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

2018 ◽  
Author(s):  
Jasper R.L. Depotter ◽  
Xiaoqian Shi-Kunne ◽  
Hélène Missonnier ◽  
Tingli Liu ◽  
Luigi Faino ◽  
...  
Keyword(s):  
Verticillium Dahliae ◽  
Plant Pathogens ◽  
Sequence Divergence ◽  
Sequence Conservation ◽  
In Planta ◽  
Effector Genes ◽  
Accelerated Evolution ◽  
Mediate Immunity ◽  
Element Activity ◽  
Genomic Regions

ABSTRACTSelection pressure impacts genomes unevenly, as different genes adapt with differential speed to establish an organism’s 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.

scholarly journals Verticillium dahliae LysM effectors differentially contribute to virulence on plant hosts

2016 ◽  
Author(s):  
Anja Kombrink ◽  
Hanna Rovenich ◽  
Xiaoqian Shi-Kunne ◽  
Eduardo Rojas-Padilla ◽  
Grardy C.M. van den Berg ◽  
...  
Keyword(s):  
Verticillium Dahliae ◽  
Plant Pathogens ◽  
Hydrolytic Enzymes ◽  
Pathogenic Fungi ◽  
Vascular Wilt ◽  
In Planta ◽  
Targeted Deletion ◽  
Effector Genes ◽  
Specific Effector ◽  
The Individual

SUMMARYChitin-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.

scholarly journals Comparative genomics of Verticillium dahliae isolates reveals the in planta-secreted effector protein recognized in V2 tomato plants

2020 ◽  
Author(s):  
Edgar A. Chavarro-Carrero ◽  
Jasper P. Vermeulen ◽  
David E. Torres ◽  
Toshiyuki Usami ◽  
Henk J. Schouten ◽  
...  
Keyword(s):  
Comparative Genomics ◽  
Verticillium Dahliae ◽  
Plant Pathogens ◽  
Effector Protein ◽  
Vascular Wilt ◽  
In Planta ◽  
Specific Sequence ◽  
Tomato Plants ◽  
Tomato Cultivars ◽  
Race 2

SUMMARYPlant pathogens secrete effector molecules during host invasion to promote host colonization. However, some of these effectors become recognized by host receptors, encoded by resistance genes, to mount defense response and establish immunity. Recently, a novel resistance was identified in tomato, mediated by the single dominant V2 locus, to control strains of the soil-borne vascular wilt fungus Verticillium dahliae that belong to race 2. We performed comparative genomics between race 2 strains and resistance-breaking race 3 strains to identify the avirulence effector that activates V2 resistance, termed Av2. We identified 277 kb of race 2-specific sequence comprising only two genes that encode predicted secreted proteins, both of which are expressed by V. dahliae during tomato colonization. Subsequent functional analysis based on genetic complementation into race 3 isolates confirmed that one of the two candidates encodes the avirulence effector Av2 that is recognized in V2 tomato plants. The identification of Av2 will not only be helpful to select tomato cultivars that are resistant to race 2 strains of V. dahliae, as the corresponding V2 resistance gene has not yet been mapped, but also to monitor adaptations in the V. dahliae population to deployment of V2-containing tomato cultivars in agriculture.

scholarly journals Verticillium dahliae Sge1 Differentially Regulates Expression of Candidate Effector Genes

2013 ◽  
Vol 26 (2) ◽  
pp. 249-256 ◽  
Author(s):  
Parthasarathy Santhanam ◽  
Bart P. H. J. Thomma
Keyword(s):  
Gene Expression ◽  
Verticillium Dahliae ◽  
Radial Growth ◽  
Transcriptional Regulator ◽  
Vascular Wilt ◽  
In Planta ◽  
Effector Gene ◽  
Effector Genes ◽  
Induced Genes

