The <italic toggle="yes">Parauncinula polyspora</italic> Draft Genome Provides Insights into Patterns of Gene Erosion and Genome Expansion in Powdery Mildew Fungi

ABSTRACT Due to their comparatively small genome size and short generation time, fungi are exquisite model systems to study eukaryotic genome evolution. Powdery mildew fungi present an exceptional case because of their strict host dependency (termed obligate biotrophy) and the atypical size of their...

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Autores principales:	Lamprinos Frantzeskakis, Márk Z. Németh, Mirna Barsoum, Stefan Kusch, Levente Kiss, Susumu Takamatsu, Ralph Panstruga
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	genome evolution plant pathogen fungal genomics transposable elements repeat-induced point mutation Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/0bdcd419743b4f31bd7de6a168cc96b2
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spelling	oai:doaj.org-article:0bdcd419743b4f31bd7de6a168cc96b22021-11-15T15:59:41ZThe <italic toggle="yes">Parauncinula polyspora</italic> Draft Genome Provides Insights into Patterns of Gene Erosion and Genome Expansion in Powdery Mildew Fungi10.1128/mBio.01692-192150-7511https://doaj.org/article/0bdcd419743b4f31bd7de6a168cc96b22019-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01692-19https://doaj.org/toc/2150-7511ABSTRACT Due to their comparatively small genome size and short generation time, fungi are exquisite model systems to study eukaryotic genome evolution. Powdery mildew fungi present an exceptional case because of their strict host dependency (termed obligate biotrophy) and the atypical size of their genomes (>100 Mb). This size expansion is largely due to the pervasiveness of transposable elements on 70% of the genome and is associated with the loss of multiple conserved ascomycete genes required for a free-living lifestyle. To date, little is known about the mechanisms that drove these changes, and information on ancestral powdery mildew genomes is lacking. We report genome analysis of the early-diverged and exclusively sexually reproducing powdery mildew fungus Parauncinula polyspora, which we performed on the basis of a natural leaf epiphytic metapopulation sample. In contrast to other sequenced species of this taxonomic group, the assembled P. polyspora draft genome is surprisingly small (<30 Mb), has a higher content of conserved ascomycete genes, and is sparsely equipped with transposons (<10%), despite the conserved absence of a common defense mechanism involved in constraining repetitive elements. We speculate that transposable element spread might have been limited by this pathogen’s unique reproduction strategy and host features and further hypothesize that the loss of conserved ascomycete genes may promote the evolutionary isolation and host niche specialization of powdery mildew fungi. Limitations associated with this evolutionary trajectory might have been in part counteracted by the evolution of plastic, transposon-rich genomes and/or the expansion of gene families encoding secreted virulence proteins. IMPORTANCE Powdery mildew fungi are widespread and agronomically relevant phytopathogens causing major yield losses. Their genomes have disproportionately large numbers of mobile genetic elements, and they have experienced a significant loss of highly conserved fungal genes. In order to learn more about the evolutionary history of this fungal group, we explored the genome of an Asian oak tree pathogen, Parauncinula polyspora, a species that diverged early during evolution from the remaining powdery mildew fungi. We found that the P. polyspora draft genome is comparatively compact, has a low number of protein-coding genes, and, despite the absence of a dedicated genome defense system, lacks the massive proliferation of repetitive sequences. Based on these findings, we infer an evolutionary trajectory that shaped the genomes of powdery mildew fungi.Lamprinos FrantzeskakisMárk Z. NémethMirna BarsoumStefan KuschLevente KissSusumu TakamatsuRalph PanstrugaAmerican Society for Microbiologyarticlegenome evolutionplant pathogenfungal genomicstransposable elementsrepeat-induced point mutationMicrobiologyQR1-502ENmBio, Vol 10, Iss 5 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	genome evolution plant pathogen fungal genomics transposable elements repeat-induced point mutation Microbiology QR1-502
