A downy mildew effector evades recognition by polymorphism of expression and subcellular localization

Shuta Asai,Jonathan D G Jones,Ken Shirasu,Sandra Goritschnig,Brian J Staskawicz,Naveed Ishaque,Oliver J Furzer,Volkan Cevik,Dae Sung Kim

doi:10.1038/s41467-018-07469-3

Abstract

Pathogen co-evolution with plants involves selection for evasion of host surveillance systems. The oomycete Hyaloperonospora arabidopsidis (Hpa) causes downy mildew on Arabidopsis, and race-specific interactions between Arabidopsis accessions and Hpa isolates fit the gene-for-gene model in which host resistance or susceptibility are determined by matching pairs of plant Resistance (R) genes and pathogen Avirulence (AVR) genes. Arabidopsis Col-0 carries R gene RPP4 that confers resistance to Hpa isolates Emoy2 and Emwa1, but its cognate recognized effector(s) were unknown. We report here the identification of the Emoy2 AVR effector gene recognized by RPP4 and show resistance-breaking isolates of Hpa on RPP4-containing Arabidopsis carry the alleles that either are not expressed, or show cytoplasmic instead of nuclear subcellular localization.

Highlights

Arabidopsis is a host for the biotrophic oomycete Hyaloperonospora arabidopsidis (Hpa; formerly Peronospora parasitica or Hyaloperonospora parasitica), a downy mildew pathogen
We defined a total of 475 Hpa gene models that encode effector candidates in the reference Hpa isolate Emoy[29] by applying the following criteria[10]: (1) proteins with a signal peptide and canonical RxLR motif, like ATR1, ATR13, and ATR39 (HaRxLs)[4,6,7], reported by Baxter et al.[9], (2) RxLR-like proteins with at least one non-canonical feature, like ATR5 (HaRxLLs)[5], (3) putative Crinkler-like proteins with RxLR motif (HaRxLCRNs)[11], (4) homologous proteins based on amino acid sequence similarity over the 5′ region including a signal peptide and RxLR motif (e.g., HaRxL1b, HaRxLL2b, and HaRxLCRN3b)
In Hpa Emoy2-infected Arabidopsis Col-0, transcripts from Hpa clearly decreased from 1 day post-inoculation, consistent with Hpa Emoy[2] growth being arrested upon recognition by

Summary

Introduction

Arabidopsis is a host for the biotrophic oomycete Hyaloperonospora arabidopsidis (Hpa; formerly Peronospora parasitica or Hyaloperonospora parasitica), a downy mildew pathogen. This model pathosystem has revealed cognate host R and pathogen AVR genes, termed RPP (recognition of Peronospora parasitica) and ATR (Arabidopsis thaliana recognized), respectively[2]. In Arabidopsis Col-0, RPP4 confers resistance to Hpa isolates Emoy[2] and Emwa[112], but its cognate AVR effector gene(s) were not identified. We report here, using comparative genomics and transcriptomics among different isolates of Hpa, that the effector candidate HaRxL103 corresponds to the AVR gene. We show that different Hpa resistance-breaking strains evade detection by RPP4 using two distinct mechanisms

Methods

Results

Conclusion