Scab resistance in 'Geneva' apple is conditioned by a resistance gene cluster with complex genetic control

Abstract

Apple scab, caused by the fungal pathogen Venturia inaequalis, is one of the most severe diseases of apple worldwide. It is the most studied plant-pathogen interaction involving a woody species using modern genetic, genomic, proteomic and bioinformatic approaches in both species. Although 'Geneva' apple was recognized long ago as a potential source of resistance to scab, this resistance has not been characterized previously. Differential interactions between various monoconidial isolates of V. inaequalis and six segregating F1 and F2 populations indicate the presence of at least five loci governing the resistance in 'Geneva'. The 17 chromosomes of apple were screened using genotyping-by-sequencing, as well as single marker mapping, to position loci controlling the V. inaequalis resistance on linkage group 4. Next, we fine mapped a 5-cM region containing five loci conferring both dominant and recessive scab resistance to the distal end of the linkage group. This region corresponds to 2.2 Mbp (from 20.3 to 22.5 Mbp) on the physical map of 'Golden Delicious' containing nine candidate nucleotide-binding site leucine-rich repeat (NBS-LRR) resistance genes. This study increases our understanding of the complex genetic basis of apple scab resistance conferred by 'Geneva', as well as the gene-for-gene (GfG) relationships between the effector genes in the pathogen and resistance genes in the host.

Keywords: Venturia inaequalis; apple scab; differential host; fine genetic mapping; gene-for-gene relationships; molecular marker; resistance.

Figure 1

Development of a high‐density linkage map using genotyping‐by‐sequencing (GBS) sequence tags and phenotypic data for reaction to the isolates EU‐NL19, EU‐B04, 1639 and 1774‐1 in ‘Gala’ × Q71 progeny. Marker names indicate the physical location of the single nucleotide polymorphism (SNPs) at the lower end of chromosome 4 of the ‘Golden Delicious’ genome assembly. LG4, linkage group 4.

Figure 2

Genetic linkage analysis for the resistant parents ‘Geneva’ among single nucleotide polymorphism (SNP) and single sequence repeat (SSR) molecular markers on linkage group 4 (LG4) of F1 families ‘Elstar’ × ‘Geneva’ and ‘Geneva’ × ‘Braeburn’, and resistance towards various monoconidial Venturia inaequalis isolates. BB, ‘Braeburn’; E, ‘Elstar’; LOD, logarithm of odds.

Figure 3

Genetic maps of linkage group 4 (in cM) of F1 resistant parents Q71, M33, Q35 crossed with ‘Gala’ (G), ‘Golden Delicious’ (GD) and ‘Elstar’ (E), respectively, and resistance towards various monoconidial Venturia inaequalis isolates. On the left of each map, arrows indicate the position on the reference ‘Golden Delicious’ physical map (in Mbp) of the closest molecular markers flanking each resistance locus. LOD, logarithm of odds.

Figure 4

Consensus map of linkage group 4 (LG4) of ‘Geneva’ derived from the populations ‘Geneva’ × BB, GD × M33, G × Q71 and E × Q35, aligned with the homologous region of the reference apple genome (Velasco et al., 2010), showing the relative positions of the mapped disease resistance loci (Rvh3.1–3 and rvh3.4–5) to candidate disease resistance genes [nucleotide‐binding site leucine‐rich repeat (NBS‐LRR) family protein] on the genome assembly. BB, ‘Braeburn’; E, ‘Elstar’; G, ‘Gala’; GD, ‘Golden Delicious’.