A chromosome‐scale genome assembly reveals a highly dynamic effector repertoire of wheat powdery mildew

Müller, Marion; Praz, Coraline R.; Sotiropoulos, Alexandros G.; Menardo, Fabrizio; Kunz, Lukas; Schudel, Seraina; Oberhänsli, Simone; Poretti, Manuel; Wehrli, Andreas; Bourras, Salim; Keller, Beat; Wicker, Thomas

doi:10.1111/nph.15529

Cited by 86 publications

(160 citation statements)

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“…Examples comprise the wheat pathogens Zymoseptoria tritici[67] and Blumeria graminis f. sp. tritici[68], and the broad host range pathogen Verticillium dahlia[69]. Moreover, different strains can encode different alleles of the same effector gene; this was, for example, reported for the low complexity regions containing Ustilago maydis effector Rsp3[58].Several reports suggest that effector proteins containing low complexity regions can play important roles in virulence[37,70], and results presented in the present work suggest that different fungal lifestyles contribute to the evolution of low complexity regions in effector proteins.ConclusionsA comparative genomics study with 121 plant colonizing fungi representing six different lifestyles showed that protein type (cytoplasmic or secreted), protein age (ancestral proteins conserved in most species or recent species-specific proteins), and lifestyle of different fungal species contribute to the evolution of low complexity regions in effector proteins.…”

supporting

confidence: 76%

Protein type and lifestyle contribute to the evolution of low complexity regions in proteins of plant colonizing fungi

Schweizer¹

2020

Preprint

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Background: Interactions between plants and fungi range from mutual symbiosis to parasitism. Fungi secrete proteins (termed effectors) to establish different forms of interactions with host plants. Such proteins are thought to coevolve with their molecular plant targets, and this can favor the emergence of novel alleles of fungal effector proteins. Low complexity regions in protein sequences are abundant in eukaryotes and were shown to contribute to the formation of novel protein sequences. This suggests that low complexity regions may play a role in the evolution of effector proteins. Several effector proteins with low complexity regions were functionally characterized in plant colonizing fungi that showed diverse lifestyles and belonged to different taxonomic groups. To investigate if low complexity regions in fungal effector proteins could contribute to the evolution of different plant-fungus interaction types, I employed publicly available genomic data from 121 species of plant colonizing fungi representing six different lifestyles and three phyla. I classified proteins in each species as cytoplasmic, secreted-non effector or effector protein and predicted low complexity regions in all protein sequences.Results: I found that the fraction of proteins that contain a low complexity region differs between cytoplasmic and secreted proteins. Moreover, the fraction of a protein sequence that spans a low complexity region differed on average between cytoplasmic and secreted proteins. Inferring homologous relationships between effector proteins revealed that this fraction is higher in recent compared to ancestral proteins, suggesting that low complexity regions contribute to the formation of novel effector alleles. Furthermore, a principal component analysis and the results of a generalized linear model showed that the lifestyle of different fungi contributes to the evolution of low complexity regions. Likewise, the relative position of low complexity regions differed between cytoplasmic and secreted proteins, between ancestral and recent effector proteins, and between effectors of different lifestyles.Conclusions: Protein type and lifestyle contribute to the evolution of low complexity regions in proteins of plant colonizing fungi, but molecular and evolutionary mechanisms explaining the differences between different protein types and proteins of different lifestyles remain to be elucidated.

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supporting

confidence: 76%

Protein type and lifestyle contribute to the evolution of low complexity regions in proteins of plant colonizing fungi

Schweizer¹

2020

Preprint

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“…In addition, all chromosomes contain a putative centromere region of variable length (Figure 3), which is, as in other fungi, characterized by high transposable element density, low gene density, absence of gene transcription and reduced CG-content (Müller et al , 2019; Smith et al , 2012; Yadav et al , 2018). Putative centromere regions were located within chromosomal regions avoid of recombination, consistent with the findings from other fungi (Laurent et al , 2018; Mancera et al , 2008; Müller et al , 2019). The exact location and length of centromere regions, however, needs to be confirmed using chromatin immunoprecipitation sequencing (CHIPseq) as applied in other basidiomycetes (Yadav et al , 2018).…”

