The Interspecific Fungal Hybrid <italic toggle="yes">Verticillium longisporum</italic> Displays Subgenome-Specific Gene Expression

ABSTRACT Hybridization is an important evolutionary mechanism that can enable organisms to adapt to environmental challenges. It has previously been shown that the fungal allodiploid species Verticillium longisporum, the causal agent of verticillium stem striping in rapeseed, originated from at leas...

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Autores principales:	Jasper R. L. Depotter, Fabian van Beveren, Luis Rodriguez-Moreno, H. Martin Kramer, Edgar A. Chavarro Carrero, Gabriel L. Fiorin, Grardy C. M. van den Berg, Thomas A. Wood, Bart P. H. J. Thomma, Michael F. Seidl
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2021
Materias:	allopolyploidization Verticillium stem striping genome rearrangements gene conversion haploidization mosaic genome Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/bbeb04c0250741998b570f7f97c03c51
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spelling	oai:doaj.org-article:bbeb04c0250741998b570f7f97c03c512021-11-10T18:37:51ZThe Interspecific Fungal Hybrid <italic toggle="yes">Verticillium longisporum</italic> Displays Subgenome-Specific Gene Expression10.1128/mBio.01496-212150-7511https://doaj.org/article/bbeb04c0250741998b570f7f97c03c512021-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01496-21https://doaj.org/toc/2150-7511ABSTRACT Hybridization is an important evolutionary mechanism that can enable organisms to adapt to environmental challenges. It has previously been shown that the fungal allodiploid species Verticillium longisporum, the causal agent of verticillium stem striping in rapeseed, originated from at least three independent hybridization events between two haploid Verticillium species. To reveal the impact of genome duplication as a consequence of hybridization, we studied the genome and transcriptome dynamics upon two independent V. longisporum hybridization events, represented by the hybrid lineages “A1/D1” and “A1/D3.” We show that V. longisporum genomes are characterized by extensive chromosomal rearrangements, including between parental chromosomal sets. V. longisporum hybrids display signs of evolutionary dynamics that are typically associated with the aftermath of allodiploidization, such as haploidization and more relaxed gene evolution. The expression patterns of the two subgenomes within the two hybrid lineages are more similar than those of the shared A1 parent between the two lineages, showing that the expression patterns of the parental genomes homogenized within a lineage. However, as genes that display differential parental expression in planta do not typically display the same pattern in vitro, we conclude that subgenome-specific responses occur in both lineages. Overall, our study uncovers genomic and transcriptomic plasticity during the evolution of the filamentous fungal hybrid V. longisporum and illustrates its adaptive potential. IMPORTANCE Verticillium is a genus of plant-associated fungi that includes a few plant pathogens that collectively affect a wide range of hosts. On several occasions, haploid Verticillium species hybridized into the stable allodiploid species Verticillium longisporum, which is, in contrast to haploid Verticillium species, a Brassicaceae specialist. Here, we studied the evolutionary genome and transcriptome dynamics of V. longisporum and the impact of the hybridization. V. longisporum genomes display a mosaic structure due to genomic rearrangements between the parental chromosome sets. Similar to other allopolyploid hybrids, V. longisporum displays an ongoing loss of heterozygosity and more relaxed gene evolution. Also, differential parental gene expression is observed, with enrichment for genes that encode secreted proteins. Intriguingly, the majority of these genes display subgenome-specific responses under differential growth conditions. In conclusion, hybridization has incited the genomic and transcriptomic plasticity that enables adaptation to environmental changes in a parental allele-specific fashion.Jasper R. L. DepotterFabian van BeverenLuis Rodriguez-MorenoH. Martin KramerEdgar A. Chavarro CarreroGabriel L. FiorinGrardy C. M. van den BergThomas A. WoodBart P. H. J. ThommaMichael F. SeidlAmerican Society for MicrobiologyarticleallopolyploidizationVerticillium stem stripinggenome rearrangementsgene conversionhaploidizationmosaic genomeMicrobiologyQR1-502ENmBio, Vol 12, Iss 4 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	allopolyploidization Verticillium stem striping genome rearrangements gene conversion haploidization mosaic genome Microbiology QR1-502
