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The transposable element-rich genome of the cereal pest Sitophilus oryzae
BACKGROUND: The rice weevil Sitophilus oryzae is one of the most important agricultural pests, causing extensive damage to cereal in fields and to stored grains. S. oryzae has an intracellular symbiotic relationship (endosymbiosis) with the Gram-negative bacterium Sodalis pierantonius and is a valua...
Autores principales: | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8576890/ https://www.ncbi.nlm.nih.gov/pubmed/34749730 http://dx.doi.org/10.1186/s12915-021-01158-2 |
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author | Parisot, Nicolas Vargas-Chávez, Carlos Goubert, Clément Baa-Puyoulet, Patrice Balmand, Séverine Beranger, Louis Blanc, Caroline Bonnamour, Aymeric Boulesteix, Matthieu Burlet, Nelly Calevro, Federica Callaerts, Patrick Chancy, Théo Charles, Hubert Colella, Stefano Da Silva Barbosa, André Dell’Aglio, Elisa Di Genova, Alex Febvay, Gérard Gabaldón, Toni Galvão Ferrarini, Mariana Gerber, Alexandra Gillet, Benjamin Hubley, Robert Hughes, Sandrine Jacquin-Joly, Emmanuelle Maire, Justin Marcet-Houben, Marina Masson, Florent Meslin, Camille Montagné, Nicolas Moya, Andrés Ribeiro de Vasconcelos, Ana Tereza Richard, Gautier Rosen, Jeb Sagot, Marie-France Smit, Arian F. A. Storer, Jessica M. Vincent-Monegat, Carole Vallier, Agnès Vigneron, Aurélien Zaidman-Rémy, Anna Zamoum, Waël Vieira, Cristina Rebollo, Rita Latorre, Amparo Heddi, Abdelaziz |
author_facet | Parisot, Nicolas Vargas-Chávez, Carlos Goubert, Clément Baa-Puyoulet, Patrice Balmand, Séverine Beranger, Louis Blanc, Caroline Bonnamour, Aymeric Boulesteix, Matthieu Burlet, Nelly Calevro, Federica Callaerts, Patrick Chancy, Théo Charles, Hubert Colella, Stefano Da Silva Barbosa, André Dell’Aglio, Elisa Di Genova, Alex Febvay, Gérard Gabaldón, Toni Galvão Ferrarini, Mariana Gerber, Alexandra Gillet, Benjamin Hubley, Robert Hughes, Sandrine Jacquin-Joly, Emmanuelle Maire, Justin Marcet-Houben, Marina Masson, Florent Meslin, Camille Montagné, Nicolas Moya, Andrés Ribeiro de Vasconcelos, Ana Tereza Richard, Gautier Rosen, Jeb Sagot, Marie-France Smit, Arian F. A. Storer, Jessica M. Vincent-Monegat, Carole Vallier, Agnès Vigneron, Aurélien Zaidman-Rémy, Anna Zamoum, Waël Vieira, Cristina Rebollo, Rita Latorre, Amparo Heddi, Abdelaziz |
author_sort | Parisot, Nicolas |
collection | PubMed |
description | BACKGROUND: The rice weevil Sitophilus oryzae is one of the most important agricultural pests, causing extensive damage to cereal in fields and to stored grains. S. oryzae has an intracellular symbiotic relationship (endosymbiosis) with the Gram-negative bacterium Sodalis pierantonius and is a valuable model to decipher host-symbiont molecular interactions. RESULTS: We sequenced the Sitophilus oryzae genome using a combination of short and long reads to produce the best assembly for a Curculionidae species to date. We show that S. oryzae has undergone successive bursts of transposable element (TE) amplification, representing 72% of the genome. In addition, we show that many TE families are transcriptionally active, and changes in their expression are associated with insect endosymbiotic state. S. oryzae has undergone a high gene expansion rate, when compared to other beetles. Reconstruction of host-symbiont metabolic networks revealed that, despite its recent association with cereal weevils (30 kyear), S. pierantonius relies on the host for several amino acids and nucleotides to survive and to produce vitamins and essential amino acids required for insect development and cuticle biosynthesis. CONCLUSIONS: Here we present the genome of an agricultural pest beetle, which may act as a foundation for pest control. In addition, S. oryzae may be a useful model for endosymbiosis, and studying TE evolution and regulation, along with the impact of TEs on eukaryotic genomes. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-021-01158-2. |
format | Online Article Text |
