Intragenomic variants of a putative effector drive early-stage infection in a broad host-range rust fungus

Abstract

Rust fungi are pathogens that impact plants of environmental, agricultural, cultural, and economic importance. Their mechanisms of pathogenicity are not well-understood but are likely governed by effectors, secreted proteins that manipulate host cellular processes to facilitate infection and suppress immune responses. We sought to understand how three effector candidates (EFC1, EFC2, and EFC3) expressed in the first stages of Austropuccinia psidii (myrtle rust) infection influence pathogenicity. We experimentally tested gene function through application of double-stranded RNA (dsRNA) and characterised the genomic landscape of putative effectors expressed during infection to assess whether putative effectors are needed for infection, and whether they are under selection pressure. One of the three screened candidates, EFC1, met our criteria of an effector in that it was predicted to be secreted, and was needed to cause but not maintain infection. We identified that this effector belongs to a gene family of intragenomic variants in tandem repeats flanked by transposable elements. Single nucleotide polymorphisms among these variants have signatures of non-neutral selection. This effector has predicted structural homology to a glycosaminoglycan-binding domain and may have a role in pectin or chitin-binding. We hypothesise that intragenomic variability in this family of effector genes facilitates host-range versatility in the A. psidii-Myrtaceae pathosystem.