Staff Publications

Staff Publications

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    'Staff publications' is the digital repository of Wageningen University & Research

    'Staff publications' contains references to publications authored by Wageningen University staff from 1976 onward.

    Publications authored by the staff of the Research Institutes are available from 1995 onwards.

    Full text documents are added when available. The database is updated daily and currently holds about 240,000 items, of which 72,000 in open access.

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Dynamic virulence-related regions of the plant pathogenic fungus Verticillium dahliae display enhanced sequence conservation
Depotter, Jasper R.L. ; Shi-Kunne, Xiaoqian ; Missonnier, Hélène ; Liu, Tingli ; Faino, Luigi ; Berg, Grardy C.M. van den; Wood, Thomas A. ; Zhang, Baolong ; Jacques, Alban ; Seidl, Michael F. ; Thomma, Bart P.H.J. - \ 2019
Molecular Ecology 28 (2019)15. - ISSN 0962-1083 - p. 3482 - 3495.
comparative genomics - effector - genome evolution - mutagenesis - two-speed genome - Verticillium wilt

Plant pathogens continuously evolve to evade host immune responses. During host colonization, many fungal pathogens secrete effectors to perturb such responses, but these in turn may become recognized by host immune receptors. To facilitate the evolution of effector repertoires, such as the elimination of recognized effectors, effector genes often reside in genomic regions that display increased plasticity, a phenomenon that is captured in the two-speed genome hypothesis. The genome of the vascular wilt fungus Verticillium dahliae displays regions with extensive presence/absence polymorphisms, so-called lineage-specific regions, that are enriched in in planta-induced putative effector genes. As expected, comparative genomics reveals differential degrees of sequence divergence between lineage-specific regions and the core genome. Unanticipated, lineage-specific regions display markedly higher sequence conservation in coding as well as noncoding regions than the core genome. We provide evidence that disqualifies horizontal transfer to explain the observed sequence conservation and conclude that sequence divergence occurs at a slower pace in lineage-specific regions of the V. dahliae genome. We hypothesize that differences in chromatin organisation may explain lower nucleotide substitution rates in the plastic, lineage-specific regions of V. dahliae.

In silico prediction and characterisation of secondary metabolite clusters in the plant pathogenic fungus Verticillium dahliae
Shi-Kunne, Xiaoqian ; Pedro Jové, Roger de; Depotter, Jasper R.L. ; Ebert, Malaika K. ; Seidl, Michael F. ; Thomma, Bart P.H.J. - \ 2019
FEMS Microbiology Letters 366 (2019)7. - ISSN 0378-1097
fungi - genomics - natural product - pathogen - Verticillium

Fungi are renowned producers of natural compounds, also known as secondary metabolites (SMs) that display a wide array of biological activities. Typically, the genes that are involved in the biosynthesis of SMs are located in close proximity to each other in so-called secondary metabolite clusters. Many plant-pathogenic fungi secrete SMs during infection in order to promote disease establishment, for instance as cytocoxic compounds. Verticillium dahliae is a notorious plant pathogen that can infect over 200 host plants worldwide. However, the SM repertoire of this vascular pathogen remains mostly uncharted. To unravel the potential of V. dahliae to produce SMs, we performed in silico predictions and in-depth analyses of its secondary metabolite clusters. Using distinctive traits of gene clusters and the conserved signatures of core genes 25 potential SM gene clusters were identified. Subsequently, phylogenetic and comparative genomics analyses were performed, revealing that two putative siderophores, ferricrocin and TAFC, DHN-melanin and fujikurin may belong to the SM repertoire of V. dahliae.

The Genome of the Fungal Pathogen Verticillium dahliae Reveals Extensive Bacterial to Fungal Gene Transfer
Shi-Kunne, Xiaoqian ; Kooten, Mathijs van; Depotter, Jasper R.L. ; Thomma, Bart P.H.J. ; Seidl, Michael F. - \ 2019
Genome Biology and Evolution 11 (2019)3. - ISSN 1759-6653 - p. 855 - 868.
Verticillium - ascomycete - bacteria - fungus - horizontal gene transfer

Horizontal gene transfer (HGT) involves the transmission of genetic material between distinct evolutionary lineages and can be an important source of biological innovation. Reports of interkingdom HGT to eukaryotic microbial pathogens have accumulated over recent years. Verticillium dahliae is a notorious plant pathogen that causes vascular wilt disease on hundreds of plant species, resulting in high economic losses every year. Previously, the effector gene Ave1 and a glucosyltransferase-encoding gene were identified as virulence factor-encoding genes that were proposed to be horizontally acquired from a plant and a bacterial donor, respectively. However, to what extent HGT contributed to the overall genome composition of V. dahliae remained elusive. Here, we systematically searched for evidence of interkingdom HGT events in the genome of V. dahliae and provide evidence for extensive horizontal gene acquisition from bacterial origin.

