The genomic determinants of adaptive evolution in a fungal pathogen

Grandaubert, Jonathan; Dutheil, Julien; Stukenbrock, Eva H.

doi:10.1002/evl3.117

Cited by 69 publications

(57 citation statements)

References 78 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…We find no significant difference of synonymous nucleotide diversity (π S , figure 5A), non-synonymous diversity (π N , figure 5B), and ratio of non-synonymous to synonymous diversity (π N /π S , figure 5C) between genes in the three categories. This contrasts with results obtained in other fungal pathogens such as Z. tritici , where genes encoding effector proteins are evolving under relaxed purifying selection evidenced by a higher π N /π S ratio (Grandaubert et al ., 2019). The ratio of non-synonymous to synonymous divergences (d N /d S = ω), however, was found to be significantly higher in clustered genes than in non-clustered effectors, which have a significantly higher d N /d S than non-effector genes (figure 5D; P -value = 0.00599).…”

Section: Resultscontrasting

confidence: 90%

“…A higher mutation rate can be caused by the activity of transposable elements (TEs), directly or indirectly: active TEs may locally introduce mutations, the generated occurrence of repeated sequence may lead to increased slippage of the DNA polymerase, and mechanisms protecting the genome against TEs may be leaky and affect surrounding regions (Horns et al ., 2012; Laurie et al ., 2012; Dutheil et al ., 2016). In addition, selection may impact diversity along the genome (Charlesworth, 2009; Gossmann et al ., 2011; Grandaubert et al ., 2019). All these mechanisms may act simultaneously and are difficult to disentangle.…”

Section: Resultsmentioning

confidence: 99%

See 1 more Smart Citation

Population genomics of the maize pathogenUstilago maydis: demographic history and role of virulence clusters in adaptation

Schweizer

Haider

Barroso

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

The tight interaction between pathogens and their hosts results in reciprocal selective forces that impact the genetic diversity of the interacting species. The footprints of this selection differ between pathosystems because of distinct life-history traits, demographic histories, or genome architectures. Here, we studied the genome-wide patterns of genetic diversity of 22 isolates of the causative agent of the corn smut disease, Ustilago maydis, originating from five locations in Mexico, the presumed center of origin of this species. In this species, many genes encoding secreted effector proteins reside in so-called virulence clusters in the genome, an arrangement that is so far not found in other filamentous plant pathogens. Using a combination of population genomic statistical analyses, we assessed the geographical, historical and genome-wide variation of genetic diversity in this fungal pathogen.We report evidence of two partially admixed subpopulations that are only loosely associated with geographic origin. Using the multiple sequentially Markov coalescent model, we inferred the demographic history of the two pathogen subpopulations over the last 0.5 million years. We show that both populations experienced a recent strong bottleneck starting around 10,000 years ago, coinciding with the assumed time of maize domestication. While the genome average genetic diversity is low compared to other fungal pathogens, we estimated that the rate of non-synonymous adaptive substitutions is three times higher in genes located within virulence clusters compared to non-clustered genes, including non-clustered effector genes. These results highlight the role that these singular genomic regions play in the evolution of this pathogen.Significance statementThe maize pathogen Ustilago maydis is a model species to study fungal cell biology and biotrophic host-pathogen interactions. Population genetic studies of this species, however, were so far restricted to using a few molecular markers, and genome-wide comparisons involved species that diverged more than 20 million years ago. Here, we sequenced the genomes of 22 Mexican U. maydis isolates to study the recent evolutionary history of this species. We identified two co-existing populations that went through a recent bottleneck and whose divergence date overlaps with the time of maize domestication. Contrasting the patterns of genetic diversity in different categories of genes, we further showed that effector genes in virulence clusters display a high rate of adaptive mutations, highlighting the importance of these effector arrangements for the adaptation of U. maydis to its host.

show abstract

Section: Resultscontrasting

confidence: 90%

Section: Resultsmentioning

confidence: 99%

Population genomics of the maize pathogenUstilago maydis: demographic history and role of virulence clusters in adaptation

Schweizer

Haider

Barroso

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…All analyzed genomes and isolates used in this study are listed in Table S1 and originate from the following studies [32,33,[77][78][79][80][81][34][35][36][37]48,49,71,76]. We identified homologs of dim2 using the predicted 'deRIPed' protein sequence of Z. tritici IPO323 [25] as a template.…”

Section: Sequence Identification and Comparison Of Dna Methyltransfermentioning

confidence: 99%

Recent loss of the Dim2 DNA methyltransferase decreases mutation rate in repeats and changes evolutionary trajectory in a fungal pathogen