Section: Discussionmentioning

confidence: 90%

“…The most striking deviations in these patterns are recombination hotspots. Such recombination hotspots are observed in many fungal species (Croll et al , 2015; Laurent et al , 2018; Müller et al , 2019; Roth et al , 2018; Van Kan et al , 2017), however their specific role in genome and gene evolution is still largely unknown. In the wheat pathogen Zymoseptoria tritic recombination hotspots may serve as ephemeral genome compartments favoring the emergence of fast-evolving virulence genes (Croll et al , 2015).…”

Section: Discussionmentioning

confidence: 99%

Chromosomal assembly and analyses of genome-wide recombination rates in the forest pathogenic fungusArmillaria ostoyae

Heinzelmann

Rigling

Sipos

et al. 2019

Preprint

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Recombination shapes the evolutionary trajectory of populations and plays an important role in the faithful transmission of chromosomes during meiosis. Levels of sexual reproduction and recombination are important properties of host-pathogen interactions because the speed of antagonistic co-evolution depends on the ability of hosts and pathogens to generate genetic variation. However, our understanding of the importance of recombination is limited because large taxonomic groups remain poorly investigated. Here, we analyze recombination rate variation in the basidiomycete fungus Armillaria ostoyae, which is an aggressive pathogen on a broad range of conifers and other trees. We constructed a dense genetic map using 198 single basidiospore progeny from a cross. Progeny were genotyped at a genome-wide set of single nucleotide polymorphism (SNP) markers using double digest restriction site associated DNA sequencing (ddRADseq). Based on a linkage map of on 11,700 SNPs spanning 1007.5 cM, we assembled genomic scaffolds into 11 putative chromosomes of a total genome size of 56.6 Mb. We identified 1984 crossover events among all progeny and found that recombination rates were highly variable along chromosomes. Recombination hotspots tended to be in regions close to the telomeres and were more gene-poor than the genomic background. Genes in proximity to recombination hotspots were encoding on average shorter proteins and were enriched for pectin degrading enzymes. Our analyses enable more powerful population and genome-scale studies of a major tree pathogen.

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“…For example, in the powdery mildew pathogen Blumeria graminis, putative effectors and some known Avr genes occur in physically co-located gene clusters that have resulted from tandem duplications. The presence/absence of specific paralogous effectors is very variable between different B. graminis strains (Müller et al, 2019).…”

Section: Application Of the D N /D S Ratio Test To Plant Pathogens: Lmentioning

confidence: 99%

Bioinformatic Detection of Positive Selection Pressure in Plant Pathogens: The Neutral Theory of Molecular Sequence Evolution in Action

Derbyshire

2020

Front. Microbiol.

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The genomes of plant pathogenic fungi and oomycetes are often exposed to strong positive selection pressure. During speciation, shifts in host range and preference can lead to major adaptive changes. Furthermore, evolution of total host resistance to most isolates can force rapid evolutionary changes in host-specific pathogens. Crop pathogens are subjected to particularly intense selective pressures from monocultures and fungicides. Detection of the footprints of positive selection in plant pathogen genomes is a worthwhile endeavor as it aids understanding of the fundamental biology of these important organisms. There are two main classes of test for detection of positively selected alleles. Tests based on the ratio of non-synonymous to synonymous substitutions per site detect the footprints of multiple fixation events between divergent lineages. Thus, they are well-suited to the study of ancient adaptation events spanning speciations. On the other hand, tests that scan genomes for local fluctuations in allelic diversity within populations are suitable for detection of recent positive selection in populations. In this review, I briefly describe some of the more widely used tests of positive selection and the theory underlying them. I then discuss various examples of their application to plant pathogen genomes, emphasizing the types of genes that are associated with signatures of positive selection. I conclude with a discussion of the practicality of such tests for identification of pathogen genes of interest and the important features of pathogen ecology that must be taken into account for accurate interpretation.

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A chromosome‐scale genome assembly reveals a highly dynamic effector repertoire of wheat powdery mildew

Cited by 86 publications

References 48 publications

Protein type and lifestyle contribute to the evolution of low complexity regions in proteins of plant colonizing fungi

Protein type and lifestyle contribute to the evolution of low complexity regions in proteins of plant colonizing fungi

Chromosomal assembly and analyses of genome-wide recombination rates in the forest pathogenic fungusArmillaria ostoyae

Bioinformatic Detection of Positive Selection Pressure in Plant Pathogens: The Neutral Theory of Molecular Sequence Evolution in Action

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