Evolution within the fungal genus Verticillium is characterized by chromosomal rearrangement and gene loss
Shi-Kunne, Xiaoqian ; Faino, Luigi ; Berg, Grardy C.M. van den; Thomma, Bart P.H.J. ; Seidl, Michael F. - \ 2018
Environmental Microbiology 20 (2018)4. - ISSN 1462-2912 - p. 1362 - 1373.
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 plant 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 genes that are shared at least between two species, only 200–600 species-specific genes occur. Intriguingly, these species-specific genes show different features than the shared genes.
Genome plasticity impacts adaptive genome evolution in the vascular wilt pathogen Verticillium
Seidl, M.F. ; Faino, L. ; Cook III, D.E. ; Kramer, H.M. ; Shi-Kunne, X. ; Berg-Velthuis, G.C.M. van den; Thomma, B.P.H.J. - \ 2017
In: Abstract Book 29th Fungal Genetics Conference Asilomar 17, Pacific Grove, CA, USA 14-19 March 2017. - Genetics Society of America - p. 80 - 81.
Genome plasticity enables organisms to adapt to environmental changes and to occupy novel niches. This is established by mechanisms ranging from single-nucleotide polymorphisms to large-scale chromosomal variations, all of which contribute to differences in chromosomal size, organization and gene content. While these mechanisms operate in all organisms, they are particularly relevant for plant pathogens that engage in a co-evolutionary arms race with their hosts. Plant pathogens secrete so-called effectors that contribute to host colonization and counteract host immunity. Effector genes often cluster in highly plastic, transposon-rich genomic regions. However, mechanistic understanding of the evolution of these plastic genomic regions remains scarce. We study these molecular mechanisms in the fungal genus Verticillium that contains economically and ecologically important plant pathogens, among which Verticillium dahliae is the most notorious pathogen that causes vascular wilt disease on >200 plant species. Using long-read sequencing technology, we completely assembled two V. dahliae strains. By comparative genomics, we established that transposable elements play important roles in shaping the genome of V. dahliae. Plastic genomic regions in V. dahliae that contain all known effectors evolve by extensive genomic rearrangements that are mediated by erroneous double-strand breaks, often over transposons. Extensive genomic rearrangements are not only restricted to V. dahliae, but also occur in related Verticillium species. Furthermore, recent segmental duplications are enhanced in the plastic regions. These regions, in contrast to the core genome, are also enriched in active transposons that further contribute to local plasticity. In fungi, transposons are located in tightly condensed chromatin, so called heterochromatin, that is supposed to suppress transposon activity and repress structural variations. In contrast, many fungal pathogens have highly plastic transposon-rich regions. Therefore, research into chromatin opens new avenues to link genome organization, genome plasticity and adaptive genome evolution in fungal pathogens.
The two-speed genome of Verticillium dahliae mediates emergence of potent virulence factors
Thomma, B.P.H.J. ; Faino, L. ; Li, J. ; Shi-Kunne, X. ; Depotter, J.R.L. ; Kramer, H.M. ; Berg-Velthuis, G.C.M. van den; Cook III, David ; Rövenich, H.J. ; Seidl, M.F. - \ 2017
In: Book of Abstracts 29th Fungal Genetics Conference Asilomar 17, Pacific Grove, CA, USA 14-19 March 2017. - - p. 4 - 4.
Genomic plasticity enables adaptation to changing environments, which is especially relevant for pathogens that engage in “arms races” with their hosts. In many pathogens, virulence genes reside in highly variable, transposon-rich, physically distinct genomic compartments. However, understanding of the evolution of such compartments, and the role of transposons therein, remains limited. We show that transposons are the major driving force for adaptive genome evolution in the fungal plant pathogen Verticillium dahliae, and that highly variable lineage-specific (LS) regions evolved by genomic rearrangements that are mediated by erroneous double-strand repair, often utilizing transposons. Remarkably, LS regions are enriched in active transposons, which may contribute to local genome plasticity. Thus, we provide evidence for genome shaping by transposons, both in an active and passive manner, which impacts the evolution of V. dahliae virulence. Based on this knowledge, we are now able to identify crucial virulence factors of V. dahliae, which also allows investigating causal relationships between particular effectors and pathotypes.
Mind the gap; seven reasons to close fragmented genome assemblies
Thomma, B. ; Seidl, M.F. ; Shi-Kunne, X. ; Cook III, D.E. ; Bolton, M.D. ; Kan, J.A.L. van; Faino, L. - \ 2016
Fungal Genetics and Biology 90 (2016). - ISSN 1087-1845 - p. 24 - 30.
