Mitotic Recombination and Rapid Genome Evolution in the Invasive Forest Pathogen <italic toggle="yes">Phytophthora ramorum</italic>

ABSTRACT Invasive alien species often have reduced genetic diversity and must adapt to new environments. Given the success of many invasions, this is sometimes called the genetic paradox of invasion. Phytophthora ramorum is invasive, limited to asexual reproduction within four lineages, and presumed...

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Autores principales:	Angela L. Dale, Nicolas Feau, Sydney E. Everhart, Braham Dhillon, Barbara Wong, Julie Sheppard, Guillaume J. Bilodeau, Avneet Brar, Javier F. Tabima, Danyu Shen, Clive M. Brasier, Brett M. Tyler, Niklaus J. Grünwald, Richard C. Hamelin
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	forest health genome evolution oomycetes sudden larch death sudden oak death tree pathogen Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/7ed7ecba6ade42a4a23f9b0a8a03f8c3
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spelling	oai:doaj.org-article:7ed7ecba6ade42a4a23f9b0a8a03f8c32021-11-15T15:55:25ZMitotic Recombination and Rapid Genome Evolution in the Invasive Forest Pathogen <italic toggle="yes">Phytophthora ramorum</italic>10.1128/mBio.02452-182150-7511https://doaj.org/article/7ed7ecba6ade42a4a23f9b0a8a03f8c32019-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02452-18https://doaj.org/toc/2150-7511ABSTRACT Invasive alien species often have reduced genetic diversity and must adapt to new environments. Given the success of many invasions, this is sometimes called the genetic paradox of invasion. Phytophthora ramorum is invasive, limited to asexual reproduction within four lineages, and presumed clonal. It is responsible for sudden oak death in the United States, sudden larch death in Europe, and ramorum blight in North America and Europe. We sequenced the genomes of 107 isolates to determine how this pathogen can overcome the invasion paradox. Mitotic recombination (MR) associated with transposons and low gene density has generated runs of homozygosity (ROH) affecting 2,698 genes, resulting in novel genotypic diversity within the lineages. One ROH enriched in effectors was fixed in the NA1 lineage. An independent ROH affected the same scaffold in the EU1 lineage, suggesting an MR hot spot and a selection target. Differences in host infection between EU1 isolates with and without the ROH suggest that they may differ in aggressiveness. Non-core regions (not shared by all lineages) had signatures of accelerated evolution and were enriched in putative pathogenicity genes and transposons. There was a striking pattern of gene loss, including all effectors, in the non-core EU2 genome. Positive selection was observed in 8.0% of RxLR and 18.8% of Crinkler effector genes compared with 0.9% of the core eukaryotic gene set. We conclude that the P. ramorum lineages are diverging via a rapidly evolving non-core genome and that the invasive asexual lineages are not clonal, but display genotypic diversity caused by MR. IMPORTANCE Alien species are often successful invaders in new environments, despite the introduction of a few isolates with a reduced genetic pool. This is called the genetic paradox of invasion. We found two mechanisms by which the invasive forest pathogen causing sudden oak and sudden larch death can evolve. Extensive mitotic recombination producing runs of homozygosity generates genotypic diversity even in the absence of sexual reproduction, and rapid turnover of genes in the non-core, or nonessential portion of genome not shared by all isolates, allows pathogenicity genes to evolve rapidly or be eliminated while retaining essential genes. Mitotic recombination events occur in genomic hot spots, resulting in similar ROH patterns in different isolates or groups; one ROH, independently generated in two different groups, was enriched in pathogenicity genes and may be a target for selection. This provides important insights into the evolution of invasive alien pathogens and their potential for adaptation and future persistence.Angela L. DaleNicolas FeauSydney E. EverhartBraham DhillonBarbara WongJulie SheppardGuillaume J. BilodeauAvneet BrarJavier F. TabimaDanyu ShenClive M. BrasierBrett M. TylerNiklaus J. GrünwaldRichard C. HamelinAmerican Society for Microbiologyarticleforest healthgenome evolutionoomycetessudden larch deathsudden oak deathtree pathogenMicrobiologyQR1-502ENmBio, Vol 10, Iss 2 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	forest health genome evolution oomycetes sudden larch death sudden oak death tree pathogen Microbiology QR1-502
