DOAJ
language	EN
topic	Biology (General) QH301-705.5
spellingShingle	Biology (General) QH301-705.5 Patrick Narbonne David E Simpson John B Gurdon Deficient induction response in a Xenopus nucleocytoplasmic hybrid.
description	Incompatibilities between the nucleus and the cytoplasm of sufficiently distant species result in developmental arrest of hybrid and nucleocytoplasmic hybrid (cybrid) embryos. Several hypotheses have been proposed to explain their lethality, including problems in embryonic genome activation (EGA) and/or nucleo-mitochondrial interactions. However, conclusive identification of the causes underlying developmental defects of cybrid embryos is still lacking. We show here that while over 80% of both Xenopus laevis and Xenopus (Silurana) tropicalis same-species androgenetic haploids develop to the swimming tadpole stage, the androgenetic cybrids formed by the combination of X. laevis egg cytoplasm and X. tropicalis sperm nucleus invariably fail to gastrulate properly and never reach the swimming tadpole stage. In spite of this arrest, these cybrids show quantitatively normal EGA and energy levels at the stage where their initial gastrulation defects are manifested. The nucleocytoplasmic incompatibility between these two species instead results from a combination of factors, including a reduced emission of induction signal from the vegetal half, a decreased sensitivity of animal cells to induction signals, and differences in a key embryonic protein (Xbra) concentration between the two species, together leading to inefficient induction and defective convergence-extension during gastrulation. Indeed, increased exposure to induction signals and/or Xbra signalling partially rescues the induction response in animal explants and whole cybrid embryos. Altogether, our study demonstrates that the egg cytoplasm of one species may not support the development promoted by the nucleus of another species, even if this nucleus does not interfere with the cytoplasmic/maternal functions of the egg, while the egg cytoplasm is also capable of activating the genome of that nucleus. Instead, our results provide evidence that inefficient signalling and differences in the concentrations of key proteins between species lead to developmental defects in cybrids. Finally, they show that the incompatibilities of cybrids can be corrected by appropriate treatments.
format	article
author	Patrick Narbonne David E Simpson John B Gurdon
author_facet	Patrick Narbonne David E Simpson John B Gurdon
author_sort	Patrick Narbonne
title	Deficient induction response in a Xenopus nucleocytoplasmic hybrid.
title_short	Deficient induction response in a Xenopus nucleocytoplasmic hybrid.
title_full	Deficient induction response in a Xenopus nucleocytoplasmic hybrid.
title_fullStr	Deficient induction response in a Xenopus nucleocytoplasmic hybrid.
title_full_unstemmed	Deficient induction response in a Xenopus nucleocytoplasmic hybrid.
title_sort	deficient induction response in a xenopus nucleocytoplasmic hybrid.
publisher	Public Library of Science (PLoS)
publishDate	2011
url	https://doaj.org/article/0d3a4e9484934e51af03556f98f329a0
work_keys_str_mv	AT patricknarbonne deficientinductionresponseinaxenopusnucleocytoplasmichybrid AT davidesimpson deficientinductionresponseinaxenopusnucleocytoplasmichybrid AT johnbgurdon deficientinductionresponseinaxenopusnucleocytoplasmichybrid
_version_	1718424832826146816

Deficient induction response in a Xenopus nucleocytoplasmic hybrid.

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