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

Abstract

Summary Blumeria graminis f. sp. tritici ( B.g. tritici ) is the causal agent of the wheat powdery mildew disease. The highly fragmented B.g. tritici genome available so far has prevented a systematic analysis of effector genes that are known to be involved in host adaptation. To study the diversity and evolution of effector genes we produced a chromosome‐scale assembly of the B.g. tritici genome. The genome assembly and annotation was achieved by combining long‐read sequencing with high‐density genetic mapping, bacterial artificial chromosome fingerprinting and transcriptomics. We found that the 166.6 Mb B.g. tritici genome encodes 844 candidate effector genes, over 40% more than previously reported. Candidate effector genes have characteristic local genomic organization such as gene clustering and enrichment for recombination‐active regions and certain transposable element families. A large group of 412 candidate effector genes shows high plasticity in terms of copy number variation in a global set of 36 isolates and of transcription levels. Our data suggest that copy number variation and transcriptional flexibility are the main drivers for adaptation in B.g. tritici . The high repeat content may play a role in providing a genomic environment that allows rapid evolution of effector genes with selection as the driving force.

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

“…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.…”

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

“…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).…”

“…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).…”

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

“…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).…”