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van den Berg, G.

Publications and source records attributed to van den Berg, G..

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Homogenization of sub-genome secretome gene expression patterns in the allodiploid fungus Verticillium longisporum

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, causal agent of Verticillium stem striping in rape seed, has originated from at least three independent hybridization events between two haploid Verticillium species. To reveal the impact of genome duplication as a consequence of the 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 the 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 a more relaxed gene evolution. Expression patterns of the two sub-genomes within the two hybrid lineages are more similar than those of the shared A1 parent between the two lineages, showing that 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 sub-genome-specific responses occur in both lineages. Overall, our study uncovers the genomic and transcriptomic plasticity during evolution of the filamentous fungal hybrid V. longisporum and illustrate its adaptive potential. ImportanceVerticillium is a genus of plant-associated fungi that include a handful of 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 do genomic rearrangements between the parental chromosome sets. Similar to other allopolyploid hybrids, V. longisporum displays an ongoing loss of heterozygosity and a more relaxed gene evolution. Also, differential parental gene expression is observed, with an enrichment for genes that encode secreted proteins. Intriguingly, the majority of these genes displays sub-genome-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.

microbiology

Dynamic virulence-related regions of the fungal plant pathogen Verticillium dahliae display remarkably enhanced sequence conservation

Selection pressure impacts genomes unevenly, as different genes adapt with differential speed to establish an organisms optimal fitness. Plant pathogens co-evolve with their hosts, which implies continuously adaption to evade host immunity. Effectors are secreted proteins that mediate immunity evasion, but may also typically become recognized by host immune receptors. To facilitate effector repertoire alterations, in many pathogens, effector genes reside in dynamic genomic regions that are thought to display accelerated evolution, a phenomenon that is captured by the two-speed genome hypothesis. The genome of the vascular wilt pathogen Verticillium dahliae has been proposed to obey to a similar two-speed regime with dynamic, lineage-specific regions that are characterized by genomic rearrangements, increased transposable element activity and enrichment in in planta-induced effector genes. However, little is known of the origin of, and sequence diversification within, these lineage-specific regions. Based on comparative genomics among Verticillium spp. we now show differential sequence divergence between core and lineage-specific genomic regions of V. dahliae. Surprisingly, we observed that lineage-specific regions display markedly increased sequence conservation. Since single nucleotide diversity is reduced in these regions, host adaptation seems to be merely achieved through presence/absence polymorphisms. Increased sequence conservation of genomic regions important for pathogenicity is an unprecedented finding for filamentous plant pathogens and signifies the diversity of genomic dynamics in host-pathogen co-evolution.

microbiology

Nuclear and mitochondrial genomes of the hybrid fungal plant pathogen Verticillium longisporum display a mosaic structure

Allopolyploidization, genome duplication through interspecific hybridization, is an important evolutionary mechanism that can enable organisms to adapt to environmental changes or stresses. This increased adaptive potential of allopolyploids can be particularly relevant for plant pathogens in their quest for host immune response evasion. Allodiploidization likely caused the shift in host range of the fungal pathogen plant Verticillium longisporum, as V. longisporum mainly infects Brassicaceae plants in contrast to haploid Verticillium spp. In this study, we investigated the allodiploid genome structure of V. longisporum and its evolution in the hybridization aftermath. The nuclear genome of V. longisporum displays a mosaic structure, as numerous contigs consists of sections of both parental origins. V. longisporum encountered extensive genome rearrangements, whereas the contribution of gene conversion is negligible. Thus, the mosaic genome structure mainly resulted from genomic rearrangements between parental chromosome sets. Furthermore, a mosaic structure was also found in the mitochondrial genome, demonstrating its bi-parental inheritance. In conclusion, the nuclear and mitochondrial genomes of V. longisporum parents interacted dynamically in the hybridization aftermath. Conceivably, novel combinations of DNA sequence of different parental origin facilitated genome stability after hybridization and consecutive niche adaptation of V. longisporum.

genomics

Evolution within the fungal genus Verticillium is characterized by chromosomal rearrangement and gene loss

The fungal genus Verticillium contains ten species, some of which are notorious plant pathogens causing vascular wilt diseases in host plants, while others are known as saprophytes and opportunistic plant pathogens. Whereas the genome of V. dahliae, the most notorious plan pathogen of the genus, has been well characterized, evolution and speciation of other members of the genus received little attention thus far. Here, we sequenced the genomes of the nine haploid Verticillium spp. to study evolutionary trajectories of their divergence from a last common ancestor. Frequent occurrence of chromosomal rearrangement and gene family loss was identified. In addition to ~11,000 core genes that are shared among all species, only 200-600 species-specific genes occur. Intriguingly, these species-specific genes show different features than core genes.

microbiology

Verticillium dahliae LysM effectors differentially contribute to virulence on plant hosts

Chitin-binding LysM effectors contribute to virulence of various plant pathogenic fungi that are causal agents of foliar diseases. Here, we report on LysM effectors of the soil-borne fungal vascular wilt pathogen Verticillium dahliae. Comparative genomics revealed three core LysM effectors that are conserved in a collection of V. dahliae strains. Remarkably, and in contrast to the previously studied LysM effectors of other plant pathogens, no expression of core LysM effectors was monitored in planta in a taxonomically diverse panel of host plants. Moreover, targeted deletion of the individual LysM effector genes in V. dahliae strain JR2 did not compromise virulence in infections on Arabidopsis, tomato or Nicotiana benthamiana. Interestingly, an additional lineage-specific LysM effector is encoded in the genome of V. dahliae strain VdLs17 but not in any other V. dahliae strain sequenced to date. Remarkably, this lineage-specific effector is expressed in planta and contributes to virulence of V. dahliae strain VdLs17 on tomato, but not on Arabidopsis or on N. benthamiana. Functional analysis revealed that this LysM effector binds chitin, is able to suppress chitin-induced immune responses, and protects fungal hyphae against hydrolysis by plant hydrolytic enzymes. Thus, in contrast to the core LysM effectors of V. dahliae, this lineage-specific LysM effector of strain VdLs17 contributes to virulence in planta.

plant biology