The transposable element-rich genome of the cereal pest Sitophilus oryzae

Abstract 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...

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Autores principales: Nicolas Parisot, Carlos Vargas-Chávez, Clément Goubert, Patrice Baa-Puyoulet, Séverine Balmand, Louis Beranger, Caroline Blanc, Aymeric Bonnamour, Matthieu Boulesteix, Nelly Burlet, Federica Calevro, Patrick Callaerts, Théo Chancy, Hubert Charles, Stefano Colella, André Da Silva Barbosa, Elisa Dell’Aglio, Alex Di Genova, Gérard Febvay, Toni Gabaldón, Mariana Galvão Ferrarini, Alexandra Gerber, Benjamin Gillet, Robert Hubley, Sandrine Hughes, Emmanuelle Jacquin-Joly, Justin Maire, Marina Marcet-Houben, Florent Masson, Camille Meslin, Nicolas Montagné, Andrés Moya, Ana Tereza Ribeiro de Vasconcelos, Gautier Richard, Jeb Rosen, Marie-France Sagot, Arian F. A. Smit, Jessica M. Storer, Carole Vincent-Monegat, Agnès Vallier, Aurélien Vigneron, Anna Zaidman-Rémy, Waël Zamoum, Cristina Vieira, Rita Rebollo, Amparo Latorre, Abdelaziz Heddi
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Publicado: BMC 2021
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spelling oai:doaj.org-article:ae3450d19e2d4fc3bd602edfb582ed692021-11-14T12:43:34ZThe transposable element-rich genome of the cereal pest Sitophilus oryzae10.1186/s12915-021-01158-21741-7007https://doaj.org/article/ae3450d19e2d4fc3bd602edfb582ed692021-11-01T00:00:00Zhttps://doi.org/10.1186/s12915-021-01158-2https://doaj.org/toc/1741-7007Abstract 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.Nicolas ParisotCarlos Vargas-ChávezClément GoubertPatrice Baa-PuyouletSéverine BalmandLouis BerangerCaroline BlancAymeric BonnamourMatthieu BoulesteixNelly BurletFederica CalevroPatrick CallaertsThéo ChancyHubert CharlesStefano ColellaAndré Da Silva BarbosaElisa Dell’AglioAlex Di GenovaGérard FebvayToni GabaldónMariana Galvão FerrariniAlexandra GerberBenjamin GilletRobert HubleySandrine HughesEmmanuelle Jacquin-JolyJustin MaireMarina Marcet-HoubenFlorent MassonCamille MeslinNicolas MontagnéAndrés MoyaAna Tereza Ribeiro de VasconcelosGautier RichardJeb RosenMarie-France SagotArian F. A. SmitJessica M. StorerCarole Vincent-MonegatAgnès VallierAurélien VigneronAnna Zaidman-RémyWaël ZamoumCristina VieiraRita RebolloAmparo LatorreAbdelaziz HeddiBMCarticleColeopteraWeevilSitophilus oryzaeGenomeTransposable elementsEndosymbiosisBiology (General)QH301-705.5ENBMC Biology, Vol 19, Iss 1, Pp 1-28 (2021)
institution DOAJ
collection DOAJ
language EN
topic Coleoptera
Weevil
Sitophilus oryzae
Genome
Transposable elements
Endosymbiosis
Biology (General)
QH301-705.5
spellingShingle Coleoptera
Weevil
Sitophilus oryzae
Genome
Transposable elements
Endosymbiosis
Biology (General)
QH301-705.5
Nicolas Parisot
Carlos Vargas-Chávez
Clément Goubert
Patrice Baa-Puyoulet
Séverine Balmand
Louis Beranger
Caroline Blanc
Aymeric Bonnamour
Matthieu Boulesteix
Nelly Burlet
Federica Calevro
Patrick Callaerts
Théo Chancy
Hubert Charles
Stefano Colella
André Da Silva Barbosa
Elisa Dell’Aglio
Alex Di Genova
Gérard Febvay
Toni Gabaldón
Mariana Galvão Ferrarini
Alexandra Gerber
Benjamin Gillet
Robert Hubley
Sandrine Hughes
Emmanuelle Jacquin-Joly
Justin Maire
Marina Marcet-Houben
Florent Masson
Camille Meslin
Nicolas Montagné
Andrés Moya
Ana Tereza Ribeiro de Vasconcelos
Gautier Richard
Jeb Rosen
Marie-France Sagot
Arian F. A. Smit
Jessica M. Storer
Carole Vincent-Monegat
Agnès Vallier
Aurélien Vigneron
Anna Zaidman-Rémy
Waël Zamoum
Cristina Vieira
Rita Rebollo
Amparo Latorre
Abdelaziz Heddi
The transposable element-rich genome of the cereal pest Sitophilus oryzae
description Abstract 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.
format article
author Nicolas Parisot
Carlos Vargas-Chávez
Clément Goubert
Patrice Baa-Puyoulet
Séverine Balmand
Louis Beranger
Caroline Blanc
Aymeric Bonnamour
Matthieu Boulesteix
Nelly Burlet
Federica Calevro
Patrick Callaerts
Théo Chancy
Hubert Charles
Stefano Colella
André Da Silva Barbosa
Elisa Dell’Aglio
Alex Di Genova
Gérard Febvay
Toni Gabaldón
Mariana Galvão Ferrarini
Alexandra Gerber
Benjamin Gillet
Robert Hubley
Sandrine Hughes
Emmanuelle Jacquin-Joly
Justin Maire
Marina Marcet-Houben
Florent Masson
Camille Meslin
Nicolas Montagné
Andrés Moya
Ana Tereza Ribeiro de Vasconcelos
Gautier Richard
Jeb Rosen
Marie-France Sagot
Arian F. A. Smit
Jessica M. Storer
Carole Vincent-Monegat
Agnès Vallier
Aurélien Vigneron
Anna Zaidman-Rémy
Waël Zamoum
Cristina Vieira
Rita Rebollo
Amparo Latorre
Abdelaziz Heddi
author_facet Nicolas Parisot
Carlos Vargas-Chávez
Clément Goubert
Patrice Baa-Puyoulet
Séverine Balmand
Louis Beranger
Caroline Blanc
Aymeric Bonnamour
Matthieu Boulesteix
Nelly Burlet
Federica Calevro
Patrick Callaerts
Théo Chancy
Hubert Charles
Stefano Colella
André Da Silva Barbosa
Elisa Dell’Aglio
Alex Di Genova
Gérard Febvay
Toni Gabaldón
Mariana Galvão Ferrarini
Alexandra Gerber
Benjamin Gillet
Robert Hubley
Sandrine Hughes
Emmanuelle Jacquin-Joly
Justin Maire
Marina Marcet-Houben
Florent Masson
Camille Meslin
Nicolas Montagné
Andrés Moya
Ana Tereza Ribeiro de Vasconcelos
Gautier Richard
Jeb Rosen
Marie-France Sagot
Arian F. A. Smit
Jessica M. Storer
Carole Vincent-Monegat
Agnès Vallier
Aurélien Vigneron
Anna Zaidman-Rémy
Waël Zamoum
Cristina Vieira
Rita Rebollo
Amparo Latorre
Abdelaziz Heddi
author_sort Nicolas Parisot
title 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_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_sort transposable element-rich genome of the cereal pest sitophilus oryzae
publisher BMC
publishDate 2021
url https://doaj.org/article/ae3450d19e2d4fc3bd602edfb582ed69
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