The ascomycete fungus Verticillium dahliae causes vascular wilt diseases in hundreds of dicotyledonous plant species. However, thus far, only few V. dahliae effectors have been identified, and regulators of pathogenicity remain unknown. In this study, we investigated the role of the V. dahliae homolog of Sge1, a transcriptional regulator that was previously implicated in pathogenicity and effector gene expression in Fusarium oxysporum. We show that V. dahliae Sge1 (VdSge1) is required for radial growth and production of asexual conidiospores, because VdSge1 deletion strains display reduced radial growth and reduced conidia production. Furthermore, we show that VdSge1 deletion strains have lost pathogenicity on tomato. Remarkably, VdSge1 is not required for induction of Ave1, the recently identified V. dahliae effector that activates resistance mediated by the Ve1 immune receptor in tomato. Further assessment of the role of VdSge1 in the induction of the nine most highly in-planta-induced genes that encode putative effectors revealed differential activity. Although the expression of one putative effector gene in addition to Ave1 was not affected by VdSge1 deletion, VdSge1 appeared to be required for the expression of six putative effector genes, whereas two of the putative effectors genes were found to be negatively regulated by VdSge1. In conclusion, our data suggest that VdSge1 differentially regulates V. dahliae effector gene expression.

scholarly journals Transposable elements contribute to genome dynamics and gene expression variation in the fungal plant pathogen Verticillium dahliae

2021 ◽  
Author(s):  
David E Torres ◽  
Bart PHJ Thomma ◽  
Michael F Seidl
Keyword(s):  
Gene Expression ◽  
Transposable Elements ◽  
Verticillium Dahliae ◽  
Plant Pathogen ◽  
Plant Pathogens ◽  
Gene Expression Variation ◽  
Expression Variation ◽  
Regulatory Variation ◽  
Fungal Plant Pathogen ◽  
Genomic Regions

AbstractTransposable elements (TEs) are a major source of genetic and regulatory variation in their host genome and are consequently thought to play important roles in evolution. Many fungal and oomycete plant pathogens have evolved dynamic and TE-rich genomic regions containing genes that are implicated in host colonization. TEs embedded in these regions have typically been thought to accelerate the evolution of these genomic compartments, but little is known about their dynamics in strains that harbor them. Here, we used whole-genome sequencing data of 42 strains of the fungal plant pathogen Verticillium dahliae to systematically identify polymorphic TEs that may be implicated in genomic as well as in gene expression variation. We identified 2,523 TE polymorphisms and characterize a subset of 8% of the TEs as dynamic elements that are evolutionary younger, less methylated, and more highly expressed when compared with the remaining 92% of the TE complement. As expected, the dynamic TEs are enriched in the dynamic genomic regions. Besides, we observed an association of dynamic TEs with pathogenicity-related genes that localize nearby and that display high expression levels. Collectively, our analyses demonstrate that TE dynamics in V. dahliae contributes to genomic variation, correlates with expression of pathogenicity-related genes, and potentially impacts the evolution of dynamic genomic regions.Significance statementTransposable elements (TEs) are ubiquitous components of genomes and are major sources of genetic and regulatory variation. Many plant pathogens have evolved TE-rich genomic regions containing genes with roles in host colonization, and TEs are thought to contribute to accelerated evolution of these dynamic regions. We analyzed the fungal plant pathogen Verticillium dahliae to identify TE variation between strains and to demonstrate that polymorphic TEs have specific characteristic that separates them from the majority of TEs. Polymorphic TEs are enriched in dynamic genomic regions and are associated with structural variants and highly expressed pathogenicity-related genes. Collectively, our results provide evidence for the hypothesis that dynamic TEs contribute to increased genomic diversity, functional variation, and the evolution of dynamic genomic regions.

scholarly journals The Pleiades are a cluster of fungal effectors that inhibit host defenses

2021 ◽  
Vol 17 (6) ◽  
pp. e1009641
Author(s):  
Fernando Navarrete ◽  
Nenad Grujic ◽  
Alexandra Stirnberg ◽  
Indira Saado ◽  
David Aleksza ◽  
...  
Keyword(s):  
Plant Pathogens ◽  
Functional Characterization ◽  
Rapid Evolution ◽  
Effector Proteins ◽  
In Planta ◽  
E3 Ligases ◽  
Effector Genes ◽  
Ros Burst ◽  
Molecular Patterns