id | pubmed-8576890 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-85768902021-11-10 The transposable element-rich genome of the cereal pest Sitophilus oryzae Parisot, Nicolas Vargas-Chávez, Carlos Goubert, Clément Baa-Puyoulet, Patrice Balmand, Séverine Beranger, Louis Blanc, Caroline Bonnamour, Aymeric Boulesteix, Matthieu Burlet, Nelly Calevro, Federica Callaerts, Patrick Chancy, Théo Charles, Hubert Colella, Stefano Da Silva Barbosa, André Dell’Aglio, Elisa Di Genova, Alex Febvay, Gérard Gabaldón, Toni Galvão Ferrarini, Mariana Gerber, Alexandra Gillet, Benjamin Hubley, Robert Hughes, Sandrine Jacquin-Joly, Emmanuelle Maire, Justin Marcet-Houben, Marina Masson, Florent Meslin, Camille Montagné, Nicolas Moya, Andrés Ribeiro de Vasconcelos, Ana Tereza Richard, Gautier Rosen, Jeb Sagot, Marie-France Smit, Arian F. A. Storer, Jessica M. Vincent-Monegat, Carole Vallier, Agnès Vigneron, Aurélien Zaidman-Rémy, Anna Zamoum, Waël Vieira, Cristina Rebollo, Rita Latorre, Amparo Heddi, Abdelaziz BMC Biol Research Article BACKGROUND: The rice weevil Sitophilus oryzae is one of the most important agricultural pests, causing extensive damage to cereal in fields and to stored grains. S. oryzae has an intracellular symbiotic relationship (endosymbiosis) with the Gram-negative bacterium Sodalis pierantonius and is a valuable model to decipher host-symbiont molecular interactions. RESULTS: We sequenced the Sitophilus oryzae genome using a combination of short and long reads to produce the best assembly for a Curculionidae species to date. We show that S. oryzae has undergone successive bursts of transposable element (TE) amplification, representing 72% of the genome. In addition, we show that many TE families are transcriptionally active, and changes in their expression are associated with insect endosymbiotic state. S. oryzae has undergone a high gene expansion rate, when compared to other beetles. Reconstruction of host-symbiont metabolic networks revealed that, despite its recent association with cereal weevils (30 kyear), S. pierantonius relies on the host for several amino acids and nucleotides to survive and to produce vitamins and essential amino acids required for insect development and cuticle biosynthesis. CONCLUSIONS: Here we present the genome of an agricultural pest beetle, which may act as a foundation for pest control. In addition, S. oryzae may be a useful model for endosymbiosis, and studying TE evolution and regulation, along with the impact of TEs on eukaryotic genomes. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-021-01158-2. BioMed Central 2021-11-09 /pmc/articles/PMC8576890/ /pubmed/34749730 http://dx.doi.org/10.1186/s12915-021-01158-2 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data. |
spellingShingle | Research Article Parisot, Nicolas Vargas-Chávez, Carlos Goubert, Clément Baa-Puyoulet, Patrice Balmand, Séverine Beranger, Louis Blanc, Caroline Bonnamour, Aymeric Boulesteix, Matthieu Burlet, Nelly Calevro, Federica Callaerts, Patrick Chancy, Théo Charles, Hubert Colella, Stefano Da Silva Barbosa, André Dell’Aglio, Elisa Di Genova, Alex Febvay, Gérard Gabaldón, Toni Galvão Ferrarini, Mariana Gerber, Alexandra Gillet, Benjamin Hubley, Robert Hughes, Sandrine Jacquin-Joly, Emmanuelle Maire, Justin Marcet-Houben, Marina Masson, Florent Meslin, Camille Montagné, Nicolas Moya, Andrés Ribeiro de Vasconcelos, Ana Tereza Richard, Gautier Rosen, Jeb Sagot, Marie-France Smit, Arian F. A. Storer, Jessica M. Vincent-Monegat, Carole Vallier, Agnès Vigneron, Aurélien Zaidman-Rémy, Anna Zamoum, Waël Vieira, Cristina Rebollo, Rita Latorre, Amparo Heddi, Abdelaziz The transposable element-rich genome of the cereal pest Sitophilus oryzae |
title | The transposable element-rich genome of the cereal pest Sitophilus oryzae |
title_full | The transposable element-rich genome of the cereal pest Sitophilus oryzae |
title_fullStr | The transposable element-rich genome of the cereal pest Sitophilus oryzae |
title_full_unstemmed | The transposable element-rich genome of the cereal pest Sitophilus oryzae |
title_short | The transposable element-rich genome of the cereal pest Sitophilus oryzae |
title_sort | transposable element-rich genome of the cereal pest sitophilus oryzae |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8576890/ https://www.ncbi.nlm.nih.gov/pubmed/34749730 http://dx.doi.org/10.1186/s12915-021-01158-2 |
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