Transcriptomic and functional analyses of the piRNA pathway in the Chagas disease vector Rhodnius prolixus.

The piRNA pathway is a surveillance system that guarantees oogenesis and adult fertility in a range of animal species. The pathway is centered on PIWI clade Argonaute proteins and the associated small non-coding RNAs termed piRNAs. In this study, we set to investigate the evolutionary conservation o...

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Published in:PLOS Neglected Tropical Diseases
Main Authors: Tarcisio Brito, Alison Julio, Mateus Berni, Lisiane de Castro Poncio, Emerson Soares Bernardes, Helena Araujo, Michael Sammeth, Attilio Pane
Format: Article in Journal/Newspaper
Language:English
Published: Public Library of Science (PLoS) 2018
Subjects:
Online Access:https://doi.org/10.1371/journal.pntd.0006760
https://doaj.org/article/f0655a1f157c40bc81b1de2e03a61ca3
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spelling ftdoajarticles:oai:doaj.org/article:f0655a1f157c40bc81b1de2e03a61ca3 2023-05-15T15:10:40+02:00 Transcriptomic and functional analyses of the piRNA pathway in the Chagas disease vector Rhodnius prolixus. Tarcisio Brito Alison Julio Mateus Berni Lisiane de Castro Poncio Emerson Soares Bernardes Helena Araujo Michael Sammeth Attilio Pane 2018-10-01T00:00:00Z https://doi.org/10.1371/journal.pntd.0006760 https://doaj.org/article/f0655a1f157c40bc81b1de2e03a61ca3 EN eng Public Library of Science (PLoS) http://europepmc.org/articles/PMC6179187?pdf=render https://doaj.org/toc/1935-2727 https://doaj.org/toc/1935-2735 1935-2727 1935-2735 doi:10.1371/journal.pntd.0006760 https://doaj.org/article/f0655a1f157c40bc81b1de2e03a61ca3 PLoS Neglected Tropical Diseases, Vol 12, Iss 10, p e0006760 (2018) Arctic medicine. Tropical medicine RC955-962 Public aspects of medicine RA1-1270 article 2018 ftdoajarticles https://doi.org/10.1371/journal.pntd.0006760 2022-12-31T14:37:39Z The piRNA pathway is a surveillance system that guarantees oogenesis and adult fertility in a range of animal species. The pathway is centered on PIWI clade Argonaute proteins and the associated small non-coding RNAs termed piRNAs. In this study, we set to investigate the evolutionary conservation of the piRNA pathway in the hemimetabolous insect Rhodnius prolixus. Our transcriptome profiling reveals that core components of the pathway are expressed during previtellogenic stages of oogenesis. Rhodnius' genome harbors four putative piwi orthologs. We show that Rp-piwi2, Rp-piwi3 and Rp-ago3, but not Rp-piwi1 transcripts are produced in the germline tissues and maternally deposited in the mature eggs. Consistent with a role in Rhodnius oogenesis, parental RNAi against the Rp-piwi2, Rp-piwi3 and Rp-ago3 results in severe egg laying and female adult fertility defects. Furthermore, we show that the reduction of the Rp-piwi2 levels by parental RNAi disrupts oogenesis by causing a dramatic loss of trophocytes, egg chamber degeneration and oogenesis arrest. Intriguingly, the putative Rp-Piwi2 protein features a polyglutamine tract at its N-terminal region, which is conserved in PIWI proteins encoded in the genome of other Triatomine species. Together with R. prolixus, these hematophagous insects are primary vectors of the Chagas disease. Thus, our data shed more light on the evolution of the piRNA pathway and provide a framework for the development of new control strategies for Chagas disease insect vectors. Article in Journal/Newspaper Arctic Directory of Open Access Journals: DOAJ Articles Arctic PLOS Neglected Tropical Diseases 12 10 e0006760
institution Open Polar
collection Directory of Open Access Journals: DOAJ Articles
op_collection_id ftdoajarticles
language English
topic Arctic medicine. Tropical medicine
RC955-962
Public aspects of medicine
RA1-1270
spellingShingle Arctic medicine. Tropical medicine
RC955-962
Public aspects of medicine
RA1-1270
Tarcisio Brito
Alison Julio
Mateus Berni
Lisiane de Castro Poncio
Emerson Soares Bernardes
Helena Araujo
Michael Sammeth
Attilio Pane
Transcriptomic and functional analyses of the piRNA pathway in the Chagas disease vector Rhodnius prolixus.