Biotrophic plant pathogens secrete effector proteins to manipulate the host physiology. Effectors suppress defenses and induce an environment favorable to disease development. Sequence-based prediction of effector function is impeded by their rapid evolution rate. In the maize pathogen Ustilago maydis, effector-coding genes frequently organize in clusters. Here we describe the functional characterization of the pleiades, a cluster of ten effector genes, by analyzing the micro- and macroscopic phenotype of the cluster deletion and expressing these proteins in planta. Deletion of the pleiades leads to strongly impaired virulence and accumulation of reactive oxygen species (ROS) in infected tissue. Eight of the Pleiades suppress the production of ROS upon perception of pathogen associated molecular patterns (PAMPs). Although functionally redundant, the Pleiades target different host components. The paralogs Taygeta1 and Merope1 suppress ROS production in either the cytoplasm or nucleus, respectively. Merope1 targets and promotes the auto-ubiquitination activity of RFI2, a conserved family of E3 ligases that regulates the production of PAMP-triggered ROS burst in plants.

scholarly journals Unconventionally Secreted Manganese Superoxide Dismutase VdSOD3 Is Required for the Virulence of Verticillium dahliae

Agronomy ◽  
2020 ◽  
Vol 11 (1) ◽  
pp. 13
Author(s):  
Li Tian ◽  
Weixia Sun ◽  
Junjiao Li ◽  
Jieyin Chen ◽  
Xiaofeng Dai ◽  
...  
Keyword(s):  
Superoxide Dismutase ◽  
Signal Peptide ◽  
Verticillium Dahliae ◽  
Manganese Superoxide Dismutase ◽  
Plant Pathogens ◽  
Dual Function ◽  
Loss Of Function ◽  
In Planta ◽  
Sod Activity ◽  
Manganese Superoxide

Plant pathogens generally employ superoxide dismutase (SOD) to detoxify host defense reactive oxygen species (ROS), and to scavenge ROS derived from their own metabolism. However, the roles of SODs in an important vascular pathogen, Verticillium dahliae, are unclear. Our previous study has shown that a putative signal-peptide-lacking manganese superoxide dismutase (VdSOD3) is present in the exoproteome of V. dahliae cultured in tissues of host cotton, suggesting that VdSOD3 may be exported out of the fungal cells and contribute to the SOD activity extracellularly. Here, we confirm that the N-terminal of VdSOD3 is not a functional signal peptide by yeast signal trap assay. Despite lacking the signal peptide, the extracellular distribution of VdSOD3 was observed in planta by confocal microscopy during infection. Loss-of-function of VdSOD3 decreased extracellular and intracellular SOD activities of V. dahliae by 58.2% and 17.4%, respectively. Deletion mutant of VdSOD3 had normal growth and conidiation but showed significantly reduced virulence to susceptible hosts of cotton and Nicotiana benthamiana. Our data show that signal-peptide-lacking VdSOD3 is a dual function superoxide dismutase, localizing and functioning intracellularly and extracellularly. Whereas nonessential for viability, VdSOD3 plays a vital role in the virulence of V. dahliae.

scholarly journals Dynamics of Verticillium dahliae race 1 population under managed agricultural ecosystems

BMC Biology ◽  
2021 ◽  
Vol 19 (1) ◽  
Author(s):  
Jie-Yin Chen ◽  
Dan-Dan Zhang ◽  
Jin-Qun Huang ◽  
Ran Li ◽  
Dan Wang ◽  
...  
Keyword(s):  
Transcriptional Regulation ◽  
Verticillium Dahliae ◽  
Plant Pathogens ◽  
Population Genomics ◽  
De Novo ◽  
Sequence Divergence ◽  
Parental Genome ◽  
Nucleotide Polymorphisms ◽  
Agricultural Ecosystems ◽  
Race 1

