bioRxiv Science⌕ Search

Biology subjects

Delmotte, F.

Publications and source records attributed to Delmotte, F..

11 recordsLinked to original sources

Long-term performance of disease-resistant grapevine varieties: insights from an 8-year field monitoring across French vineyards

Breeding disease-resistant varieties (DRV) is a central strategy for reducing reliance on phytosanitary products. However, the successful deployment and long-term durability of these cultivars rely on acquiring field data across diverse production conditions, a step that remains frequently neglected, especially in perennial crops. Since 2018, the OSCAR observatory, a network of vineyard plots planted in France with varieties resistant to downy and powdery mildew, the two major pathogens of grapevine, has aimed to close this gap for viticulture. The observatory comprises over 199 commercial plots, covering 127 hectares across diverse agroclimatic conditions, all managed by winegrowers under their own production practices. The observatory currently monitors 30 disease-resistant grapevine varieties, tracking both their agronomic performance and the dynamics of key pathogens. Since 2018, while phytosanitary treatments have been reduced by an average of 79% compared to conventional plots, the incidence of downy and powdery mildew, remain low, even in years highly conducive to these diseases. However, the long-term survey also highlights the decline in efficacy of some resistances to downy mildew and the emergence of black rot, a disease effectively controlled by conventional phytosanitary programs. Beyond acting as a rapid warning system for resistance breakdown, the observatory promotes sustainable disease management in viticulture. It provides valuable insights to winegrowers on effective DRV management. It also delivers actionable feedback to breeders to guide more durable DRV breeding strategies. Highlights- OSCAR observatory monitors 199 plots of grapevine disease resistant varieties (DRV) - Grapevine DRV cuts fungicide uses by 79% while maintaining good disease control - Some resistances efficacy declines against downy mildew, but not powdery mildew - Black rot, a disease usually controlled by fungicide, is rising in OSCAR plots OSCAR provides useful feedback to breeders and winegrowers on DRV management

plant biology↗

A rapid and accurate PCR-based method for mating-type determination in the heterothallic oomycete Plasmopara viticola, the causal agent of grapevine downy mildew

Plasmopara viticola is a heterothallic diploid oomycete responsible for grapevine downy mildew, one of the most damaging grapevine diseases worldwide. Since no rapid method for mating type characterization of strains is currently available, mating type identification must be performed through crossing assays, which are time-consuming. This study reports the development of two PCR-based molecular markers (MT_indel1 and MT_indel2) based on size variation to distinguish between the mating-type alleles of the oomycete Plasmopara viticola. For both markers, P1 strains (Mat-a/Mat-b) exhibited a double-band profile, whereas P2 strains (Mat-a/Mat-a) displayed a single PCR band. The markers were validated on a set of 37 reference strains collected across Europe and showed perfect concordance with mating-type phenotypes determined by crossing tests. They provide a robust, sensitive, and inexpensive DNA-based detection system for mating-type identification in P. viticola, offering valuable insights into the pathogens reproductive biology and genetic diversity.

molecular biology↗

A multivirulent Plasmopara viticola strain from Cilaos on Reunion Island breaks down Rpv1, Rpv3.1 and Rpv10 mediated resistance of grapevine

AbstractGrapevine downy mildew, caused by Plasmopara viticola, is one of the most destructive diseases in viticulture. Resistance-based management strategies rely on grapevine varieties carrying major resistance loci (Rpv). Although breakdown of several loci has been reported, Rpv1 had remained effective until now. Here, we provide the first evidence of Rpv1 breakdown by P. viticola in Cilaos on Reunion Island (France) and the first case of a strain simultaneously overcoming three resistances of grapevine. We combined pathogenicity assays with whole-genome sequencing to characterize a P. viticola strain collected in Cilaos in 2023, alongside a panel of eight reference strains of known virulence. Hypersensitive response and sporulation were assessed for each strain on Chardonnay (susceptible variety) and four resistant varieties carrying Rpv1, Rpv3.1, Rpv10, or Rpv12. The strain collected in Cilaos was able to overcome not only Rpv1 but also Rpv3.1 and Rpv10. On Rpv1, we observed a complete loss of host recognition with high sporulation. On Rpv3.1, the phenotype was consistent with previous breakdowns, and the strain carried the vir1 allele previously described in France. By contrast, the breakdown of Rpv10 differed from that reported in European populations: whereas European strains displayed only partial breakdown of resistance, the strain of Cilaos showed complete loss of host recognition with high sporulation. Moreover, genomic analyses revealed a novel mutation, a large homozygous deletion in the corresponding avr locus. Our genomic data analyses further suggests that this P. viticola strain shares a genetic background with populations from mainland France, raising serious concerns about the potential emergence and spread of multivirulent lineages in Europe. These findings highlight the need for large-scale virulence monitoring of P. viticola and improved strategies for the sustainable management of grapevine resistance in Europe.

plant biology↗

Multiple geographic breakdown events of the Rpv1/Rpv3.1 pyramided resistance in grapevine by Plasmopara viticola.

