Double maternal-effect: duplicated nucleoplasmin 2 genes, npm2a and npm2b, with essential but distinct functions are shared by fish and tetrapods
Abstract Background Nucleoplasmin 2 (npm2) is an essential maternal-effect gene that mediates early embryonic events through its function as a histone chaperone that remodels chromatin. Recently, two npm2 (npm2a and npm2b) genes have been annotated in zebrafish. Thus, we examined the evolution of np...
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doaj-02787d2141484607a77c8e2f3e1daed62021-09-02T06:02:15ZengBMCBMC Evolutionary Biology1471-21482018-11-0118111610.1186/s12862-018-1281-3Double maternal-effect: duplicated nucleoplasmin 2 genes, npm2a and npm2b, with essential but distinct functions are shared by fish and tetrapodsCaroline T. Cheung0Jérémy Pasquier1Aurélien Bouleau2Thaovi Nguyen3Franck Chesnel4Yann Guiguen5Julien Bobe6INRA LPGP UR1037INRA LPGP UR1037INRA LPGP UR1037INRA LPGP UR1037CNRS/UMR6290, Université de Rennes 1INRA LPGP UR1037INRA LPGP UR1037Abstract Background Nucleoplasmin 2 (npm2) is an essential maternal-effect gene that mediates early embryonic events through its function as a histone chaperone that remodels chromatin. Recently, two npm2 (npm2a and npm2b) genes have been annotated in zebrafish. Thus, we examined the evolution of npm2a and npm2b in a variety of vertebrates, their potential phylogenetic relationships, and their biological functions using knockout models via the CRISPR/cas9 system. Results We demonstrated that the two npm2 duplicates exist in a wide range of vertebrates, including sharks, ray-finned fish, amphibians, and sauropsids, while npm2a was lost in coelacanth and mammals, as well as some specific teleost lineages. Using phylogeny and synteny analyses, we traced their origins to the early stages of vertebrate evolution. Our findings suggested that npm2a and npm2b resulted from an ancient local gene duplication, and their functions diverged although key protein domains were conserved. We then investigated their functions by examining their tissue distribution in a wide variety of species and found that they shared ovarian-specific expression, a key feature of maternal-effect genes. We also demonstrated that both npm2a and npm2b are maternally-inherited transcripts in vertebrates, and that they play essential, but distinct, roles in early embryogenesis using zebrafish knockout models. Both npm2a and npm2b function early during oogenesis and may play a role in cortical granule function that impact egg activation and fertilization, while npm2b is also involved in early embryogenesis. Conclusion These novel findings will broaden our knowledge on the evolutionary history of maternal-effect genes and underlying mechanisms that contribute to vertebrate reproductive success. In addition, our results demonstrate the existence of a newly described maternal-effect gene, npm2a, that contributes to egg competence, an area that still requires further comprehension.http://link.springer.com/article/10.1186/s12862-018-1281-3npm2VertebratesEvolutionMaternal-effect genesCRISPR-cas9 knockout |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Caroline T. Cheung Jérémy Pasquier Aurélien Bouleau Thaovi Nguyen Franck Chesnel Yann Guiguen Julien Bobe |
spellingShingle |
Caroline T. Cheung Jérémy Pasquier Aurélien Bouleau Thaovi Nguyen Franck Chesnel Yann Guiguen Julien Bobe Double maternal-effect: duplicated nucleoplasmin 2 genes, npm2a and npm2b, with essential but distinct functions are shared by fish and tetrapods BMC Evolutionary Biology npm2 Vertebrates Evolution Maternal-effect genes CRISPR-cas9 knockout |
author_facet |
Caroline T. Cheung Jérémy Pasquier Aurélien Bouleau Thaovi Nguyen Franck Chesnel Yann Guiguen Julien Bobe |
author_sort |
Caroline T. Cheung |
title |
Double maternal-effect: duplicated nucleoplasmin 2 genes, npm2a and npm2b, with essential but distinct functions are shared by fish and tetrapods |
title_short |
Double maternal-effect: duplicated nucleoplasmin 2 genes, npm2a and npm2b, with essential but distinct functions are shared by fish and tetrapods |
title_full |
Double maternal-effect: duplicated nucleoplasmin 2 genes, npm2a and npm2b, with essential but distinct functions are shared by fish and tetrapods |
title_fullStr |
Double maternal-effect: duplicated nucleoplasmin 2 genes, npm2a and npm2b, with essential but distinct functions are shared by fish and tetrapods |
title_full_unstemmed |
Double maternal-effect: duplicated nucleoplasmin 2 genes, npm2a and npm2b, with essential but distinct functions are shared by fish and tetrapods |
title_sort |
double maternal-effect: duplicated nucleoplasmin 2 genes, npm2a and npm2b, with essential but distinct functions are shared by fish and tetrapods |
publisher |
BMC |
series |
BMC Evolutionary Biology |
issn |
1471-2148 |
publishDate |
2018-11-01 |
description |
Abstract Background Nucleoplasmin 2 (npm2) is an essential maternal-effect gene that mediates early embryonic events through its function as a histone chaperone that remodels chromatin. Recently, two npm2 (npm2a and npm2b) genes have been annotated in zebrafish. Thus, we examined the evolution of npm2a and npm2b in a variety of vertebrates, their potential phylogenetic relationships, and their biological functions using knockout models via the CRISPR/cas9 system. Results We demonstrated that the two npm2 duplicates exist in a wide range of vertebrates, including sharks, ray-finned fish, amphibians, and sauropsids, while npm2a was lost in coelacanth and mammals, as well as some specific teleost lineages. Using phylogeny and synteny analyses, we traced their origins to the early stages of vertebrate evolution. Our findings suggested that npm2a and npm2b resulted from an ancient local gene duplication, and their functions diverged although key protein domains were conserved. We then investigated their functions by examining their tissue distribution in a wide variety of species and found that they shared ovarian-specific expression, a key feature of maternal-effect genes. We also demonstrated that both npm2a and npm2b are maternally-inherited transcripts in vertebrates, and that they play essential, but distinct, roles in early embryogenesis using zebrafish knockout models. Both npm2a and npm2b function early during oogenesis and may play a role in cortical granule function that impact egg activation and fertilization, while npm2b is also involved in early embryogenesis. Conclusion These novel findings will broaden our knowledge on the evolutionary history of maternal-effect genes and underlying mechanisms that contribute to vertebrate reproductive success. In addition, our results demonstrate the existence of a newly described maternal-effect gene, npm2a, that contributes to egg competence, an area that still requires further comprehension. |
topic |
npm2 Vertebrates Evolution Maternal-effect genes CRISPR-cas9 knockout |
url |
http://link.springer.com/article/10.1186/s12862-018-1281-3 |
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