Transposon-Mediated Horizontal Transfer of the Host-Specific Virulence Protein ToxA between Three Fungal Wheat Pathogens

ABSTRACT Most known examples of horizontal gene transfer (HGT) between eukaryotes are ancient. These events are identified primarily using phylogenetic methods on coding regions alone. Only rarely are there examples of HGT where noncoding DNA is also reported. The gene encoding the wheat virulence p...

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Autores principales:	Megan C. McDonald, Adam P. Taranto, Erin Hill, Benjamin Schwessinger, Zhaohui Liu, Steven Simpfendorfer, Andrew Milgate, Peter S. Solomon
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	horizontal transfer transposon fungal wheat pathogen adaptive evolution ToxA fungal pathogen Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/46e560643b474d7a99cc5bf5624b7f24
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spelling	oai:doaj.org-article:46e560643b474d7a99cc5bf5624b7f242021-11-15T15:59:42ZTransposon-Mediated Horizontal Transfer of the Host-Specific Virulence Protein ToxA between Three Fungal Wheat Pathogens10.1128/mBio.01515-192150-7511https://doaj.org/article/46e560643b474d7a99cc5bf5624b7f242019-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01515-19https://doaj.org/toc/2150-7511ABSTRACT Most known examples of horizontal gene transfer (HGT) between eukaryotes are ancient. These events are identified primarily using phylogenetic methods on coding regions alone. Only rarely are there examples of HGT where noncoding DNA is also reported. The gene encoding the wheat virulence protein ToxA and the surrounding 14 kb is one of these rare examples. ToxA has been horizontally transferred between three fungal wheat pathogens (Parastagonospora nodorum, Pyrenophora tritici-repentis, and Bipolaris sorokiniana) as part of a conserved ∼14 kb element which contains coding and noncoding regions. Here we used long-read sequencing to define the extent of HGT between these three fungal species. Construction of near-chromosomal-level assemblies enabled identification of terminal inverted repeats on either end of the 14 kb region, typical of a type II DNA transposon. This is the first description of ToxA with complete transposon features, which we call ToxhAT. In all three species, ToxhAT resides in a large (140-to-250 kb) transposon-rich genomic island which is absent in isolates that do not carry the gene (annotated here as toxa−). We demonstrate that the horizontal transfer of ToxhAT between P. tritici-repentis and P. nodorum occurred as part of a large (∼80 kb) HGT which is now undergoing extensive decay. In B. sorokiniana, in contrast, ToxhAT and its resident genomic island are mobile within the genome. Together, these data provide insight into the noncoding regions that facilitate HGT between eukaryotes and into the genomic processes which mask the extent of HGT between these species. IMPORTANCE This work dissects the tripartite horizontal transfer of ToxA, a gene that has a direct negative impact on global wheat yields. Defining the extent of horizontally transferred DNA is important because it can provide clues to the mechanisms that facilitate HGT. Our analysis of ToxA and its surrounding 14 kb suggests that this gene was horizontally transferred in two independent events, with one event likely facilitated by a type II DNA transposon. These horizontal transfer events are now in various processes of decay in each species due to the repeated insertion of new transposons and subsequent rounds of targeted mutation by a fungal genome defense mechanism known as repeat induced point mutation. This work highlights the role that HGT plays in the evolution of host adaptation in eukaryotic pathogens. It also increases the growing body of evidence indicating that transposons facilitate adaptive HGT events between fungi present in similar environments and hosts.Megan C. McDonaldAdam P. TarantoErin HillBenjamin SchwessingerZhaohui LiuSteven SimpfendorferAndrew MilgatePeter S. SolomonAmerican Society for Microbiologyarticlehorizontal transfertransposonfungal wheat pathogenadaptive evolutionToxAfungal pathogenMicrobiologyQR1-502ENmBio, Vol 10, Iss 5 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	horizontal transfer transposon fungal wheat pathogen adaptive evolution ToxA fungal pathogen Microbiology QR1-502
