GENETICS AND GENOMICS OF VENTURIA INAEQUALIS, PODOSPHAERA LEUCOTRICHA, AND PODOSPHAERA APHANIS: KEY FUNGAL PATHOGENS OF UK FRUIT CROPS

The value of UK fruit production in 2020 was estimated to be over £1.5 billion. Plant pests and diseases pose a serious threat to productivity, causing losses of up to one?third. Amongst the most damaging diseases for UK apple and strawberry growers are apple scab, apple powdery mildew, and strawberry powdery mildew. Molecular techniques are increasingly relied upon for pathogen identification and the study of infection and crop resistance; it is therefore essential to have a genomic understanding of pathogens. To address this issue, a study was conducted to investigate the genetics of the fungal pathogens responsible for these diseases: Venturia inaequalis, Podosphaera leucotricha, and Podosphaera aphanis.

Quantitative Trait Loci (QTL) mapping was used to identify genetic loci associated with reduced susceptibility to tebuconazole in V. inaequalis. This resulted in the identification of two loci and polygenic resistance. Both QTL were distal to the CYP51 target of azole fungicides. These loci may contain a trans regulatory transcription factor affecting CYP51 or imply that a CYP51 independent resistance mechanism has developed in V. inaequalis, such as increased efflux transporter activity. Within QTL regions, non-synonymous mutations were observed in several ATP-Binding Cassette and Major Facilitator SuperFamily transporter genes. This work has been published in the Journal of Fungi (Heaven et al., 2023a).

Genome assemblies were constructed for P. leucotricha and P. aphanis. These include the first genome assembly for P. aphanis and the first assembly from a European population of P. leucotricha, published in Phytopathology (Heaven et al., 2023b). Collection of field samples avoided difficulties maintaining powdery mildew cultures, whilst still yielding high-quality genome assemblies following stringent controls for purity. This method has the potential to be applied to other challenging plant pathogens which cannot be cultured easily. The genomic resources developed in this study will accelerate research into apple and strawberry powdery mildew.

Analyses of P. aphanis and P. leucotricha genomes revealed lineage-specific loss of conserved ascomycete genes. Additionally, large numbers of candidate secreted effector proteins (CSEPs) were identified: 330-401 for P. aphanis and 678-718 for P. leucotricha. Five CSEPs were unique to P. aphanis whilst 108 were unique to P. leucotricha. The expansion of the apple powdery mildew effector repertoire may be the result of an arms race between plant and pathogen. Improved powdery mildew resistance is a long-standing objective of apple and strawberry breeding programmes. Knowledge of powdery mildew effectors will accelerate the discovery and functional profiling of host resistance genes and, ultimately, resistance breeding.

This research lays the groundwork for the development of sequencing-based molecular diagnostics for these species, allowing detection of the pathogens and fungicide resistance. Early detection enables growers to identify and respond to disease outbreaks before they become severe, thereby preventing crop damage and reducing the need for extensive spraying. Furthermore, enhanced diagnostic precision can help growers to determine the exact pathogen strain present in the crop, enabling the selection of effective agrochemicals for control and reducing the risk of resistance to these chemicals over time.