spellingShingle	genome evolution plant pathogen fungal genomics transposable elements repeat-induced point mutation Microbiology QR1-502 Lamprinos Frantzeskakis Márk Z. Németh Mirna Barsoum Stefan Kusch Levente Kiss Susumu Takamatsu Ralph Panstruga The <italic toggle="yes">Parauncinula polyspora</italic> Draft Genome Provides Insights into Patterns of Gene Erosion and Genome Expansion in Powdery Mildew Fungi
description	ABSTRACT Due to their comparatively small genome size and short generation time, fungi are exquisite model systems to study eukaryotic genome evolution. Powdery mildew fungi present an exceptional case because of their strict host dependency (termed obligate biotrophy) and the atypical size of their genomes (>100 Mb). This size expansion is largely due to the pervasiveness of transposable elements on 70% of the genome and is associated with the loss of multiple conserved ascomycete genes required for a free-living lifestyle. To date, little is known about the mechanisms that drove these changes, and information on ancestral powdery mildew genomes is lacking. We report genome analysis of the early-diverged and exclusively sexually reproducing powdery mildew fungus Parauncinula polyspora, which we performed on the basis of a natural leaf epiphytic metapopulation sample. In contrast to other sequenced species of this taxonomic group, the assembled P. polyspora draft genome is surprisingly small (<30 Mb), has a higher content of conserved ascomycete genes, and is sparsely equipped with transposons (<10%), despite the conserved absence of a common defense mechanism involved in constraining repetitive elements. We speculate that transposable element spread might have been limited by this pathogen’s unique reproduction strategy and host features and further hypothesize that the loss of conserved ascomycete genes may promote the evolutionary isolation and host niche specialization of powdery mildew fungi. Limitations associated with this evolutionary trajectory might have been in part counteracted by the evolution of plastic, transposon-rich genomes and/or the expansion of gene families encoding secreted virulence proteins. IMPORTANCE Powdery mildew fungi are widespread and agronomically relevant phytopathogens causing major yield losses. Their genomes have disproportionately large numbers of mobile genetic elements, and they have experienced a significant loss of highly conserved fungal genes. In order to learn more about the evolutionary history of this fungal group, we explored the genome of an Asian oak tree pathogen, Parauncinula polyspora, a species that diverged early during evolution from the remaining powdery mildew fungi. We found that the P. polyspora draft genome is comparatively compact, has a low number of protein-coding genes, and, despite the absence of a dedicated genome defense system, lacks the massive proliferation of repetitive sequences. Based on these findings, we infer an evolutionary trajectory that shaped the genomes of powdery mildew fungi.
format	article
author	Lamprinos Frantzeskakis Márk Z. Németh Mirna Barsoum Stefan Kusch Levente Kiss Susumu Takamatsu Ralph Panstruga
author_facet	Lamprinos Frantzeskakis Márk Z. Németh Mirna Barsoum Stefan Kusch Levente Kiss Susumu Takamatsu Ralph Panstruga
author_sort	Lamprinos Frantzeskakis
title	The <italic toggle="yes">Parauncinula polyspora</italic> Draft Genome Provides Insights into Patterns of Gene Erosion and Genome Expansion in Powdery Mildew Fungi
title_short	The <italic toggle="yes">Parauncinula polyspora</italic> Draft Genome Provides Insights into Patterns of Gene Erosion and Genome Expansion in Powdery Mildew Fungi
title_full	The <italic toggle="yes">Parauncinula polyspora</italic> Draft Genome Provides Insights into Patterns of Gene Erosion and Genome Expansion in Powdery Mildew Fungi
title_fullStr	The <italic toggle="yes">Parauncinula polyspora</italic> Draft Genome Provides Insights into Patterns of Gene Erosion and Genome Expansion in Powdery Mildew Fungi
title_full_unstemmed	The <italic toggle="yes">Parauncinula polyspora</italic> Draft Genome Provides Insights into Patterns of Gene Erosion and Genome Expansion in Powdery Mildew Fungi
title_sort	<italic toggle="yes">parauncinula polyspora</italic> draft genome provides insights into patterns of gene erosion and genome expansion in powdery mildew fungi
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/0bdcd419743b4f31bd7de6a168cc96b2
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The <italic toggle="yes">Parauncinula polyspora</italic> Draft Genome Provides Insights into Patterns of Gene Erosion and Genome Expansion in Powdery Mildew Fungi

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