Cargando…
Gene expression patterns that support novel developmental stress buffering in embryos of the annual killifish Austrofundulus limnaeus
BACKGROUND: The cellular signaling mechanisms and morphogenic movements involved in axis formation and gastrulation are well conserved between vertebrates. In nearly all described fish, gastrulation and the initial patterning of the embryonic axis occur concurrently with epiboly. However, annual kil...
Autores principales: | , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2015
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4372997/ https://www.ncbi.nlm.nih.gov/pubmed/25810897 http://dx.doi.org/10.1186/2041-9139-6-2 |
_version_ | 1782363271388463104 |
---|---|
author | Wagner, Josiah T Podrabsky, Jason E |
author_facet | Wagner, Josiah T Podrabsky, Jason E |
author_sort | Wagner, Josiah T |
collection | PubMed |
description | BACKGROUND: The cellular signaling mechanisms and morphogenic movements involved in axis formation and gastrulation are well conserved between vertebrates. In nearly all described fish, gastrulation and the initial patterning of the embryonic axis occur concurrently with epiboly. However, annual killifish may be an exception to this norm. Annual killifish inhabit ephemeral ponds in South America and Africa and permanent populations persist by the production of stress-tolerant eggs. Early development of annual killifish is unique among vertebrates because their embryonic blastomeres disperse randomly across the yolk during epiboly and reaggregate several days later to form the embryo proper. In addition, annual killifish are able to arrest embryonic development in one to three stages, known as diapause I, II, and III. Little is known about how the highly conserved developmental signaling mechanisms associated with early vertebrate development may have shifted in order to promote the annual killifish phenotype. One of the most well-characterized and conserved transcription factors, oct4 (Pou5f1), may have a role in maintaining pluripotency. In contrast, BMP-antagonists such as chordin, noggin, and follistatin, have been previously shown to establish dorsal-ventral asymmetry during axis formation. Transcription factors from the SOXB1 group, such as sox2 and sox3, likely work to induce neural specification. Here, we determine the temporal expression of these developmental factors during embryonic development in the annual killifish Austrofundulus limnaeus using quantitative PCR and compare these patterns to other vertebrates. RESULTS: Partial transcript sequences to oct4, sox2, sox3, chordin, noggin-1, noggin-2, and follistatin were cloned, sequenced, and identified in A. limnaeus. We found oct4, sox3, chordin, and noggin-1 transcripts to likely be maternally inherited. Expression of sox2, follistatin, and noggin-2 transcripts were highest in stages following a visible embryonic axis. CONCLUSIONS: Our data suggest that embryonic cells acquire their germ layer identity following embryonic blastomere reaggregation in A. limnaeus. This process of cellular differentiation and axis formation may involve similar conserved signaling mechanisms to other vertebrates. We propose that the undifferentiated state is prolonged during blastomere dispersal, thus functioning as a developmental stress buffer prior to the establishment of embryonic asymmetry and positional identity among the embryonic cells. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/2041-9139-6-2) contains supplementary material, which is available to authorized users. |
format | Online Article Text |
id | pubmed-4372997 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2015 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-43729972015-03-26 Gene expression patterns that support novel developmental stress buffering in embryos of the annual killifish Austrofundulus limnaeus Wagner, Josiah T Podrabsky, Jason E EvoDevo Research BACKGROUND: The cellular signaling mechanisms and morphogenic movements involved in axis formation and gastrulation are well conserved between vertebrates. In nearly all described fish, gastrulation and the initial patterning of the embryonic axis occur concurrently with epiboly. However, annual killifish may be an exception to this norm. Annual killifish inhabit ephemeral ponds in South America and Africa and permanent populations persist by the production of stress-tolerant eggs. Early development of annual killifish is unique among vertebrates because their embryonic blastomeres disperse randomly across the yolk during epiboly and reaggregate several days later to form the embryo proper. In addition, annual killifish are able to arrest embryonic development in one to three stages, known as diapause I, II, and III. Little is known about how the highly conserved developmental signaling mechanisms associated with early vertebrate development may have shifted in order to promote the annual killifish phenotype. One of the most well-characterized and conserved transcription factors, oct4 (Pou5f1), may have a role in maintaining pluripotency. In contrast, BMP-antagonists such as chordin, noggin, and follistatin, have been previously shown to establish dorsal-ventral asymmetry during axis formation. Transcription factors from the SOXB1 group, such as sox2 and sox3, likely work to induce neural specification. Here, we determine the temporal expression of these developmental factors during embryonic development in the annual killifish Austrofundulus limnaeus using quantitative PCR and compare these patterns to other vertebrates. RESULTS: Partial transcript sequences to oct4, sox2, sox3, chordin, noggin-1, noggin-2, and follistatin were cloned, sequenced, and identified in A. limnaeus. We found oct4, sox3, chordin, and noggin-1 transcripts to likely be maternally inherited. Expression of sox2, follistatin, and noggin-2 transcripts were highest in stages following a visible embryonic axis. CONCLUSIONS: Our data suggest that embryonic cells acquire their germ layer identity following embryonic blastomere reaggregation in A. limnaeus. This process of cellular differentiation and axis formation may involve similar conserved signaling mechanisms to other vertebrates. We propose that the undifferentiated state is prolonged during blastomere dispersal, thus functioning as a developmental stress buffer prior to the establishment of embryonic asymmetry and positional identity among the embryonic cells. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/2041-9139-6-2) contains supplementary material, which is available to authorized users. BioMed Central 2015-01-21 /pmc/articles/PMC4372997/ /pubmed/25810897 http://dx.doi.org/10.1186/2041-9139-6-2 Text en © Wagner and Podrabsky; licensee BioMed Central. 2015 This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. |
spellingShingle | Research Wagner, Josiah T Podrabsky, Jason E Gene expression patterns that support novel developmental stress buffering in embryos of the annual killifish Austrofundulus limnaeus |
title | Gene expression patterns that support novel developmental stress buffering in embryos of the annual killifish Austrofundulus limnaeus |
title_full | Gene expression patterns that support novel developmental stress buffering in embryos of the annual killifish Austrofundulus limnaeus |
title_fullStr | Gene expression patterns that support novel developmental stress buffering in embryos of the annual killifish Austrofundulus limnaeus |
title_full_unstemmed | Gene expression patterns that support novel developmental stress buffering in embryos of the annual killifish Austrofundulus limnaeus |
title_short | Gene expression patterns that support novel developmental stress buffering in embryos of the annual killifish Austrofundulus limnaeus |
title_sort | gene expression patterns that support novel developmental stress buffering in embryos of the annual killifish austrofundulus limnaeus |
topic | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4372997/ https://www.ncbi.nlm.nih.gov/pubmed/25810897 http://dx.doi.org/10.1186/2041-9139-6-2 |
work_keys_str_mv | AT wagnerjosiaht geneexpressionpatternsthatsupportnoveldevelopmentalstressbufferinginembryosoftheannualkillifishaustrofunduluslimnaeus AT podrabskyjasone geneexpressionpatternsthatsupportnoveldevelopmentalstressbufferinginembryosoftheannualkillifishaustrofunduluslimnaeus |