spellingShingle	forest health genome evolution oomycetes sudden larch death sudden oak death tree pathogen Microbiology QR1-502 Angela L. Dale Nicolas Feau Sydney E. Everhart Braham Dhillon Barbara Wong Julie Sheppard Guillaume J. Bilodeau Avneet Brar Javier F. Tabima Danyu Shen Clive M. Brasier Brett M. Tyler Niklaus J. Grünwald Richard C. Hamelin Mitotic Recombination and Rapid Genome Evolution in the Invasive Forest Pathogen <italic toggle="yes">Phytophthora ramorum</italic>
description	ABSTRACT Invasive alien species often have reduced genetic diversity and must adapt to new environments. Given the success of many invasions, this is sometimes called the genetic paradox of invasion. Phytophthora ramorum is invasive, limited to asexual reproduction within four lineages, and presumed clonal. It is responsible for sudden oak death in the United States, sudden larch death in Europe, and ramorum blight in North America and Europe. We sequenced the genomes of 107 isolates to determine how this pathogen can overcome the invasion paradox. Mitotic recombination (MR) associated with transposons and low gene density has generated runs of homozygosity (ROH) affecting 2,698 genes, resulting in novel genotypic diversity within the lineages. One ROH enriched in effectors was fixed in the NA1 lineage. An independent ROH affected the same scaffold in the EU1 lineage, suggesting an MR hot spot and a selection target. Differences in host infection between EU1 isolates with and without the ROH suggest that they may differ in aggressiveness. Non-core regions (not shared by all lineages) had signatures of accelerated evolution and were enriched in putative pathogenicity genes and transposons. There was a striking pattern of gene loss, including all effectors, in the non-core EU2 genome. Positive selection was observed in 8.0% of RxLR and 18.8% of Crinkler effector genes compared with 0.9% of the core eukaryotic gene set. We conclude that the P. ramorum lineages are diverging via a rapidly evolving non-core genome and that the invasive asexual lineages are not clonal, but display genotypic diversity caused by MR. IMPORTANCE Alien species are often successful invaders in new environments, despite the introduction of a few isolates with a reduced genetic pool. This is called the genetic paradox of invasion. We found two mechanisms by which the invasive forest pathogen causing sudden oak and sudden larch death can evolve. Extensive mitotic recombination producing runs of homozygosity generates genotypic diversity even in the absence of sexual reproduction, and rapid turnover of genes in the non-core, or nonessential portion of genome not shared by all isolates, allows pathogenicity genes to evolve rapidly or be eliminated while retaining essential genes. Mitotic recombination events occur in genomic hot spots, resulting in similar ROH patterns in different isolates or groups; one ROH, independently generated in two different groups, was enriched in pathogenicity genes and may be a target for selection. This provides important insights into the evolution of invasive alien pathogens and their potential for adaptation and future persistence.
format	article
author	Angela L. Dale Nicolas Feau Sydney E. Everhart Braham Dhillon Barbara Wong Julie Sheppard Guillaume J. Bilodeau Avneet Brar Javier F. Tabima Danyu Shen Clive M. Brasier Brett M. Tyler Niklaus J. Grünwald Richard C. Hamelin
author_facet	Angela L. Dale Nicolas Feau Sydney E. Everhart Braham Dhillon Barbara Wong Julie Sheppard Guillaume J. Bilodeau Avneet Brar Javier F. Tabima Danyu Shen Clive M. Brasier Brett M. Tyler Niklaus J. Grünwald Richard C. Hamelin
author_sort	Angela L. Dale
title	Mitotic Recombination and Rapid Genome Evolution in the Invasive Forest Pathogen <italic toggle="yes">Phytophthora ramorum</italic>
title_short	Mitotic Recombination and Rapid Genome Evolution in the Invasive Forest Pathogen <italic toggle="yes">Phytophthora ramorum</italic>
title_full	Mitotic Recombination and Rapid Genome Evolution in the Invasive Forest Pathogen <italic toggle="yes">Phytophthora ramorum</italic>
title_fullStr	Mitotic Recombination and Rapid Genome Evolution in the Invasive Forest Pathogen <italic toggle="yes">Phytophthora ramorum</italic>
title_full_unstemmed	Mitotic Recombination and Rapid Genome Evolution in the Invasive Forest Pathogen <italic toggle="yes">Phytophthora ramorum</italic>
title_sort	mitotic recombination and rapid genome evolution in the invasive forest pathogen <italic toggle="yes">phytophthora ramorum</italic>
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/7ed7ecba6ade42a4a23f9b0a8a03f8c3
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Mitotic Recombination and Rapid Genome Evolution in the Invasive Forest Pathogen <italic toggle="yes">Phytophthora ramorum</italic>

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