Search bioRxiv⌕ Search

Biology subjects

Caffier, V.

Publications and source records attributed to Caffier, V..

4 recordsLinked to original sources

Ancient MAX Effector Variants of a Fungal Pathogen Evade Apoplastic Immunity in Apple

Venturia inaequalis is an Ascomycota fungus responsible for apple scab, the main disease in apple orchards. During infection, the pathogen colonizes the subcuticular space and secretes effectors to promote virulence. To mitigate disease impact, resistance genes such as Rvi6, which encodes a membrane-localized receptor-like protein, have been introduced into apple cultivars. However, over the past three decades, Rvi6-mediated resistance has been circumvented in orchards, with the emergence of virulent V. inaequalis strains. Through comparative genomics analyses and functional validation by complementation, we identified AvrRvi6 as the fungal determinant that activates Rvi6-mediated immunity. Screening 122 V. inaequalis strains worldwide, we identified 20 distinct AvrRvi6 alleles, of which only five are not recognized by Rvi6. Evolution analysis demonstrated that the emergence of these virulent alleles predates the domestication of apple, thus revealing that wild Malus species constitute a reservoir of virulence. Using AlphaFold structural modeling, we showed that AvrRvi6 belongs to an expanded family that adopts a MAX effector fold, originally described for cytoplasmic effectors of the blast fungus Pyricularia oryzae. Transient expression in Nicotiana benthamiana demonstrated that AvrRvi6 triggers allele-specific apoplastic immunity and validated three different molecular mechanisms (mutation, partial deletion and transposon insertion in the promoter) that V. inaequalis employs to circumvent Rvi6 recognition. This study delivers the first characterization of a V. inaequalis avirulence factor, uncovers an unexpected apoplastic role for a MAX effector, and demonstrates how ancestral virulence diversity maintained in wild populations compromises resistance durability in apple.

microbiology↗

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↗

Asian wild apples threatened by gene flow from domesticated apples and by their pestified pathogen

Massive gene flow between crops and their wild relatives may threaten the genetic integrity of wild species. Such threats are now well documented, but little is known about indirect consequences involving the spillover of crop pathogens to wild plants or introgression between crop and wild pathogens. To address these questions, we used population genetics approaches, demographic inference and pathogenicity tests on host-pathogen pairs composed of wild or domesticated apple trees of Central Asia and their fungal pathogen, Venturia inaequalis, itself showing differentiated agricultural-type and wild-type populations. We confirmed the occurrence of gene flow from cultivated to wild apple trees in Asian forests, threatening the Asian wild apple genetic integrity. SNP markers and demographic modeling revealed the occurrence of a secondary contact followed by hybridization between agricultural-type and wild-type fungal pathogen populations, and the dispersal of the agricultural-type pathogen in wild forests. We detected a SNP predicting the ability of the fungus to parasitize the different host populations, which induced an early stop codon in a gene coding for a small secreted protein in the agricultural-type fungal population, thus representing a putative avirulence gene which function loss would enable to parasitize cultivated apples. Pathogenicity tests in fact revealed the pestification of V. inaequalis, with higher virulence of the agricultural-type population on both wild and domesticated trees. Our findings highlight the threat posed by cultivating a crop near its center of origin, with the invasion of a pestified pathogen on wild plants and introgression in the wild-type pathogen.

evolutionary biology↗

Population genome sequencing of the scab fungal species Venturia inaequalis, Venturia pirina, Venturia aucupariae and Venturia asperata.

The Venturia genus comprises fungal species that are pathogens on Rosaceae host plants, including V. inaequalis and V. asperata on apple, V. aucupariae on sorbus and V. pirina on pear. Although the genetic structure of V. inaequalis populations has been investigated in detail, genomic features underlying these subdivisions remain poorly understood. Here, we report whole genome sequencing of 87 Venturia strains that represent each species and each population within V. inaequalis. We present a PacBio genome assembly for the V. inaequalis EU-B04 reference isolate. The size of selected genomes was determined by flow cytometry, and varied from 45 to 93 Mb. Genome assemblies of V. inaequalis and V. aucupariae contain a high content of transposable elements (TEs), most of which belong to the Gypsy or Copia LTR superfamilies and have been inactivated by Repeat-Induced Point mutations. The reference assembly of V. inaequalis presents a mosaic structure of GC-equilibrated regions that mainly contain predicted genes and AT-rich regions, mainly composed of TEs. Six pairs of strains were identified as clones. Single-Nucleotide Polymorphism (SNP) analysis between these clones revealed a high number of SNPs that are mostly located in AT-rich regions due to misalignments and allowed determining a false discovery rate. The availability of these genome sequences is expected to stimulate genetics and population genomics research of Venturia pathogens. Especially, it will help understanding the evolutionary history of Venturia species that are pathogenic on different hosts, a history that has probably been substantially influenced by TEs.

plant biology↗