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The Easter Egg Weevil (Pachyrhynchus) genome reveals syntenic patterns in Coleoptera across 200 million years of evolution

Patterns of genomic architecture across insects remain largely undocumented or decoupled from a broader phylogenetic context. For instance, it is unknown whether translocation rates differ between insect orders. We address broad scale patterns of genome architecture across Insecta by examining synte...

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Autores principales: Van Dam, Matthew H., Cabras, Analyn Anzano, Henderson, James B., Rominger, Andrew J., Pérez Estrada, Cynthia, Omer, Arina D., Dudchenko, Olga, Lieberman Aiden, Erez, Lam, Athena W.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8432895/
https://www.ncbi.nlm.nih.gov/pubmed/34460814
http://dx.doi.org/10.1371/journal.pgen.1009745
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author Van Dam, Matthew H.
Cabras, Analyn Anzano
Henderson, James B.
Rominger, Andrew J.
Pérez Estrada, Cynthia
Omer, Arina D.
Dudchenko, Olga
Lieberman Aiden, Erez
Lam, Athena W.
author_facet Van Dam, Matthew H.
Cabras, Analyn Anzano
Henderson, James B.
Rominger, Andrew J.
Pérez Estrada, Cynthia
Omer, Arina D.
Dudchenko, Olga
Lieberman Aiden, Erez
Lam, Athena W.
author_sort Van Dam, Matthew H.
collection PubMed
description Patterns of genomic architecture across insects remain largely undocumented or decoupled from a broader phylogenetic context. For instance, it is unknown whether translocation rates differ between insect orders. We address broad scale patterns of genome architecture across Insecta by examining synteny in a phylogenetic framework from open-source insect genomes. To accomplish this, we add a chromosome level genome to a crucial lineage, Coleoptera. Our assembly of the Pachyrhynchus sulphureomaculatus genome is the first chromosome scale genome for the hyperdiverse Phytophaga lineage and currently the largest insect genome assembled to this scale. The genome is significantly larger than those of other weevils, and this increase in size is caused by repetitive elements. Our results also indicate that, among beetles, there are instances of long-lasting (>200 Ma) localization of genes to a particular chromosome with few translocation events. While some chromosomes have a paucity of translocations, intra-chromosomal synteny was almost absent, with gene order thoroughly shuffled along a chromosome. This large amount of reshuffling within chromosomes with few inter-chromosomal events contrasts with patterns seen in mammals in which the chromosomes tend to exchange larger blocks of material more readily. To place our findings in an evolutionary context, we compared syntenic patterns across Insecta in a phylogenetic framework. For the first time, we find that synteny decays at an exponential rate relative to phylogenetic distance. Additionally, there are significant differences in decay rates between insect orders, this pattern was not driven by Lepidoptera alone which has a substantially different rate.
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spelling pubmed-84328952021-09-11 The Easter Egg Weevil (Pachyrhynchus) genome reveals syntenic patterns in Coleoptera across 200 million years of evolution Van Dam, Matthew H. Cabras, Analyn Anzano Henderson, James B. Rominger, Andrew J. Pérez Estrada, Cynthia Omer, Arina D. Dudchenko, Olga Lieberman Aiden, Erez Lam, Athena W. PLoS Genet Research Article Patterns of genomic architecture across insects remain largely undocumented or decoupled from a broader phylogenetic context. For instance, it is unknown whether translocation rates differ between insect orders. We address broad scale patterns of genome architecture across Insecta by examining synteny in a phylogenetic framework from open-source insect genomes. To accomplish this, we add a chromosome level genome to a crucial lineage, Coleoptera. Our assembly of the Pachyrhynchus sulphureomaculatus genome is the first chromosome scale genome for the hyperdiverse Phytophaga lineage and currently the largest insect genome assembled to this scale. The genome is significantly larger than those of other weevils, and this increase in size is caused by repetitive elements. Our results also indicate that, among beetles, there are instances of long-lasting (>200 Ma) localization of genes to a particular chromosome with few translocation events. While some chromosomes have a paucity of translocations, intra-chromosomal synteny was almost absent, with gene order thoroughly shuffled along a chromosome. This large amount of reshuffling within chromosomes with few inter-chromosomal events contrasts with patterns seen in mammals in which the chromosomes tend to exchange larger blocks of material more readily. To place our findings in an evolutionary context, we compared syntenic patterns across Insecta in a phylogenetic framework. For the first time, we find that synteny decays at an exponential rate relative to phylogenetic distance. Additionally, there are significant differences in decay rates between insect orders, this pattern was not driven by Lepidoptera alone which has a substantially different rate. Public Library of Science 2021-08-30 /pmc/articles/PMC8432895/ /pubmed/34460814 http://dx.doi.org/10.1371/journal.pgen.1009745 Text en © 2021 Van Dam et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Van Dam, Matthew H.
Cabras, Analyn Anzano
Henderson, James B.
Rominger, Andrew J.
Pérez Estrada, Cynthia
Omer, Arina D.
Dudchenko, Olga
Lieberman Aiden, Erez
Lam, Athena W.
The Easter Egg Weevil (Pachyrhynchus) genome reveals syntenic patterns in Coleoptera across 200 million years of evolution
title The Easter Egg Weevil (Pachyrhynchus) genome reveals syntenic patterns in Coleoptera across 200 million years of evolution
title_full The Easter Egg Weevil (Pachyrhynchus) genome reveals syntenic patterns in Coleoptera across 200 million years of evolution
title_fullStr The Easter Egg Weevil (Pachyrhynchus) genome reveals syntenic patterns in Coleoptera across 200 million years of evolution
title_full_unstemmed The Easter Egg Weevil (Pachyrhynchus) genome reveals syntenic patterns in Coleoptera across 200 million years of evolution
title_short The Easter Egg Weevil (Pachyrhynchus) genome reveals syntenic patterns in Coleoptera across 200 million years of evolution
title_sort easter egg weevil (pachyrhynchus) genome reveals syntenic patterns in coleoptera across 200 million years of evolution
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8432895/
https://www.ncbi.nlm.nih.gov/pubmed/34460814
http://dx.doi.org/10.1371/journal.pgen.1009745
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