topic_facet Arctic medicine. Tropical medicine
RC955-962
Public aspects of medicine
RA1-1270
description The piRNA pathway is a surveillance system that guarantees oogenesis and adult fertility in a range of animal species. The pathway is centered on PIWI clade Argonaute proteins and the associated small non-coding RNAs termed piRNAs. In this study, we set to investigate the evolutionary conservation of the piRNA pathway in the hemimetabolous insect Rhodnius prolixus. Our transcriptome profiling reveals that core components of the pathway are expressed during previtellogenic stages of oogenesis. Rhodnius' genome harbors four putative piwi orthologs. We show that Rp-piwi2, Rp-piwi3 and Rp-ago3, but not Rp-piwi1 transcripts are produced in the germline tissues and maternally deposited in the mature eggs. Consistent with a role in Rhodnius oogenesis, parental RNAi against the Rp-piwi2, Rp-piwi3 and Rp-ago3 results in severe egg laying and female adult fertility defects. Furthermore, we show that the reduction of the Rp-piwi2 levels by parental RNAi disrupts oogenesis by causing a dramatic loss of trophocytes, egg chamber degeneration and oogenesis arrest. Intriguingly, the putative Rp-Piwi2 protein features a polyglutamine tract at its N-terminal region, which is conserved in PIWI proteins encoded in the genome of other Triatomine species. Together with R. prolixus, these hematophagous insects are primary vectors of the Chagas disease. Thus, our data shed more light on the evolution of the piRNA pathway and provide a framework for the development of new control strategies for Chagas disease insect vectors.
format Article in Journal/Newspaper
author Tarcisio Brito
Alison Julio
Mateus Berni
Lisiane de Castro Poncio
Emerson Soares Bernardes
Helena Araujo
Michael Sammeth
Attilio Pane
author_facet Tarcisio Brito
Alison Julio
Mateus Berni
Lisiane de Castro Poncio
Emerson Soares Bernardes
Helena Araujo
Michael Sammeth
Attilio Pane
author_sort Tarcisio Brito
title Transcriptomic and functional analyses of the piRNA pathway in the Chagas disease vector Rhodnius prolixus.
title_short Transcriptomic and functional analyses of the piRNA pathway in the Chagas disease vector Rhodnius prolixus.
title_full Transcriptomic and functional analyses of the piRNA pathway in the Chagas disease vector Rhodnius prolixus.
title_fullStr Transcriptomic and functional analyses of the piRNA pathway in the Chagas disease vector Rhodnius prolixus.
title_full_unstemmed Transcriptomic and functional analyses of the piRNA pathway in the Chagas disease vector Rhodnius prolixus.
title_sort transcriptomic and functional analyses of the pirna pathway in the chagas disease vector rhodnius prolixus.
publisher Public Library of Science (PLoS)
publishDate 2018
url https://doi.org/10.1371/journal.pntd.0006760
https://doaj.org/article/f0655a1f157c40bc81b1de2e03a61ca3
geographic Arctic
geographic_facet Arctic
genre Arctic
genre_facet Arctic
op_source PLoS Neglected Tropical Diseases, Vol 12, Iss 10, p e0006760 (2018)
op_relation http://europepmc.org/articles/PMC6179187?pdf=render
https://doaj.org/toc/1935-2727
https://doaj.org/toc/1935-2735
1935-2727
1935-2735
doi:10.1371/journal.pntd.0006760
https://doaj.org/article/f0655a1f157c40bc81b1de2e03a61ca3
op_doi https://doi.org/10.1371/journal.pntd.0006760
container_title PLOS Neglected Tropical Diseases
container_volume 12
container_issue 10
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