Comparative analysis of the predicted secretomes of Rosaceae scab pathogens Venturia inaequalis and V. pirina reveals expanded effector families and putative determinants of host range

Abstract

BackgroundFungal plant pathogens belonging to the genus Venturia cause damaging scab diseases of members of the Rosaceae. In terms of economic impact, the most important of these are V. inaequalis, which infects apple, and V. pirina, which is a pathogen of European pear. Given that Venturia fungi colonise the sub-cuticular space without penetrating plant cells, it is assumed that effectors that contribute to virulence and determination of host range will be secreted into this plant-pathogen interface. Thus the predicted secretomes of a range of isolates of Venturia with distinct host-ranges were interrogated to reveal putative proteins involved in virulence and pathogenicity.ResultsGenomes of Venturia pirina (one European pear scab isolate) and Venturia inaequalis (three apple scab, and one loquat scab, isolates) were sequenced and the predicted secretomes of each isolate identified. RNA-Seq was conducted on the apple-specific V. inaequalis isolate Vi1 (in vitro and infected apple leaves) to highlight virulence and pathogenicity components of the secretome. Genes encoding over 600 small secreted proteins (candidate effectors) were identified, most of which are novel to Venturia, with expansion of putative effector families a feature of the genus. Numerous genes with similarity to Leptosphaeria maculans AvrLm6 and the Verticillium spp. Ave1 were identified. Candidates for avirulence effectors with cognate resistance genes involved in race-cultivar specificity were identified, as were putative proteins involved in host-species determination. Candidate effectors were found, on average, to be in regions of relatively low gene-density and in closer proximity to repeats (e.g. transposable elements), compared with core eukaryotic genes.ConclusionsComparative secretomics has revealed candidate effectors from Venturia fungal plant pathogens that attack pome fruit. Effectors that are putative determinants of host range were identified; both those that may be involved in race-cultivar and host-species specificity. Since many of the effector candidates are in close proximity to repetitive sequences this may point to a possible mechanism for the effector gene family expansion observed and a route to diversification via transposition and repeat-induced point mutation.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-017-3699-1) contains supplementary material, which is available to authorized users.

Specific Hypersensitive Response–Associated Recognition of New Apoplastic Effectors from Cladosporium fulvum in Wild Tomato

“…Homologs of Ecp10-1 were also identified in several Sordariomycete fungi. Interestingly, Ecp10-1 homologs were found to be massively expanded in V. inaequalis and V. pirina, which is not uncommon for effector candidates from these fungi (Deng et al 2017). Smaller expansions were also identified in other fungal plant pathogens.…”

Chromosome-level genome reference ofVenturia effusa, causative agent of pecan scab

“…At present, there are more than 90 genome assemblies available for Venturia species, representing an active research area of fungal genomics. However, many of the genomes are highly fragmented ranging from 66 scaffolds to more than 40,000 (Bock et al 2016b;Chen et al 2017;Deng et al 2017;Passey et al 2018;Johnson et al 2019;Le Cam et al 2019;Prokchorchik et al 2019). Here, we present the first entire and finished genome sequence for the genus Venturia.…”

“…Subsequently, the evolution of effector genes underlying gene-for-gene interactions in the L. maculans-Brassica Napus pathosystem has been shown to be associated with their proximity to or position within AT-rich regions (Van de Wouw et al 2010;Rouxel et al 2011). Gene-for-gene interactions have been described for other Venturia species (Bus et al 2011;Deng et al 2017) and effectors are likely to be important for the V. effusa-C. illinoinensis interaction. A gapless genome assembly of V. effusa spanning complete AT-rich regions is crucial to identify and understand the evolution of effector genes in the species.…”

“…Although other Venturia genomes have been sequenced (Bock et al 2016b;Chen et al 2017;Deng et al 2017;Passey et al 2018;Johnson et al 2019;Le Cam et al 2019;Prokchorchik et al 2019), the complete genome sequence of V. effusa FRT5LL7-Albino represents the first chromosomal level assembly of a Venturia species. This valuable resource is a basis for scientists in the Venturia research community to advance the comparative genomics of scab pathogens; it is a useful resource for the identification of effectors, will provide insights into the epidemiology and population biology of the pathogens, and the evolution of the genus Venturia.…”

Draft Genome Sequence of the Asian Pear Scab Pathogen, Venturia nashicola

“…Here, we present the first draft assembly of the WGS of the Asian pear scab fungus, V. nashicola, isolate Yasato 2-1-1. This draft WGS of V. nashicola will enable the identification of candidate effectors and genes involved in fungicide resistance, and contributes to the current genomic resources for Venturia spp., specifically V. pirina (Cooke et al 2014), Fusicladium effusum (pecan scab fungus) (Bock et al 2016), V. inaequalis (apple scab fungus) (Deng et al 2017) and V. carpophila (peach scab fungus) (Chen et al 2017).…”