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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...

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Autores principales: 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
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
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.
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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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