Genome-Enabled Insights into Downy Mildew Biology and Evolution

Fletcher, Kyle; Michelmore, Richard W.

doi:10.1146/annurev-phyto-021622-103440

Cited by 2 publications

(12 citation statements)

References 140 publications

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“…In contrast to the overall conserved chromosome structure in Peronosporaceae (S. Figure 5A), we discovered the presence of an accessory chromosome in 19 out of 32 P. effusa isolates that is does not correspond with any of the chromosomes in B. lactucae or P. sorghi (Fletcher et al, 2021(Fletcher et al, , 2023.…”

Section: Discussioncontrasting

confidence: 87%

“…The copyright holder for this preprint this version posted June 2, 2024. ; https://doi.org/10.1101/2024.05.30.596583 doi: bioRxiv preprint 31 Croll, 2020; Everhart, Gambhir and Stam, 2021). Especially chromosome-level genome assemblies will be essential to achieve the necessary resolution to uncover and study highly variable regions that are enriched for pathogenicity-related genes (Fletcher and Michelmore, 2023;Westerhoven et al, 2024).…”

Section: Discussionmentioning

confidence: 99%

“…The previously published genome assembly of the P. effusa isolate UA-202013 has 17 chromosomes (Fletcher et al, 2022), and is comparable in total genome size as well as gene and repeat content to the here assembled P. effusa isolates. Since the overall chromosome organization of oomycetes is thought to be highly conserved (Fletcher and Michelmore, 2023), we sought to investigate the co-linearity between our Pe1 isolate, the UA-202013 isolate, and chromosome-level genome assemblies from Bremia lactucae, Peronosclerospora sorghi, and Phytophthora infestans (Fletcher et al, 2019(Fletcher et al, , 2022(Fletcher et al, , 2023Matson et al, 2022). To this end, we performed whole-genome alignments of these genomes based on sequence similarity and on relative position of protein-coding genes (S. Figure 5A).…”

Section: Chromosome-level Genome Assemblies Of Six Peronospora Effusa...mentioning

confidence: 99%

“…A pangenome can be defined as the total number of unique genes discovered among genomes of the same species (McInerney, McNally and O’Connell, 2017; Badet et al ., 2020; Hickey et al ., 2023). However, this definition ignores the contribution of TEs and other non-coding sequences to genome diversity and adaptation (Fedoroff, 2012; Faino et al ., 2016; Badet and Croll, 2020; Torres, Thomma and Seidl, 2021), which is particularly relevant for TE-rich accessory regions in filamentous plant pathogens (Fletcher and Michelmore, 2023). To include these regions, a pangenome needs to be defined as the total genome content of a species, thus creating a sequence-resolved pangenome.…”

Section: Introductionmentioning

confidence: 99%

“…P. effusa can reproduce both sexually and asexually and thus new races can emerge both from sexual and asexual recombination (Feng et al ., 2020; Skiadas et al ., 2022). P. effusa is one of few oomycetes with a publicly available chromosome-level reference genome (Fletcher et al ., 2022; Matson et al ., 2022; Fletcher and Michelmore, 2023). The P. effusa genome is relatively small compared with other oomycetes and organised in 17 chromosomes (Fletcher et al ., 2022).…”

Section: Introductionmentioning

confidence: 99%

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Pangenome graph analysis reveals extensive effector copy-number variation in spinach downy mildew