spellingShingle	horizontal transfer transposon fungal wheat pathogen adaptive evolution ToxA fungal pathogen Microbiology QR1-502 Megan C. McDonald Adam P. Taranto Erin Hill Benjamin Schwessinger Zhaohui Liu Steven Simpfendorfer Andrew Milgate Peter S. Solomon Transposon-Mediated Horizontal Transfer of the Host-Specific Virulence Protein ToxA between Three Fungal Wheat Pathogens
description	ABSTRACT Most known examples of horizontal gene transfer (HGT) between eukaryotes are ancient. These events are identified primarily using phylogenetic methods on coding regions alone. Only rarely are there examples of HGT where noncoding DNA is also reported. The gene encoding the wheat virulence protein ToxA and the surrounding 14 kb is one of these rare examples. ToxA has been horizontally transferred between three fungal wheat pathogens (Parastagonospora nodorum, Pyrenophora tritici-repentis, and Bipolaris sorokiniana) as part of a conserved ∼14 kb element which contains coding and noncoding regions. Here we used long-read sequencing to define the extent of HGT between these three fungal species. Construction of near-chromosomal-level assemblies enabled identification of terminal inverted repeats on either end of the 14 kb region, typical of a type II DNA transposon. This is the first description of ToxA with complete transposon features, which we call ToxhAT. In all three species, ToxhAT resides in a large (140-to-250 kb) transposon-rich genomic island which is absent in isolates that do not carry the gene (annotated here as toxa−). We demonstrate that the horizontal transfer of ToxhAT between P. tritici-repentis and P. nodorum occurred as part of a large (∼80 kb) HGT which is now undergoing extensive decay. In B. sorokiniana, in contrast, ToxhAT and its resident genomic island are mobile within the genome. Together, these data provide insight into the noncoding regions that facilitate HGT between eukaryotes and into the genomic processes which mask the extent of HGT between these species. IMPORTANCE This work dissects the tripartite horizontal transfer of ToxA, a gene that has a direct negative impact on global wheat yields. Defining the extent of horizontally transferred DNA is important because it can provide clues to the mechanisms that facilitate HGT. Our analysis of ToxA and its surrounding 14 kb suggests that this gene was horizontally transferred in two independent events, with one event likely facilitated by a type II DNA transposon. These horizontal transfer events are now in various processes of decay in each species due to the repeated insertion of new transposons and subsequent rounds of targeted mutation by a fungal genome defense mechanism known as repeat induced point mutation. This work highlights the role that HGT plays in the evolution of host adaptation in eukaryotic pathogens. It also increases the growing body of evidence indicating that transposons facilitate adaptive HGT events between fungi present in similar environments and hosts.
format	article
author	Megan C. McDonald Adam P. Taranto Erin Hill Benjamin Schwessinger Zhaohui Liu Steven Simpfendorfer Andrew Milgate Peter S. Solomon
author_facet	Megan C. McDonald Adam P. Taranto Erin Hill Benjamin Schwessinger Zhaohui Liu Steven Simpfendorfer Andrew Milgate Peter S. Solomon
author_sort	Megan C. McDonald
title	Transposon-Mediated Horizontal Transfer of the Host-Specific Virulence Protein ToxA between Three Fungal Wheat Pathogens
title_short	Transposon-Mediated Horizontal Transfer of the Host-Specific Virulence Protein ToxA between Three Fungal Wheat Pathogens
title_full	Transposon-Mediated Horizontal Transfer of the Host-Specific Virulence Protein ToxA between Three Fungal Wheat Pathogens
title_fullStr	Transposon-Mediated Horizontal Transfer of the Host-Specific Virulence Protein ToxA between Three Fungal Wheat Pathogens
title_full_unstemmed	Transposon-Mediated Horizontal Transfer of the Host-Specific Virulence Protein ToxA between Three Fungal Wheat Pathogens
title_sort	transposon-mediated horizontal transfer of the host-specific virulence protein toxa between three fungal wheat pathogens
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/46e560643b474d7a99cc5bf5624b7f24
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Transposon-Mediated Horizontal Transfer of the Host-Specific Virulence Protein ToxA between Three Fungal Wheat Pathogens

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