Cargando…
Toll signals regulate dorsal–ventral patterning and anterior–posterior placement of the embryo in the hemipteran Rhodnius prolixus
BACKGROUND: Insect embryonic dorso-ventral patterning depends greatly on two pathways: the Toll pathway and the Bone Morphogenetic Protein pathway. While the relative contribution of each pathway has been investigated in holometabolous insects, their role has not been explored in insects with a hemi...
Autores principales: | , , , , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2014
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4407881/ https://www.ncbi.nlm.nih.gov/pubmed/25908955 http://dx.doi.org/10.1186/2041-9139-5-38 |
_version_ | 1782367976026013696 |
---|---|
author | Berni, Mateus Fontenele, Marcio Ribeiro Tobias-Santos, Vitoria Caceres-Rodrigues, Aline Mury, Flavia Borges Vionette-do-Amaral, Raquel Masuda, Hatisaburo Sorgine, Marcos da Fonseca, Rodrigo Nunes Araujo, Helena |
author_facet | Berni, Mateus Fontenele, Marcio Ribeiro Tobias-Santos, Vitoria Caceres-Rodrigues, Aline Mury, Flavia Borges Vionette-do-Amaral, Raquel Masuda, Hatisaburo Sorgine, Marcos da Fonseca, Rodrigo Nunes Araujo, Helena |
author_sort | Berni, Mateus |
collection | PubMed |
description | BACKGROUND: Insect embryonic dorso-ventral patterning depends greatly on two pathways: the Toll pathway and the Bone Morphogenetic Protein pathway. While the relative contribution of each pathway has been investigated in holometabolous insects, their role has not been explored in insects with a hemimetabolous type of development. The hemimetabolous insect Rhodnius prolixus, an important vector of Chagas disease in the Americas, develops from an intermediate germ band and displays complex movements during katatrepsis that are not observed in other orders. However, little is known about the molecular events that regulate its embryogenesis. Here we investigate the expression and function of genes potentially involved in the initial patterning events that establish the embryonic dorso-ventral axis in this hemipteran. RESULTS: We establish a staging system for early embryogenesis that allows us to correlate embryo morphology with gene expression profiles. Using this system, we investigate the role of Toll pathway genes during embryogenesis. Detailed analyses of gene expression throughout development, coupled with functional analyses using parental RNA interference, revealed that maternal Toll is required to establish germ layers along the dorso-ventral axis and for embryo placement along the anterior-posterior axis. Interestingly, knockdown of the Toll pathway effector Rp-dorsal appears to regulate the expression of the Bone Morphogenetic Protein antagonist Rp-short-gastrulation. CONCLUSIONS: Our results indicate that Toll signals are the initiating event in dorso-ventral patterning during Rhodnius embryogenesis, and this is the first report of a conserved role for Toll in a hemipteran. Furthermore, as Rp-dorsal RNA interference generates anteriorly misplaced embryos, our results indicate a novel role for Toll signals in establishment of the anterior-posterior axis in Rhodnius. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/2041-9139-5-38) contains supplementary material, which is available to authorized users. |
format | Online Article Text |
id | pubmed-4407881 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2014 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-44078812015-04-24 Toll signals regulate dorsal–ventral patterning and anterior–posterior placement of the embryo in the hemipteran Rhodnius prolixus Berni, Mateus Fontenele, Marcio Ribeiro Tobias-Santos, Vitoria Caceres-Rodrigues, Aline Mury, Flavia Borges Vionette-do-Amaral, Raquel Masuda, Hatisaburo Sorgine, Marcos da Fonseca, Rodrigo Nunes Araujo, Helena EvoDevo Research BACKGROUND: Insect embryonic dorso-ventral patterning depends greatly on two pathways: the Toll pathway and the Bone Morphogenetic Protein pathway. While the relative contribution of each pathway has been investigated in holometabolous insects, their role has not been explored in insects with a hemimetabolous type of development. The hemimetabolous insect Rhodnius prolixus, an important vector of Chagas disease in the Americas, develops from an intermediate germ band and displays complex movements during katatrepsis that are not observed in other orders. However, little is known about the