Skiadas,

Vidal,

Dommisse

et al. 2024

Preprint

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Plant pathogens adapt at speeds that challenge contemporary disease management strategies like the deployment of disease resistance genes. The strong evolutionary pressure to adapt, shapes pathogens’ genomes, and comparative genomics has been instrumental in characterizing this process. With the aim to capture genomic variation at high resolution and study the processes contributing to adaptation, we here leverage and expand on an innovative, multi-genome method to construct, annotate, and analyse the first pangenome graph of an oomycete plant pathogen. We generated telomere-to-telomere genome assemblies of six genetically diverse isolates of the oomycete pathogenPeronospora effusa, the economically most important disease in cultivated spinach worldwide. The pangenome graph demonstrates thatP. effusagenomes are highly conserved, both in chromosomal structure and gene content, and revealed the continued activity of transposable elements which are directly responsible for 80% of the observed variation between the isolates. While most genes are generally conserved, pathogenicity related genes are highly variable between the isolates. Most of the variation is found in large gene clusters resulting from extensive copy-number expansion. Pangenome graph-based discovery can thus be effectively used to capture genomic variation at exceptional resolution, thereby providing a framework to study the biology and evolution of plant pathogens.Author SummaryPlant pathogens are known to evolve rapidly and overcome disease resistance of newly introduced crop varieties. This swift adaptation is visible in the genomes of these pathogens, which can be highly variable. Such genomic variation cannot be captured with contemporary comparative genomic methods that rely on a single reference genome or focus solely on protein coding genes. To overcome these limitations and compare multiple genomes in a robust and scalable method, we constructed the first pangenome graph for an oomycete filamentous plant pathogen with six telomere-to-telomere genome assemblies ofPeronospora effusa. This high-resolution pangenomic framework enabled detailed comparisons of the genomes at any level, from the nucleotide to the chromosome, and for any subset of protein-coding genes or transposable elements, to discover novel biology and potential mechanisms for the rapid evolution of this devastating pathogen.

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Section: Discussioncontrasting

confidence: 87%

Section: Discussionmentioning

confidence: 99%

Section: Chromosome-level Genome Assemblies Of Six Peronospora Effusa...mentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Pangenome graph analysis reveals extensive effector copy-number variation in spinach downy mildew

Skiadas,

Vidal,

Dommisse

et al. 2024

Preprint

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Recombination landscape and karyotypic variations revealed by linkage mapping in the grapevine downy mildew pathogenPlasmopara viticola

Dvorak,

Mazet,

Couture

et al. 2024

Preprint

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Plasmopara viticola, the causal agent of grapevine downy mildew, is a biotrophic oomycete engaged in atight coevolutionary relationship with its host. Rapid adaptation of the pathogen is favored by annual sexual reproduction which generates genotypic diversity. With the aim of studying the recombination landscape across theP. viticolagenome, we generated two half-siblings F1 progenies (N=189 and 162). Offspring were genotyped by targeted sequencing of a set of 5,000 informative SNPs. This enabled the construction of unprecedented high-density linkage maps for this species. The reference genome could be assembled into 17 pseudo-chromosomes, anchoring 88% of its physical length. We observed a strong collinearity between parental genomes and extensive synteny with the downy mildewPeronospora effusa. In the consensus map, the median recombination rate was 13.8 cM/Mb. The local recombination rate was highly variable along chromosomes and recombination was suppressed in putative centromeric regions. Recombination rate was found negatively correlated with repeats coverage and positively correlated with gene coverage. However, genes encoding secreted proteins and putative effectors were under-represented in highly recombining regions. In both progenies, about 5% of the individuals presented karyotypic anomalies. Aneuploidies and triploidies almost exclusively originated from the male-transmitted chromosomes. Triploids resulted from fertilization by diploid gametes, but also from dispermy. Obligatory sexual reproduction each year may explain the lower level of karyotypic variation inP. viticolacompared to other oomycetes. The linkage maps will be useful to guide futurede novochromosome-scale assemblies ofP. viticolagenomes and to perform forward genetics.SummarySexual reproduction contributes to the rapid adaptation of plant pathogens thanks to the recombination of genetic variants. By crossing strains of grapevine downy mildew, we built a set of linkage maps and describe the recombination landscape along the 17 chromosomes of the genome. The recombination rate varied greatly and was higher in gene-rich regions, but not in effector-rich regions. We observed an abnormal number of chromosomes in 5% of the offspring, which was mostly due to the male parent.

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Genome-Enabled Insights into Downy Mildew Biology and Evolution

Cited by 2 publications

References 140 publications

Pangenome graph analysis reveals extensive effector copy-number variation in spinach downy mildew

Pangenome graph analysis reveals extensive effector copy-number variation in spinach downy mildew

Recombination landscape and karyotypic variations revealed by linkage mapping in the grapevine downy mildew pathogenPlasmopara viticola

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