Like other domains of life, research into the biology of filamentous microbes has greatly benefited from the advent of whole-genome sequencing. Next-generation sequencing (NGS) technologies have revolutionized sequencing, making genomic sciences accessible to many academic laboratories including those that study non-model organisms. Thus, hundreds of fungal genomes have been sequenced and are publically available today, although these initiatives have typically yielded considerably fragmented genome assemblies that often lack large contiguous genomic regions. Many important genomic features are contained in intergenic DNA that is often missing in current genome assemblies, and recent studies underscore the significance of non-coding regions and repetitive elements for the life style, adaptability and evolution of many organisms. The study of particular types of genetic elements, such as telomeres, centromeres, repetitive elements, effectors, and clusters of co-regulated genes, but also of phenomena such as structural rearrangements, genome compartmentalization and epigenetics, greatly benefits from having a contiguous and high-quality, preferably even complete and gapless, genome assembly. Here we discuss a number of important reasons to produce gapless, finished, genome assemblies to help answer important biological questions.
The occurrence of chromosomal rearrangements in the fungal genus Verticillium
Shi-Kunne, Xiaoqian ; Bolton, M.D. ; Seidl, M.F. ; Faino, L. ; Thomma, B. - \ 2015
In: Book of Abstracts 28th Fungal Genetics Conference. - - p. 165 - 165.
Based on a recent comparative population genomics study, extensive chromosomal rearrangements between strains of the plant pathogenic species V. dahliae have been found (de Jonge et al., 2013). The rearrangements result in the occurrence of lineage-specific genomic regions that appear to be greatly enriched for in planta-expressed genes that encode virulence factors that enable host colonization. Thus, it is speculated that genomic rearrangements foster evolution of aggressiveness in the asexual pathogen V. dahliae (de Jonge et al., 2013). In this project, we aim to investigate the occurrence and regulation of chromosomal rearrangements in the genus Verticillium that comprises plant pathogenic (V. dahliae, V. longisporum, V. albo-atrum, V. alfafae, V. nonalfalfae), and saprophytic and weakly pathogenic (V. tricorpus, V. zagamsianum, V. nubilum, V. isaacii and V. klebahnii) species. We hypothesize that chromosomal rearrangements occur in the virulent plant pathogens and are not observed in the weak pathogens and saprophytes. To investigate this hypothesis, the genomes of multiple strains of each of the species within the Verticillium genus were sequenced and assembled to investigate chromosomal structures within and between each of the species. Furthermore, we investigated chromosomal size polymorphisms based on karyotyping. Collectively, our data show that inter-chromosomal rearrangements are not confined to pathogenic Verticillium spp.
Draft genome sequence of a strain of cosmopolitan fungus Trichoderma atroviride
Shi-Kunne, X. ; Seidl, M.F. ; Faino, L. ; Thomma, B.P.H.J. - \ 2015
Genome Announcements 3 (2015)3. - ISSN 2169-8287 - 2 p.
An unknown fungus has been isolated as a contaminant of in vitro-grown fungal cultures. In an attempt to identify the contamination, we isolated the causal agent and performed whole-genome sequencing. BLAST analysis of the internal transcribed spacer (ITS) sequence against the NCBI database showed 100% identity to Trichoderma atroviride, and further alignment of the genome assembly confirmed the unknown fungus to be T. atroviride. Here, we report the draft genome sequence of a T. atroviride strain.
Genome plasticity mediated by transposable elements drives the evolution of virulence in the vascular wilt pathogen Verticillium dahliae
Seidl, M.F. ; Faino, L. ; Cook III, D.E. ; Shi-Kunne, Xiaoqian ; Berg, G.C.M. van den; Thomma, B.P.H.J. - \ 2015
In: Book of Abstracts 28th Fungal Genetics Conference. - - p. 62 - 62.
Verticillium dahliae is a soil-borne pathogen that aggressively colonizes hundreds of host plants, including high value crops such as tomato and potato, leading to the formation of vascular wilt disease. Resistance in the host population exert selective pressure on the pathogen forcing the rapid evolution of adaptive traits to successfully participate in the arms race with the host. By comparative genomics of the V. dahliae population, we recently revealed genomic rearrangements that facilitate the gain and loss of genetic material and establish highly dynamic lineage-specific (LS) regions. LS regions are enriched for transposable elements (TEs) and in planta induced effector genes encoding secreted protein that significantly contribute to aggressiveness towards the host, and thus have been hypothesized to contribute to the genome plasticity required for adaptive genome evolution. However, the factors that drive genome plasticity in