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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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) |
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DOAJ |
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EN |
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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. |
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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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