In 2024, three vineyard sites located within a radius of 40 km in southeastern France, each planted with Artaban, a grapevine variety carrying pyramided resistance (Rpv1 and Rpv3.1), exhibited severe downy mildew symptoms following climatic conditions highly conducive to disease development. Twenty-one Plasmopara viticola isolates were collected from these vineyards and, after monosporangium isolation, tested under controlled conditions on a panel of susceptible and resistant grapevine varieties to assess their virulence. Among the 21 tested field strains, 19 overcame Rpv3.1 mediated resistance, 10 overcame Rpv1 alone, and four genetically distinct strains from two separate vineyards were overcoming the pyramided Rpv1-Rpv3.1 combination. The genetic characterization of the strains suggests that this adaptation likely resulted from convergent evolution. To our knowledge, these represent the first documented cases in Europe of a breakdown in resistance conferred by Rpv1, whether deployed alone or in combination with Rpv3.1.

plant biology↗

Phylogenomics of Plasmopara halstedii reveals genomic regions associated with the breakdown of sunflower downy mildew resistance genes

O_LIUnderstanding the genetic diversity and evolutionary history of plant pathogens is crucial for effective disease management strategies. Sunflower downy mildew, caused by the oomycete Plasmopara halstedii, is a worldwide threat to the sunflower oil crop. We aimed to explain through phylogenomic studies how downy mildew resistance breakdown occurred recurrently in the last decades in France, leading to new virulence profiles. C_LIO_LIWe assembled high-quality genomes of three founder pathotypes of Pl. halstedii. Performing comparative genomic analyses, population genetics, and phylogenomic analyses, we studied the genomic structure among the 16 reference French pathotypes of Pl. halstedii. C_LIO_LIWe revealed a conserved genomic organisation among pathotypes and a strong synteny with other Peronosporales species. The history of Pl. halstedii invasion in France over the last 60 years was documented by identifying founder strains and their admixture patterns. The emergence of pathotypes with broader virulence spectra and therefore capable of overcoming host resistance was associated with genomic reshuffling. We highlighted genomic mosaicism in admixed pathotypes and identified regions associated with the breakdown of host resistance genes harbouring putative effector genes. C_LIO_LIOur findings provide insights into evolutionary mechanisms underlying plant pathogen host adaptation, which has implications for a sustainable deployment of multiple resistance genes. C_LI

plant biology↗

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

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 the P. viticola genome, 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 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 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 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. 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.

genetics↗

An effector deletion leads to the breakdown of partial grapevine resistance to downy mildew

Grapevine downy mildew, caused by the oomycete Plasmopara viticola, is a globally destructive disease that particularly affect the Eurasian wine grape V. vinifera. While genetically resistant varieties are becoming more accessible, populations of P. viticola are demonstrating rapid adaptability, successfully over-coming these resistances. Here we aimed to identify the avirulence genes involved in the interaction with the Rpv3.1-mediated resistance in grapevine. We sequenced the full genome of 136 P. viticola strains sampled in a natural population of Bordeaux (France) and characterized their development on both resistant and sensitive cultivars. The genome-wide association study allowed the identification of a genomic region associated with the breakdown of Rpv3.1 grapevine resistance (avrRpv3.1 locus). A diploid-aware reassembly of the P. viticola INRA-Pv221 genome allowed to detect structural variations in this locus, including a major 30 Kbp deletion. At the avrRpv3.1 locus, virulent P. viticola strains presented deletion on both haplotypes indicating that avirulence is recessive. The deletion involves two closely-related genes that encode proteins containing 800-900 amino acids with a signal peptide. The structure of the predicted proteins contains repeats of the LWY-fold structural modules, typical of oomycete effectors. Moreover, when these proteins were transiently expressed, they induced cell death in grapevines carrying Rpv3.1 resistance, confirming their avirulence nature. The first description of candidate effectors of P. viticola involved in the interaction with resistance gene provides valuable insights into the genetic mechanisms that enable P. viticola to adapt to grapevine resistance, laying a foundation for developing strategies to manage this damaging crop pathogen.

evolutionary biology↗

The quasi-universality of nestedness in the structure of quantitative plant-parasite interactions

AO_SCPLOWBSTRACTC_SCPLOWUnderstanding the relationships between host range and pathogenicity for parasites, and between the efficiency and scope of immunity for hosts are essential to implement efficient disease control strategies. In the case of plant parasites, most studies have focused on describing qualitative interactions and a variety of genetic and evolutionary models has been proposed in this context. Although plant quantitative resistance benefits from advantages in terms of durability, we presently lack models that account for quantitative interactions between plants and their parasites and the evolution of these interactions. Nestedness and modularity are important features to unravel the overall structure of host-parasite interaction matrices. Here, we analysed these two features on 32 matrices of quantitative pathogenicity trait data gathered from 15 plant-parasite pathosystems consisting of either annual or perennial plants along with fungi or oomycetes, bacteria, nematodes, insects and viruses. The performance of several nestedness and modularity algorithms was evaluated through a simulation approach, which helped interpretation of the results. We observed significant modularity in only six of the 32 matrices, with two or three modules detected. For three of these matrices, modules could be related to resistance quantitative trait loci present in the host. In contrast, we found high and significant nestedness in 30 of the 32 matrices. Nestedness was linked to other properties of plant-parasite interactions. First, pathogenicity trait values were explained in majority by a parasite strain effect and a plant accession effect, with no or minor parasite-plant interaction term. Second, correlations between the efficiency and scope of the resistance of plant genotypes, and between the host range breadth and pathogenicity level of parasite strains were overall positive. This latter result questions the efficiency of strategies based on the deployment of several genetically-differentiated cultivars of a given crop species in the case of quantitative plant immunity.