V. dahliae remain enigmatic. Using long-read sequencing technologies, we re-sequenced two V. dahliae strains and analyzed the previously identified genomic rearrangements in unprecedented detail, revealing multiple genomic breakpoints down to the nucleotide level. Genomic breakpoints are flanked by multiple TEs, suggesting that these elements play essential roles in their formation. Comparative analyses of V. dahliae with the recently sequenced non-pathogenic Verticillium tricorpus revealed a highly expanded TE repertoire in pathogenic V. dahliae, where in planta induced effector candidates, but also other genes encoding secreted proteins, are frequently flanked by TEs. Additionally, whole-genome bisulfite sequencing of V. dahliae identified DNA methylation predominantly targeting TEs. In fungi, inactivation of TEs by DNA methylation is common, and we hypothesize that it could also influence the expression of nested effector candidates, thereby providing yet another route how TEs can affect the interaction between the pathogen and its host. In summary, we highlight the profound role of TEs on the evolution of virulence in the vascular wilt pathogen V. dahliae.
Evolution of virulence in the vascular wilt pathogen Verticillium dahliae
Faino, L. ; Seidl, M.F. ; Cook III, D.E. ; Shi-Kunne, Xiaoqian ; Boshoven, J.C. ; Rövenich, H.J. ; Damme, M.M.A. van; Li, J. ; Rojas Padilla, J.E. ; Song, Y. ; Valkenburg, D.J. ; Berg, G.C.M. van den; Thomma, B.P.H.J. - \ 2015
In: Book of Abstracts 28th Fungal Genetics Conference. - - p. 4 - 4.
Fungi cause severe crop losses and threaten food security worldwide. The soil-borne fungal pathogen Verticillium dahliae causes vascular wilt disease on hundreds of plant species, and disease control is challenging because resistance in plants is relatively rare. Moreover, V. dahliae has a flexible genome allowing it to escape host immunity and maintain aggressiveness. So far, knowledge on mechanisms governing this genomic flexibility remains limited. Through comparative population genomics we have started to unravel mechanisms to establish the genomic diversity that is essential for adaptive genome co-evolution during the continued arms race with host plants. To this end, two V. dahliae genomes were assembled from telomere-to-telomere using long-read sequencing technology and optical mapping, and compared these to the genomes of other Verticillium spp., revealing a pre-speciation genome duplication event. Comparative genomics using the two finished V. dahliae genomes furthermore revealed recent segmental duplications that established lineage-specific regions. Interestingly, these regions are enriched for in planta-expressed effector genes encoding secreted proteins that enable host colonization, and thus contribute to the evolution of virulence. Our evidence suggests that error-prone homology-dependent DNA repair has caused genomic rearrangements, leading to extensive structural variations. Re-sequencing of additional strains showed that independent losses of genetic material favored the escape of host recognition and, likely, host specificity. We propose that evolution of V. dahliae is linked to segmental genome duplications mediated by improperly repaired DNA breaks.
The genome of the saprophytic fungus Verticillium tricorpus reveals a complex effector repertoire resembling that of its pathogenic relatives
Seidl, M.F. ; Faino, L. ; Shi-Kunne, Xiaoqian ; Berg, G.C.M. van den; Bolton, M.D. ; Thomma, B.P.H.J. - \ 2015
Molecular Plant-Microbe Interactions 28 (2015)3. - ISSN 0894-0282 - p. 362 - 373.
chitin-triggered immunity - hidden markov model - rna-seq - eukaryotic genomes - signal peptides - plant-pathogens - protein family - evolution - annotation - wilt
Vascular wilts caused by Verticillium spp. are destructive plant diseases, affecting hundreds of hosts. Only few Verticillium spp. are causal agents of vascular wilt diseases, of which V. dahliae is the most notorious pathogen, and several V. dahliae genomes are available. In contrast, V. tricorpus is mainly known as saprophyte and causal agent of opportunistic infections. Based on a hybrid approach that combines second and third generation sequencing, a near-gapless V. tricorpus genome assembly was obtained. With comparative genomics, we aimed to identify genomic features in V. dahliae that confer the ability to cause vascular wilt disease. Unexpectedly, both species encode similar effector repertoires and share a genomic structure with genes encoding secreted proteins clustered in genomic islands. Intriguingly, V. tricorpus contains significantly less repetitive elements and an extended spectrum of secreted carbohydrate-active enzymes when compared with V. dahliae. In conclusion, we highlight the technical advances of a hybrid sequencing and assembly approach and reveal that the saprophyte V. tricorpus shares many hallmark features with V. dahliae.
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