Cargando…

Genome compartmentalization predates species divergence in the plant pathogen genus Zymoseptoria

BACKGROUND: Antagonistic co-evolution can drive rapid adaptation in pathogens and shape genome architecture. Comparative genome analyses of several fungal pathogens revealed highly variable genomes, for many species characterized by specific repeat-rich genome compartments with exceptionally high se...

Descripción completa

Detalles Bibliográficos
Autores principales: Feurtey, Alice, Lorrain, Cécile, Croll, Daniel, Eschenbrenner, Christoph, Freitag, Michael, Habig, Michael, Haueisen, Janine, Möller, Mareike, Schotanus, Klaas, Stukenbrock, Eva H.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7448473/
https://www.ncbi.nlm.nih.gov/pubmed/32842972
http://dx.doi.org/10.1186/s12864-020-06871-w
_version_ 1783574505382215680
author Feurtey, Alice
Lorrain, Cécile
Croll, Daniel
Eschenbrenner, Christoph
Freitag, Michael
Habig, Michael
Haueisen, Janine
Möller, Mareike
Schotanus, Klaas
Stukenbrock, Eva H.
author_facet Feurtey, Alice
Lorrain, Cécile
Croll, Daniel
Eschenbrenner, Christoph
Freitag, Michael
Habig, Michael
Haueisen, Janine
Möller, Mareike
Schotanus, Klaas
Stukenbrock, Eva H.
author_sort Feurtey, Alice
collection PubMed
description BACKGROUND: Antagonistic co-evolution can drive rapid adaptation in pathogens and shape genome architecture. Comparative genome analyses of several fungal pathogens revealed highly variable genomes, for many species characterized by specific repeat-rich genome compartments with exceptionally high sequence variability. Dynamic genome structure may enable fast adaptation to host genetics. The wheat pathogen Zymoseptoria tritici with its highly variable genome, has emerged as a model organism to study genome evolution of plant pathogens. Here, we compared genomes of Z. tritici isolates and of sister species infecting wild grasses to address the evolution of genome composition and structure. RESULTS: Using long-read technology, we sequenced and assembled genomes of Z. ardabiliae, Z. brevis, Z. pseudotritici and Z. passerinii, together with two isolates of Z. tritici. We report a high extent of genome collinearity among Zymoseptoria species and high conservation of genomic, transcriptomic and epigenomic signatures of compartmentalization. We identify high gene content variability both within and between species. In addition, such variability is mainly limited to the accessory chromosomes and accessory compartments. Despite strong host specificity and non-overlapping host-range between species, predicted effectors are mainly shared among Zymoseptoria species, yet exhibiting a high level of presence-absence polymorphism within Z. tritici. Using in planta transcriptomic data from Z. tritici, we suggest different roles for the shared orthologs and for the accessory genes during infection of their hosts. CONCLUSION: Despite previous reports of high genomic plasticity in Z. tritici, we describe here a high level of conservation in genomic, epigenomic and transcriptomic composition and structure across the genus Zymoseptoria. The compartmentalized genome allows the maintenance of a functional core genome co-occurring with a highly variable accessory genome.
format Online
Article
Text
id pubmed-7448473
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-74484732020-08-27 Genome compartmentalization predates species divergence in the plant pathogen genus Zymoseptoria Feurtey, Alice Lorrain, Cécile Croll, Daniel Eschenbrenner, Christoph Freitag, Michael Habig, Michael Haueisen, Janine Möller, Mareike Schotanus, Klaas Stukenbrock, Eva H. BMC Genomics Research Article BACKGROUND: Antagonistic co-evolution can drive rapid adaptation in pathogens and shape genome architecture. Comparative genome analyses of several fungal pathogens revealed highly variable genomes, for many species characterized by specific repeat-rich genome compartments with exceptionally high sequence variability. Dynamic genome structure may enable fast adaptation to host genetics. The