Möller

Habig

Lorrain

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

DNA methylation is found throughout all domains of life, yet the extent and function of DNA methylation differ between eukaryotes. Many strains of the plant pathogenic fungus Zymoseptoria tritici appeared to lack cytosine DNA methylation (5mC) because gene amplification followed by Repeat-Induced Point mutation (RIP) resulted in the inactivation of the Ztdim2 DNA methyltransferase gene. 5mC is, however, present in closely related sister species. We demonstrate that inactivation of Ztdim2 occurred recently as some Z. tritici isolates carry a functional Ztdim2 gene. Moreover, we show that Ztdim2 inactivation occurred by a different path than previously hypothesized. We mapped the genome-wide distribution of 5mC in strains with and without functional Ztdim2. Presence of functional Ztdim2 correlated with high levels of 5mC in transposable elements (TEs), suggesting a role in genome defense.We identified low levels of 5mC in strains carrying inactive Ztdim2 alleles, suggesting that 5mC is maintained over time, presumably by an active Ztdnmt5 gene. Integration of a functional Ztdim2 allele in strains with mutated Ztdim2 restored normal 5mC levels, demonstrating de novo cytosine methylation activity of Ztdim2. To assess the importance of 5mC for genome evolution, we performed an evolution experiment, comparing genomes of strains with high levels of 5mC to genomes of strains lacking Ztdim2. We found that the presence of Ztdim2 alters nucleotide composition by promoting C to T transitions (C→T) specifically at CpA (CA) sites during mitosis, likely contributing to TE inactivation. Our results show that dense 5mC at TEs is a polymorphic trait in Z. tritici populations that can impact genome evolution. SignificanceCytosine DNA methylation (5mC) is known to silence transposable elements in fungi and thereby appears to contribute to genome stability. The genomes of plant pathogenic fungi are highly diverse, differing substantially in transposon content and distribution. Here, we show extensive differences of 5mC levels within a single species of an important wheat pathogen that were caused by inactivation of the DNA methyltransferase ZtDim2 in the majority of studied isolates. Presence of widespread 5mC increased point mutation rates in regions with active or mutated transposable elements during mitosis. The mutation pattern is dependent on the presence of ZtDim2 and resembles a mitotic version of Repeat-Induced Point mutation (RIP). Thus, loss of 5mC may represent an evolutionary trade-off offering adaptive potential at the cost of transposon control. occurred recently as two closely related sister species of Z. tritici, Zymoseptoria ardabiliae and Zymoseptoria pseudotritici were shown to carry a single intact dim2 gene and have 5mC (25).By genome analyses of multiple Z. tritici isolates from the center of origin of the pathogen, the Middle East, we discovered several Z. tritici isolates with an intact Ztdim2 gene. This finding suggests that the loss of 5mC not only occurred very recently but is a polymorphic trait in Z.triti...

show abstract

“…Understanding the mechanisms and timescales associated with new epidemics is essential for both basic studies and the implementation of effective response measures [3]. A fundamental component of this knowledge is a detailed genome-scale understanding of the population structure and dynamics of global plant pathogen populations [4][5][6]. Population genetic information drives the selection of isolates for activities as diverse as basic mechanistic research and plant germplasm screening for disease resistance.…”

Section: Introductionmentioning

confidence: 99%

Differential loss of effector genes in three recently expanded pandemic clonal lineages of the rice blast fungus

et al. 2020

View full text Add to dashboard Cite

Background: Understanding the mechanisms and timescales of plant pathogen outbreaks requires a detailed genome-scale analysis of their population history. The fungus Magnaporthe (Syn. Pyricularia) oryzae-the causal agent of blast disease of cereals-is among the most destructive plant pathogens to world agriculture and a major threat to the production of rice, wheat, and other cereals. Although M. oryzae is a multihost pathogen that infects more than 50 species of cereals and grasses, all rice-infecting isolates belong to a single genetically defined lineage. Here, we combined the two largest genomic datasets to reconstruct the genetic history of the rice-infecting lineage of M. oryzae based on 131 isolates from 21 countries. Results: The global population of the rice blast fungus consists mainly of three well-defined genetic groups and a diverse set of individuals. Multiple population genetic tests revealed that the rice-infecting lineage of the blast fungus probably originated from a recombining diverse group in Southeast Asia followed by three independent clonal expansions that took place over the last~200 years. Patterns of allele sharing identified a subpopulation from the recombining diverse group that introgressed with one of the clonal lineages before its global expansion. Remarkably, the four genetic lineages of the rice blast fungus vary in the number and patterns of presence and absence of candidate effector genes. These genes encode secreted proteins that modulate plant defense and allow pathogen colonization. In particular, clonal lineages carry a reduced repertoire of effector genes compared with the diverse group, and specific combinations of presence and absence of effector genes define each of the pandemic clonal lineages. Conclusions: Our analyses reconstruct the genetic history of the rice-infecting lineage of M. oryzae revealing three clonal lineages associated with rice blast pandemics. Each of these lineages displays a specific pattern of presence and absence of effector genes that may have shaped their adaptation to the rice host and their evolutionary history.

show abstract

The genomic determinants of adaptive evolution in a fungal pathogen

Cited by 69 publications

References 78 publications

Population genomics of the maize pathogenUstilago maydis: demographic history and role of virulence clusters in adaptation

Population genomics of the maize pathogenUstilago maydis: demographic history and role of virulence clusters in adaptation

Recent loss of the Dim2 DNA methyltransferase decreases mutation rate in repeats and changes evolutionary trajectory in a fungal pathogen

Differential loss of effector genes in three recently expanded pandemic clonal lineages of the rice blast fungus

Contact Info

Product

Resources

About