The Evolution of Orphan Regions in Genomes of a Fungal Pathogen of Wheat

ABSTRACT Fungal plant pathogens rapidly evolve virulence on resistant hosts through mutations in genes encoding proteins that modulate the host immune responses. The mutational spectrum likely includes chromosomal rearrangements responsible for gains or losses of entire genes. However, the mechanism...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Clémence Plissonneau, Alessandra Stürchler, Daniel Croll
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/8a85545b0a2848ba9097f3308c382fca
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:8a85545b0a2848ba9097f3308c382fca
record_format	dspace
spelling	oai:doaj.org-article:8a85545b0a2848ba9097f3308c382fca2021-11-15T15:50:15ZThe Evolution of Orphan Regions in Genomes of a Fungal Pathogen of Wheat10.1128/mBio.01231-162150-7511https://doaj.org/article/8a85545b0a2848ba9097f3308c382fca2016-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01231-16https://doaj.org/toc/2150-7511ABSTRACT Fungal plant pathogens rapidly evolve virulence on resistant hosts through mutations in genes encoding proteins that modulate the host immune responses. The mutational spectrum likely includes chromosomal rearrangements responsible for gains or losses of entire genes. However, the mechanisms creating adaptive structural variation in fungal pathogen populations are poorly understood. We used complete genome assemblies to quantify structural variants segregating in the highly polymorphic fungal wheat pathogen Zymoseptoria tritici. The genetic basis of virulence in Z. tritici is complex, and populations harbor significant genetic variation for virulence; hence, we aimed to identify whether structural variation led to functional differences. We combined single-molecule real-time sequencing, genetic maps, and transcriptomics data to generate a fully assembled and annotated genome of the highly virulent field isolate 3D7. Comparative genomics analyses against the complete reference genome IPO323 identified large chromosomal inversions and the complete gain or loss of transposable-element clusters, explaining the extensive chromosomal-length polymorphisms found in this species. Both the 3D7 and IPO323 genomes harbored long tracts of sequences exclusive to one of the two genomes. These orphan regions contained 296 genes unique to the 3D7 genome and not previously known for this species. These orphan genes tended to be organized in clusters and showed evidence of mutational decay. Moreover, the orphan genes were enriched in genes encoding putative effectors and included a gene that is one of the most upregulated putative effector genes during wheat infection. Our study showed that this pathogen species harbored extensive chromosomal structure polymorphism that may drive the evolution of virulence. IMPORTANCE Pathogen outbreak populations often harbor previously unknown genes conferring virulence. Hence, a key puzzle of rapid pathogen evolution is the origin of such evolutionary novelty in genomes. Chromosomal rearrangements and structural variation in pathogen populations likely play a key role. However, identifying such polymorphism is challenging, as most genome-sequencing approaches only yield information about point mutations. We combined long-read technology and genetic maps to assemble the complete genome of a strain of a highly polymorphic fungal pathogen of wheat. Comparisons against the reference genome of the species showed substantial variation in the chromosome structure and revealed large regions unique to each assembled genome. These regions were enriched in genes encoding likely effector proteins, which are important components of pathogenicity. Our study showed that pathogen populations harbor extensive polymorphism at the chromosome level and that this polymorphism can be a source of adaptive genetic variation in pathogen evolution.Clémence PlissonneauAlessandra StürchlerDaniel CrollAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 7, Iss 5 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Clémence Plissonneau Alessandra Stürchler Daniel Croll The Evolution of Orphan Regions in Genomes of a Fungal Pathogen of Wheat
description	ABSTRACT Fungal plant pathogens rapidly evolve virulence on resistant hosts through mutations in genes encoding proteins that modulate the host immune responses. The mutational spectrum likely includes chromosomal rearrangements responsible for gains or losses of entire genes. However, the mechanisms creating adaptive structural variation in fungal pathogen populations are poorly understood. We used complete genome assemblies to quantify structural variants segregating in the highly polymorphic fungal wheat pathogen Zymoseptoria tritici. The genetic basis of virulence in Z. tritici is complex, and populations harbor significant genetic variation for virulence; hence, we aimed to identify whether structural variation led to functional differences. We combined single-molecule real-time sequencing, genetic maps, and transcriptomics data to generate a fully assembled and annotated genome of the highly virulent field isolate 3D7. Comparative genomics analyses against the complete reference genome IPO323 identified large chromosomal inversions and the complete gain or loss of transposable-element clusters, explaining the extensive chromosomal-length polymorphisms found in this species. Both the 3D7 and IPO323 genomes harbored long tracts of sequences exclusive to one of the two genomes. These orphan regions contained 296 genes unique to the 3D7 genome and not previously known for this species. These orphan genes tended to be organized in clusters and showed evidence of mutational decay. Moreover, the orphan genes were enriched in genes encoding putative effectors and included a gene that is one of the most upregulated putative effector genes during wheat infection. Our study showed that this pathogen species harbored extensive chromosomal structure polymorphism that may drive the evolution of virulence. IMPORTANCE Pathogen outbreak populations often harbor previously unknown genes conferring virulence. Hence, a key puzzle of rapid pathogen evolution is the origin of such evolutionary novelty in genomes. Chromosomal rearrangements and structural variation in pathogen populations likely play a key role. However, identifying such polymorphism is challenging, as most genome-sequencing approaches only yield information about point mutations. We combined long-read technology and genetic maps to assemble the complete genome of a strain of a highly polymorphic fungal pathogen of wheat. Comparisons against the reference genome of the species showed substantial variation in the chromosome structure and revealed large regions unique to each assembled genome. These regions were enriched in genes encoding likely effector proteins, which are important components of pathogenicity. Our study showed that pathogen populations harbor extensive polymorphism at the chromosome level and that this polymorphism can be a source of adaptive genetic variation in pathogen evolution.
format	article
author	Clémence Plissonneau Alessandra Stürchler Daniel Croll
author_facet	Clémence Plissonneau Alessandra Stürchler Daniel Croll
author_sort	Clémence Plissonneau
title	The Evolution of Orphan Regions in Genomes of a Fungal Pathogen of Wheat
title_short	The Evolution of Orphan Regions in Genomes of a Fungal Pathogen of Wheat
title_full	The Evolution of Orphan Regions in Genomes of a Fungal Pathogen of Wheat
title_fullStr	The Evolution of Orphan Regions in Genomes of a Fungal Pathogen of Wheat
title_full_unstemmed	The Evolution of Orphan Regions in Genomes of a Fungal Pathogen of Wheat
title_sort	evolution of orphan regions in genomes of a fungal pathogen of wheat
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/8a85545b0a2848ba9097f3308c382fca
work_keys_str_mv	AT clemenceplissonneau theevolutionoforphanregionsingenomesofafungalpathogenofwheat AT alessandrasturchler theevolutionoforphanregionsingenomesofafungalpathogenofwheat AT danielcroll theevolutionoforphanregionsingenomesofafungalpathogenofwheat AT clemenceplissonneau evolutionoforphanregionsingenomesofafungalpathogenofwheat AT alessandrasturchler evolutionoforphanregionsingenomesofafungalpathogenofwheat AT danielcroll evolutionoforphanregionsingenomesofafungalpathogenofwheat
_version_	1718427471062237184

The Evolution of Orphan Regions in Genomes of a Fungal Pathogen of Wheat

Ejemplares similares