Multiple deletions of candidate effector genes lead to the breakdown of partial grapevine resistance to downy mildew

Paineau, Manon; Minio, Andrea; Mestre, Pere; Fabre, Frédéric; Mazet, Isabelle D.; Couture, Carole; Legeai, Fabrice; Dumartinet, Thomas; Cantu, Dario; Delmotte, François

doi:10.1111/nph.19861

Cited by 4 publications

(1 citation statement)

References 84 publications

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“…LOH can provide an additional way of adaptation during the growing season, through the fixation of beneficial alleles faster than annual sexual reproduction. For example, important traits such as fungicide tolerance and virulence are determined by co-dominant or recessive alleles (Lamour et al, 2012;Matson et al, 2022;Paineau et al, 2024). It has been shown that LOH can lead to a gain of virulence in Pe.…”

Section: Adaptation By Loss Of Heterozygositymentioning

confidence: 99%

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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Section: Adaptation By Loss Of Heterozygositymentioning

confidence: 99%

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

Dvorak,

Mazet,

Couture

et al. 2024

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

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

Dvorak,

Mazet,

Couture

et al. 2024

G3: Genes, Genomes, Genetics

View full text Add to dashboard Cite

Plasmopara viticola, the causal agent of grapevine downy mildew, is a biotrophic oomycete engaged in a tight coevolutionary relationship with its host. Rapid adaptation of the pathogen is favored by annual sexual reproduction that generates genotypic diversity. With the aim of studying the recombination landscape across the P. viticola genome, we generated 2 half-sibling F1 progenies (N = 189 and 162). Using targeted SNP sequencing, between 1,405 and 1,894 markers were included in parental linkage maps, and a consensus map was obtained by integrating 4,509 markers. The reference genome could be assembled into 17 pseudochromosomes, anchoring 88% of its physical length. We observed a strong collinearity between parental genomes and extensive synteny with the downy mildew Peronospora 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 underrepresented 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 in P. viticola compared to other oomycetes. The linkage maps will be useful to guide future de novo chromosome-scale assemblies of P. viticola genomes and to perform forward genetics.

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Advances in grape and pathogen genomics toward durable grapevine disease resistance

Paineau,

Zaccheo,

Massonnet

et al. 2024

Journal of Experimental Botany

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The future sustainability of viticulture depends on the development of grapevine cultivars with genetic resistance to diseases such as powdery mildew, downy mildew, and Pierce’s disease. Recent advances in grape and pathogen genomics have dramatically improved our approach to durable disease resistance. The availability of diploid genome references for wild species, combined with the ability to phase resistance haplotypes and conduct genome-wide association and expression analyses, has greatly enhanced our ability to dissect genetic resistance loci. This progress is yielding candidate genes that will form the foundation for precise breeding, gene stacking, and genome editing in grape improvement programs. As resistance genes are deployed in vineyards, pathogen populations evolve to adapt and evade these defenses, posing ongoing challenges. Understanding the adaptive mechanisms of grapevine pathogens in response to resistant cultivars is crucial. Grape pathogenomics is advancing rapidly, marked by the sequencing of many pathogen genomes, the discovery of effectors, including the first ones responsible for disease resistance breakdown, and the development of graph-based pangenomes. These advancements offer valuable insights into pathogen evolution and inform strategies for sustainable disease management. Together, these genomic tools and insights are paving the way for developing resilient grapevine varieties, ensuring the long-term sustainability of viticulture.

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Multiple deletions of candidate effector genes lead to the breakdown of partial grapevine resistance to downy mildew

Cited by 4 publications

References 84 publications

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

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

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

Advances in grape and pathogen genomics toward durable grapevine disease resistance

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