Utilizing Gene Tree Variation to Identify Candidate Effector Genes in <i>Zymoseptoria tritici</i>

McDonald, Megan C.; McGinness, Lachlan; Hane, James K.; Williams, Angela H.; Milgate, Andrew; Solomon, Peter S.

doi:10.1534/g3.115.025197

Cited by 23 publications

(27 citation statements)

References 71 publications

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“…As for the in vitro experiments, no strains 166 lacking more than one chromosome were found. Interestingly, chromosome 18, which was 167 found to be lost at high rates in our plant experiments, was shown to be frequently absent 168 in field isolates of Z. tritici (Croll et al 2013;McDonald et al 2016). In summary, our findings 169…”

Section: Introduction 31mentioning

confidence: 74%

Extraordinary genome instability and widespread chromosome rearrangements during vegetative growth

Stukenbrock

Möller

Habig

et al. 2018

Preprint

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The haploid genome of the pathogenic fungus Zymoseptoria tritici is contained on “core” and “accessory” chromosomes. While 13 core chromosomes are found in all strains, as many as eight accessory chromosomes show presence/absence variation and rearrangements among field isolates. We investigated chromosome stability using experimental evolution, karyotyping and genome sequencing. We report extremely high and variable rates of accessory chromosome loss during mitotic propagation in vitro and in planta. Spontaneous chromosome loss was observed in 2 to >50 % of cells during four weeks of incubation. Similar rates of chromosome loss in the closely related Z. ardabiliae suggest that this extreme chromosome dynamic is a conserved phenomenon in the genus. Elevating the incubation temperature greatly increases instability of accessory and even core chromosomes, causing severe rearrangements involving telomere fusion and chromosome breakage. Chromosome losses do not impact the fitness of Z. tritici in vitro, but some lead to increased virulence suggesting an adaptive role of this extraordinary chromosome instability.

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Section: Introduction 31mentioning

confidence: 74%

Extraordinary genome instability and widespread chromosome rearrangements during vegetative growth

Stukenbrock

Möller

Habig

et al. 2018

Preprint

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“…Therefore, such genes may be located in genome compartments unique to individual genomes. A previous study identified reference genome genes which were likely missing in 13 sequenced Australian isolates (35). Using BLAST, we searched for genes in the IPO323 genome that were absent in the 3D7 genome.…”

Section: Resultsmentioning

confidence: 99%

“…Genes encoding SSPs evolved more rapidly than the genomic background (25, 34) and were more likely to lack orthologs in closely related species (33). Genomic analyses suggested that numerous genes (including effector genes) were deleted in at least some isolates of the species (31, 35). …”

Section: Introductionmentioning

confidence: 99%

The Evolution of Orphan Regions in Genomes of a Fungal Pathogen of Wheat

Plissonneau

Sturchler

Croll

2016

mBio

127

133

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Fungal plant pathogens rapidly evolve virulence on resistant hosts through mutations in genes encoding proteins that modulate the host immune responses. The mutational spectrum likely includes chromosomal rearrangements responsible for gains or losses of entire genes. However, the mechanisms creating adaptive structural variation in fungal pathogen populations are poorly understood. We used complete genome assemblies to quantify structural variants segregating in the highly polymorphic fungal wheat pathogen Zymoseptoria tritici. The genetic basis of virulence in Z. tritici is complex, and populations harbor significant genetic variation for virulence; hence, we aimed to identify whether structural variation led to functional differences. We combined single-molecule real-time sequencing, genetic maps, and transcriptomics data to generate a fully assembled and annotated genome of the highly virulent field isolate 3D7. Comparative genomics analyses against the complete reference genome IPO323 identified large chromosomal inversions and the complete gain or loss of transposable-element clusters, explaining the extensive chromosomal-length polymorphisms found in this species. Both the 3D7 and IPO323 genomes harbored long tracts of sequences exclusive to one of the two genomes. These orphan regions contained 296 genes unique to the 3D7 genome and not previously known for this species. These orphan genes tended to be organized in clusters and showed evidence of mutational decay. Moreover, the orphan genes were enriched in genes encoding putative effectors and included a gene that is one of the most upregulated putative effector genes during wheat infection. Our study showed that this pathogen species harbored extensive chromosomal structure polymorphism that may drive the evolution of virulence.

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“…For comparison, population genomic sequencing of 13 isolates of Z. tritici sampled from one region in Australia showed more than 800 000 SNPs [56]. Although the number of polymorphic nucleotides was found to be relatively low, the 11 isolates of V. dahliae were found to exhibit a dramatic variation in their genome composition and genome content.…”

Section: Example 2: Hybridization Of Crop Plants Driving Hybrid Specimentioning

confidence: 99%

Rapid emergence of pathogens in agro-ecosystems: global threats to agricultural sustainability and food security

McDonald

Stukenbrock

2016

Phil. Trans. R. Soc. B

292

199

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Agricultural ecosystems are composed of genetically depauperate populations of crop plants grown at a high density and over large spatial scales, with the regional composition of crop species changing little from year to year. These environments are highly conducive for the emergence and dissemination of pathogens. The uniform host populations facilitate the specialization of pathogens to particular crop cultivars and allow the build-up of large population sizes. Population genetic and genomic studies have shed light on the evolutionary mechanisms underlying speciation processes, adaptive evolution and long-distance dispersal of highly damaging pathogens in agro-ecosystems. These studies document the speed with which pathogens evolve to overcome crop resistance genes and pesticides. They also show that crop pathogens can be disseminated very quickly across and among continents through human activities. In this review, we discuss how the peculiar architecture of agro-ecosystems facilitates pathogen emergence, evolution and dispersal. We present four example pathosystems that illustrate both pathogen specialization and pathogen speciation, including different time frames for emergence and different mechanisms underlying the emergence process. Lastly, we argue for a re-design of agro-ecosystems that embraces the concept of dynamic diversity to improve their resilience to pathogens. This article is part of the themed issue ‘Tackling emerging fungal threats to animal health, food security and ecosystem resilience’.

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Utilizing Gene Tree Variation to Identify Candidate Effector Genes in Zymoseptoria tritici

Cited by 23 publications

References 71 publications

Extraordinary genome instability and widespread chromosome rearrangements during vegetative growth

Extraordinary genome instability and widespread chromosome rearrangements during vegetative growth

The Evolution of Orphan Regions in Genomes of a Fungal Pathogen of Wheat

Rapid emergence of pathogens in agro-ecosystems: global threats to agricultural sustainability and food security

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