Abstract Background Plant pathogens and their hosts undergo adaptive changes in managed agricultural ecosystems, by overcoming host resistance, but the underlying genetic adaptations are difficult to determine in natural settings. Verticillium dahliae is a fungal pathogen that causes Verticillium wilt on many economically important crops including lettuce. We assessed the dynamics of changes in the V. dahliae genome under selection in a long-term field experiment. Results In this study, a field was fumigated before the Verticillium dahliae race 1 strain (VdLs.16) was introduced. A derivative 145-strain population was collected over a 6-year period from this field in which a seggregating population of lettuce derived from Vr1/vr1 parents were evaluated. We de novo sequenced the parental genome of VdLs.16 strain and resequenced the derivative strains to analyze the genetic variations that accumulate over time in the field cropped with lettuce. Population genomics analyses identified 2769 single-nucleotide polymorphisms (SNPs) and 750 insertion/deletions (In-Dels) in the 145 isolates compared with the parental genome. Sequence divergence was identified in the coding sequence regions of 378 genes and in the putative promoter regions of 604 genes. Five-hundred and nine SNPs/In-Dels were identified as fixed. The SNPs and In-Dels were significantly enriched in the transposon-rich, gene-sparse regions, and in those genes with functional roles in signaling and transcriptional regulation. Conclusions Under the managed ecosystem continuously cropped to lettuce, the local adaptation of V. dahliae evolves at a whole genome scale to accumulate SNPs/In-Dels nonrandomly in hypervariable regions that encode components of signal transduction and transcriptional regulation.

Key Insights and Research Prospects at the Dawn of the Population Genomics Era for Verticillium dahliae

2021 ◽  
Vol 59 (1) ◽  
Author(s):  
Jie-Yin Chen ◽  
Steven J. Klosterman ◽  
Xiao-Ping Hu ◽  
Xiao-Feng Dai ◽  
Krishna V. Subbarao
Keyword(s):  
Population Structure ◽  
Verticillium Dahliae ◽  
Plant Pathogens ◽  
Population Genomics ◽  
Population Divergence ◽  
Annual Review ◽  
Publication Date ◽  
Disease Symptoms ◽  
Historical Perspectives ◽  
Characteristic Features

The genomics era has ushered in exciting possibilities to examine the genetic bases that undergird the characteristic features of Verticillium dahliae and other plant pathogens. In this review, we provide historical perspectives on some of the salient biological characteristics of V. dahliae, including its morphology, microsclerotia formation, host range, disease symptoms, vascular niche, reproduction, and population structure. The kaleidoscopic population structure of this pathogen is summarized, including different races of the pathogen, defoliating and nondefoliating phenotypes, vegetative compatibility groupings, and clonal populations. Where possible, we place the characteristic differences in the context of comparative and functional genomics analyses that have offered insights into population divergence within V. dahliae and the related species. Current challenges are highlighted along with some suggested future population genomics studies that will contribute to advancing our understanding of the population divergence in V. dahliae. Expected final online publication date for the Annual Review of Phytopathology, Volume 59 is August 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

scholarly journals In planta bacterial multi-omics analysis illuminates regulatory principles underlying plant-pathogen interactions

2019 ◽  
Author(s):  
Tatsuya Nobori ◽  
Yiming Wang ◽  
Jingni Wu ◽  
Sara Christina Stolze ◽  
Yayoi Tsuda ◽  
...  
Keyword(s):  
Gene Regulation ◽  
Pseudomonas Syringae ◽  
Protein Level ◽  
Plant Pathogens ◽  
Plant Immunity ◽  
Bacterial Pathogen ◽  
Bacterial Virulence ◽  
In Planta ◽  
Bacterial Gene ◽  
Global Food Security

AbstractUnderstanding how gene expression is regulated in plant pathogens is crucial for pest control and thus global food security. An integrated understanding of bacterial gene regulation in the host is dependent on multi-omic datasets, but these are largely lacking. Here, we simultaneously characterized the transcriptome and proteome of a foliar bacterial pathogen, Pseudomonas syringae, in Arabidopsis thaliana and identified a number of bacterial processes influenced by plant immunity at the mRNA and the protein level. We found instances of both concordant and discordant regulation of bacterial mRNAs and proteins. Notably, the tip component of bacterial type III secretion system was selectively suppressed by the plant salicylic acid pathway at the protein level, suggesting protein-level targeting of the bacterial virulence system by plant immunity. Furthermore, gene co-expression analysis illuminated previously unknown gene regulatory modules underlying bacterial virulence and their regulatory hierarchy. Collectively, the integrated in planta bacterial omics approach provides molecular insights into multiple layers of bacterial gene regulation that contribute to bacterial growth in planta and elucidate the role of plant immunity in controlling pathogens.

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