On the origin and spread of the Scab disease of apple: out of central Asia

Abstract

Background: Venturia inaequalis is an ascomycete fungus responsible for apple scab, a disease that has invaded almost all apple growing regions worldwide, with the corresponding adverse effects on apple production. Monitoring and predicting the effectiveness of intervention strategies require knowledge of the origin, introduction pathways, and population biology of pathogen populations. Analysis of the variation of genetic markers using the inferential framework of population genetics offers the potential to retrieve this information.

Methodology/principal findings: Here, we present a population genetic analysis of microsatellite variation in 1,273 strains of V. inaequalis representing 28 orchard samples from seven regions in five continents. Analysis of molecular variance revealed that most of the variation (88%) was distributed within localities, which is consistent with extensive historical migrations of the fungus among and within regions. Despite this shallow population structure, clustering analyses partitioned the data set into separate groups corresponding roughly to geography, indicating that each region hosts a distinct population of the fungus. Comparison of the levels of variability among populations, along with coalescent analyses of migration models and estimates of genetic distances, was consistent with a scenario in which the fungus emerged in Central Asia, where apple was domesticated, before its introduction into Europe and, more recently, into other continents with the expansion of apple growing. Across the novel range, levels of variability pointed to multiple introductions and all populations displayed signatures of significant post-introduction increases in population size. Most populations exhibited high genotypic diversity and random association of alleles across loci, indicating recombination both in native and introduced areas.

Conclusions/significance: Venturia inaequalis is a model of invasive phytopathogenic fungus that has now reached the ultimate stage of the invasion process with a broad geographic distribution and well-established populations displaying high genetic variability, regular sexual reproduction, and demographic expansion.

Figure 1. Scatterplot of allelic richness and arc surface distance from the most eastern Chinese sample.

A least-square regression line represents the relationship between the two variables. Significance of the correlation was tested using Spearman's r (r = −0.74, P<0.0001).

Figure 2. Principal component analysis of a matrix of chord distance among 29 samples of multilocus microsatellite haplotypes of Venturia inaequalis.

The first, second and third principal components account for 23.2%, 20.9% and 18.7% of variance respectively. For each samples, the diameter of the disk is proportional to allelic richness. CN = China, IR = Iran, AZ = Azerbaijan, F = France, SE = Sweden, SP = Spain, MA = Morocco, US = USA, CA = Canada, BR = Brazil, SA = South Africa, NZ = New Zealand.

Figure 3. Population structure of Venturia inaequalis inferred from 1180 multilocus microsatellite haplotypes using the programs Baps and Structure , .

Each haplotype is represented by a line partitioned into K segments that represent the haplotype's estimated membership fractions in K clusters. K = 6 and K = 7 are the population structure models that best fitted the data using Baps and Structure. CN = China, IR = Iran, AZ = Azerbaijan, F = France, SE = Sweden, SP = Spain, MA = Morocco, US = USA, CA = Canada, BR = Brazil, SA = South Africa, NZ = New Zealand.

Figure 4. Percentage of haplotypes of Venturia inaequalis assigned to 7 regional populations using the assignement method implemented in Geneclass 2 .