spellingShingle	allopolyploidization Verticillium stem striping genome rearrangements gene conversion haploidization mosaic genome Microbiology QR1-502 Jasper R. L. Depotter Fabian van Beveren Luis Rodriguez-Moreno H. Martin Kramer Edgar A. Chavarro Carrero Gabriel L. Fiorin Grardy C. M. van den Berg Thomas A. Wood Bart P. H. J. Thomma Michael F. Seidl The Interspecific Fungal Hybrid <italic toggle="yes">Verticillium longisporum</italic> Displays Subgenome-Specific Gene Expression
description	ABSTRACT Hybridization is an important evolutionary mechanism that can enable organisms to adapt to environmental challenges. It has previously been shown that the fungal allodiploid species Verticillium longisporum, the causal agent of verticillium stem striping in rapeseed, originated from at least three independent hybridization events between two haploid Verticillium species. To reveal the impact of genome duplication as a consequence of hybridization, we studied the genome and transcriptome dynamics upon two independent V. longisporum hybridization events, represented by the hybrid lineages “A1/D1” and “A1/D3.” We show that V. longisporum genomes are characterized by extensive chromosomal rearrangements, including between parental chromosomal sets. V. longisporum hybrids display signs of evolutionary dynamics that are typically associated with the aftermath of allodiploidization, such as haploidization and more relaxed gene evolution. The expression patterns of the two subgenomes within the two hybrid lineages are more similar than those of the shared A1 parent between the two lineages, showing that the expression patterns of the parental genomes homogenized within a lineage. However, as genes that display differential parental expression in planta do not typically display the same pattern in vitro, we conclude that subgenome-specific responses occur in both lineages. Overall, our study uncovers genomic and transcriptomic plasticity during the evolution of the filamentous fungal hybrid V. longisporum and illustrates its adaptive potential. IMPORTANCE Verticillium is a genus of plant-associated fungi that includes a few plant pathogens that collectively affect a wide range of hosts. On several occasions, haploid Verticillium species hybridized into the stable allodiploid species Verticillium longisporum, which is, in contrast to haploid Verticillium species, a Brassicaceae specialist. Here, we studied the evolutionary genome and transcriptome dynamics of V. longisporum and the impact of the hybridization. V. longisporum genomes display a mosaic structure due to genomic rearrangements between the parental chromosome sets. Similar to other allopolyploid hybrids, V. longisporum displays an ongoing loss of heterozygosity and more relaxed gene evolution. Also, differential parental gene expression is observed, with enrichment for genes that encode secreted proteins. Intriguingly, the majority of these genes display subgenome-specific responses under differential growth conditions. In conclusion, hybridization has incited the genomic and transcriptomic plasticity that enables adaptation to environmental changes in a parental allele-specific fashion.
format	article
author	Jasper R. L. Depotter Fabian van Beveren Luis Rodriguez-Moreno H. Martin Kramer Edgar A. Chavarro Carrero Gabriel L. Fiorin Grardy C. M. van den Berg Thomas A. Wood Bart P. H. J. Thomma Michael F. Seidl
author_facet	Jasper R. L. Depotter Fabian van Beveren Luis Rodriguez-Moreno H. Martin Kramer Edgar A. Chavarro Carrero Gabriel L. Fiorin Grardy C. M. van den Berg Thomas A. Wood Bart P. H. J. Thomma Michael F. Seidl
author_sort	Jasper R. L. Depotter
title	The Interspecific Fungal Hybrid <italic toggle="yes">Verticillium longisporum</italic> Displays Subgenome-Specific Gene Expression
title_short	The Interspecific Fungal Hybrid <italic toggle="yes">Verticillium longisporum</italic> Displays Subgenome-Specific Gene Expression
title_full	The Interspecific Fungal Hybrid <italic toggle="yes">Verticillium longisporum</italic> Displays Subgenome-Specific Gene Expression
title_fullStr	The Interspecific Fungal Hybrid <italic toggle="yes">Verticillium longisporum</italic> Displays Subgenome-Specific Gene Expression
title_full_unstemmed	The Interspecific Fungal Hybrid <italic toggle="yes">Verticillium longisporum</italic> Displays Subgenome-Specific Gene Expression
title_sort	interspecific fungal hybrid <italic toggle="yes">verticillium longisporum</italic> displays subgenome-specific gene expression
publisher	American Society for Microbiology
publishDate	2021
url	https://doaj.org/article/bbeb04c0250741998b570f7f97c03c51
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The Interspecific Fungal Hybrid <italic toggle="yes">Verticillium longisporum</italic> Displays Subgenome-Specific Gene Expression

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