pathology↗

Europe as a bridgehead in the worldwide invasion history of grapevine downy mildew, Plasmopara viticola

Europe is the historical cradle of viticulture, but grapevines have been increasingly threatened by pathogens of American origin. The invasive oomycete Plasmopara viticola causes downy mildew, one of the most devastating grapevine diseases worldwide. Despite major economic consequences, its invasion history remains poorly understood. Comprehensive population genetic analyses of ~2000 samples from the most important wine-producing countries revealed very low genetic diversity in invasive downy mildew populations worldwide. All the populations originated from one of five native North American lineages, the one parasitizing wild summer grape. After an initial introduction into Europe, invasive European populations served as a secondary source of introduction into vineyards worldwide, including China, South Africa and, twice independently, Australia. Invasion of Argentina probably represents a tertiary introduction from Australia. Our findings provide a striking example of a global pathogen invasion resulting from secondary dispersal of a successful invasive population. It will help designing quarantine regulations and efficient breeding for resistance against grapevine downy mildew.

evolutionary biology↗

Identification of the first oomycete mating-type locus sequence in the grapevine downy mildew pathogen, Plasmopara viticola

Mating types are self-incompatibility systems that promote outcrossing in plants, fungi and oomycetes. Mating-type genes have been widely studied in plants and fungi, but have yet to be identified in oomycetes, eukaryotic organisms closely related to brown algae that cause many destructive animal and plant diseases. We identified the mating-type locus of Plasmopara viticola, the oomycete responsible for grapevine downy mildew, one of the most damaging grapevine diseases worldwide. Using a genome-wide association approach, we identified a 570 kb repeat-rich non-recombining region controlling mating types, with two highly divergent alleles. We showed that one mating type was homozygous, whereas the other was heterozygous at this locus. The mating-type locus encompassed 40 genes, including one encoding a putative hormone receptor. Our findings have fundamental implications for our understanding of the evolution of mating types, as they reveal a unique determinism involving an asymmetry of heterozygosity, as in sex chromosomes and unlike other mating-type systems. This identification of the mating-type locus in such an economically important crop pathogen also has applied implications, as outcrossing facilitates rapid evolution and resistance to harsh environmental conditions.

evolutionary biology↗

A high-quality grapevine downy mildew genome assembly reveals rapidly evolving and lineage-specific putative host adaptation genes

Downy mildews are obligate biotrophic oomycete pathogens that cause devastating plant diseases on economically important crops. Plasmopara viticola is the causal agent of grapevine downy mildew, a major disease in vineyards worldwide. We sequenced the genome of Pl. viticola with PacBio long reads and obtained a new 92.94 Mb assembly with high continuity (359 scaffolds for a N50 of 706.5 kb) due to a better resolution of repeat regions. This assembly presented a high level of gene completeness, recovering 1,592 genes encoding secreted proteins involved in plant-pathogen interactions. Pl. viticola had a two-speed genome architecture, with secreted protein-encoding genes preferentially located in gene-sparse, repeat-rich regions and evolving rapidly, as indicated by pairwise dN/dS values. We also used short reads to assemble the genome of Plasmopara muralis, a closely related species infecting grape ivy (Parthenocissus tricuspidata). The lineage-specific proteins identified by comparative genomics analysis included a large proportion of RxLR cytoplasmic effectors and, more generally, genes with high dN/dS values. We identified 270 candidate genes under positive selection, including several genes encoding transporters and components of the RNA machinery potentially involved in host specialization. Finally, the Pl. viticola genome assembly generated here will allow the development of robust population genomics approaches for investigating the mechanisms involved in adaptation to biotic and abiotic selective pressures in this species.\n\nDATA AVAILABILITYRaw reads and genome assemblies have been deposited in GenBank (BioProjects PRJNA329579 for Pl. viticola and PRJNA448661 for Pl. muralis). Genome assemblies, gene annotations and analysis files (e.g. orthology relationships, full tables for GO enrichment analyses, pairwise dN/dS values and branch-site tests) have been deposited in Dataverse (Pl. viticola assembly and annotation: doi.org/10.15454/4NYHD6, Pl. muralis assembly and annotation: doi.org/10.15454/Q1QJYK, analysis files: doi.org/10.15454/8NZ8X9). Links to the data and information about the grapevine downy mildew genome project can be found at http://grapevine-downy-mildew-genome.com/.

genomics↗