wheat pathogen Zymoseptoria tritici with its highly variable genome, has emerged as a model organism to study genome evolution of plant pathogens. Here, we compared genomes of Z. tritici isolates and of sister species infecting wild grasses to address the evolution of genome composition and structure. RESULTS: Using long-read technology, we sequenced and assembled genomes of Z. ardabiliae, Z. brevis, Z. pseudotritici and Z. passerinii, together with two isolates of Z. tritici. We report a high extent of genome collinearity among Zymoseptoria species and high conservation of genomic, transcriptomic and epigenomic signatures of compartmentalization. We identify high gene content variability both within and between species. In addition, such variability is mainly limited to the accessory chromosomes and accessory compartments. Despite strong host specificity and non-overlapping host-range between species, predicted effectors are mainly shared among Zymoseptoria species, yet exhibiting a high level of presence-absence polymorphism within Z. tritici. Using in planta transcriptomic data from Z. tritici, we suggest different roles for the shared orthologs and for the accessory genes during infection of their hosts. CONCLUSION: Despite previous reports of high genomic plasticity in Z. tritici, we describe here a high level of conservation in genomic, epigenomic and transcriptomic composition and structure across the genus Zymoseptoria. The compartmentalized genome allows the maintenance of a functional core genome co-occurring with a highly variable accessory genome. BioMed Central 2020-08-26 /pmc/articles/PMC7448473/ /pubmed/32842972 http://dx.doi.org/10.1186/s12864-020-06871-w Text en © The Author(s) 2020 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/. The Creative Commons Public Domain Dedication waiver (http://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
Feurtey, Alice
Lorrain, Cécile
Croll, Daniel
Eschenbrenner, Christoph
Freitag, Michael
Habig, Michael
Haueisen, Janine
Möller, Mareike
Schotanus, Klaas
Stukenbrock, Eva H.
Genome compartmentalization predates species divergence in the plant pathogen genus Zymoseptoria
title Genome compartmentalization predates species divergence in the plant pathogen genus Zymoseptoria
title_full Genome compartmentalization predates species divergence in the plant pathogen genus Zymoseptoria
title_fullStr Genome compartmentalization predates species divergence in the plant pathogen genus Zymoseptoria
title_full_unstemmed Genome compartmentalization predates species divergence in the plant pathogen genus Zymoseptoria
title_short Genome compartmentalization predates species divergence in the plant pathogen genus Zymoseptoria
title_sort genome compartmentalization predates species divergence in the plant pathogen genus zymoseptoria
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7448473/
https://www.ncbi.nlm.nih.gov/pubmed/32842972
http://dx.doi.org/10.1186/s12864-020-06871-w
work_keys_str_mv AT feurteyalice genomecompartmentalizationpredatesspeciesdivergenceintheplantpathogengenuszymoseptoria
AT lorraincecile genomecompartmentalizationpredatesspeciesdivergenceintheplantpathogengenuszymoseptoria
AT crolldaniel genomecompartmentalizationpredatesspeciesdivergenceintheplantpathogengenuszymoseptoria
AT eschenbrennerchristoph genomecompartmentalizationpredatesspeciesdivergenceintheplantpathogengenuszymoseptoria
AT freitagmichael genomecompartmentalizationpredatesspeciesdivergenceintheplantpathogengenuszymoseptoria
AT habigmichael genomecompartmentalizationpredatesspeciesdivergenceintheplantpathogengenuszymoseptoria
AT haueisenjanine genomecompartmentalizationpredatesspeciesdivergenceintheplantpathogengenuszymoseptoria
AT mollermareike genomecompartmentalizationpredatesspeciesdivergenceintheplantpathogengenuszymoseptoria
AT schotanusklaas genomecompartmentalizationpredatesspeciesdivergenceintheplantpathogengenuszymoseptoria
AT stukenbrockevah genomecompartmentalizationpredatesspeciesdivergenceintheplantpathogengenuszymoseptoria