molecular events that regulate its embryogenesis. Here we investigate the expression and function of genes potentially involved in the initial patterning events that establish the embryonic dorso-ventral axis in this hemipteran. RESULTS: We establish a staging system for early embryogenesis that allows us to correlate embryo morphology with gene expression profiles. Using this system, we investigate the role of Toll pathway genes during embryogenesis. Detailed analyses of gene expression throughout development, coupled with functional analyses using parental RNA interference, revealed that maternal Toll is required to establish germ layers along the dorso-ventral axis and for embryo placement along the anterior-posterior axis. Interestingly, knockdown of the Toll pathway effector Rp-dorsal appears to regulate the expression of the Bone Morphogenetic Protein antagonist Rp-short-gastrulation. CONCLUSIONS: Our results indicate that Toll signals are the initiating event in dorso-ventral patterning during Rhodnius embryogenesis, and this is the first report of a conserved role for Toll in a hemipteran. Furthermore, as Rp-dorsal RNA interference generates anteriorly misplaced embryos, our results indicate a novel role for Toll signals in establishment of the anterior-posterior axis in Rhodnius. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/2041-9139-5-38) contains supplementary material, which is available to authorized users. BioMed Central 2014-10-27 /pmc/articles/PMC4407881/ /pubmed/25908955 http://dx.doi.org/10.1186/2041-9139-5-38 Text en © Berni et al.; licensee BioMed Central Ltd. 2014 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 Berni, Mateus Fontenele, Marcio Ribeiro Tobias-Santos, Vitoria Caceres-Rodrigues, Aline Mury, Flavia Borges Vionette-do-Amaral, Raquel Masuda, Hatisaburo Sorgine, Marcos da Fonseca, Rodrigo Nunes Araujo, Helena Toll signals regulate dorsal–ventral patterning and anterior–posterior placement of the embryo in the hemipteran Rhodnius prolixus |
title | Toll signals regulate dorsal–ventral patterning and anterior–posterior placement of the embryo in the hemipteran Rhodnius prolixus |
title_full | Toll signals regulate dorsal–ventral patterning and anterior–posterior placement of the embryo in the hemipteran Rhodnius prolixus |
title_fullStr | Toll signals regulate dorsal–ventral patterning and anterior–posterior placement of the embryo in the hemipteran Rhodnius prolixus |
title_full_unstemmed | Toll signals regulate dorsal–ventral patterning and anterior–posterior placement of the embryo in the hemipteran Rhodnius prolixus |
title_short | Toll signals regulate dorsal–ventral patterning and anterior–posterior placement of the embryo in the hemipteran Rhodnius prolixus |
title_sort | toll signals regulate dorsal–ventral patterning and anterior–posterior placement of the embryo in the hemipteran rhodnius prolixus |
topic | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4407881/ https://www.ncbi.nlm.nih.gov/pubmed/25908955 http://dx.doi.org/10.1186/2041-9139-5-38 |
work_keys_str_mv | AT bernimateus tollsignalsregulatedorsalventralpatterningandanteriorposteriorplacementoftheembryointhehemipteranrhodniusprolixus AT fontenelemarcioribeiro tollsignalsregulatedorsalventralpatterningandanteriorposteriorplacementoftheembryointhehemipteranrhodniusprolixus AT tobiassantosvitoria tollsignalsregulatedorsalventralpatterningandanteriorposteriorplacementoftheembryointhehemipteranrhodniusprolixus AT caceresrodriguesaline tollsignalsregulatedorsalventralpatterningandanteriorposteriorplacementoftheembryointhehemipteranrhodniusprolixus AT muryflaviaborges tollsignalsregulatedorsalventralpatterningandanteriorposteriorplacementoftheembryointhehemipteranrhodniusprolixus AT vionettedoamaralraquel tollsignalsregulatedorsalventralpatterningandanteriorposteriorplacementoftheembryointhehemipteranrhodniusprolixus AT masudahatisaburo tollsignalsregulatedorsalventralpatterningandanteriorposteriorplacementoftheembryointhehemipteranrhodniusprolixus AT sorginemarcos tollsignalsregulatedorsalventralpatterningandanteriorposteriorplacementoftheembryointhehemipteranrhodniusprolixus AT dafonsecarodrigonunes tollsignalsregulatedorsalventralpatterningandanteriorposteriorplacementoftheembryointhehemipteranrhodniusprolixus AT araujohelena tollsignalsregulatedorsalventralpatterningandanteriorposteriorplacementoftheembryointhehemipteranrhodniusprolixus |