Universität zu Köln

Depotter, Jasper R. L., van Beveren, Fabian ORCID: 0000-0003-2883-3090, Rodriguez-Moreno, Luis, Kramer, H. Martin, Carrero, Edgar A. Chavarro, Fiorin, Gabriel L., van den Berg, Grardy C. M., Wood, Thomas A., Thomma, Bart P. H. J. and Seidl, Michael F. (2021). The Interspecific Fungal Hybrid Verticillium longisporum Displays Subgenome-Specific Gene Expression. mBio, 12 (4). WASHINGTON: AMER SOC MICROBIOLOGY. ISSN 2150-7511

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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.

Item Type:	Journal Article
Creators:	Creators Email ORCID ORCID Put Code Depotter, Jasper R. L. UNSPECIFIED UNSPECIFIED UNSPECIFIED van Beveren, Fabian UNSPECIFIED orcid.org/0000-0003-2883-3090 UNSPECIFIED Rodriguez-Moreno, Luis UNSPECIFIED UNSPECIFIED UNSPECIFIED Kramer, H. Martin UNSPECIFIED UNSPECIFIED UNSPECIFIED Carrero, Edgar A. Chavarro UNSPECIFIED UNSPECIFIED UNSPECIFIED Fiorin, Gabriel L. UNSPECIFIED UNSPECIFIED UNSPECIFIED van den Berg, Grardy C. M. UNSPECIFIED UNSPECIFIED UNSPECIFIED Wood, Thomas A. UNSPECIFIED UNSPECIFIED UNSPECIFIED Thomma, Bart P. H. J. UNSPECIFIED UNSPECIFIED UNSPECIFIED Seidl, Michael F. UNSPECIFIED UNSPECIFIED UNSPECIFIED
URN:	urn:nbn:de:hbz:38-588527
DOI:	10.1128/mBio.01496-21
Journal or Publication Title:	mBio
Volume:	12
Number:	4
Date:	2021
Publisher:	AMER SOC MICROBIOLOGY
Place of Publication:	WASHINGTON
ISSN:	2150-7511
Language:	English
Faculty:	Unspecified
Divisions:	Unspecified
Subjects:	no entry
Uncontrolled Keywords:	Keywords Language MULTIPLE SEQUENCE ALIGNMENT; PHYLOGENETIC ANALYSIS; GENOME DUPLICATIONS; LEVEL DOMINANCE; YEAST HYBRID; EVOLUTION; HYBRIDIZATION; EMERGENCE; ANNOTATION; PATHOGENS Multiple languages Microbiology Multiple languages
URI:	http://kups.ub.uni-koeln.de/id/eprint/58852