Expression Profiling during Arabidopsis/Downy Mildew Interaction Reveals a Highly-Expressed Effector That Attenuates Responses to Salicylic Acid

Abstract

Plants have evolved strong innate immunity mechanisms, but successful pathogens evade or suppress plant immunity via effectors delivered into the plant cell. Hyaloperonospora arabidopsidis (Hpa) causes downy mildew on Arabidopsis thaliana, and a genome sequence is available for isolate Emoy2. Here, we exploit the availability of genome sequences for Hpa and Arabidopsis to measure gene-expression changes in both Hpa and Arabidopsis simultaneously during infection. Using a high-throughput cDNA tag sequencing method, we reveal expression patterns of Hpa predicted effectors and Arabidopsis genes in compatible and incompatible interactions, and promoter elements associated with Hpa genes expressed during infection. By resequencing Hpa isolate Waco9, we found it evades Arabidopsis resistance gene RPP1 through deletion of the cognate recognized effector ATR1. Arabidopsis salicylic acid (SA)-responsive genes including PR1 were activated not only at early time points in the incompatible interaction but also at late time points in the compatible interaction. By histochemical analysis, we found that Hpa suppresses SA-inducible PR1 expression, specifically in the haustoriated cells into which host-translocated effectors are delivered, but not in non-haustoriated adjacent cells. Finally, we found a highly-expressed Hpa effector candidate that suppresses responsiveness to SA. As this approach can be easily applied to host-pathogen interactions for which both host and pathogen genome sequences are available, this work opens the door towards transcriptome studies in infection biology that should help unravel pathogen infection strategies and the mechanisms by which host defense responses are overcome.

Probing formation of cargo/importin‐α transport complexes in plant cells using a pathogen effector

“…(a) Sequencing reads of the nine Arabidopsis importin- αs detected by RNA-Seq in Col-0 rosette leaves (Asai et al ., 2014). Error bars show standard deviation (SD) of three biological replicates.…”

Characterization of the secretome of Plasmopara viticola by de novo transcriptome analysis

“…Similar to the P. sojae 'immediateearly' effectors, Group 1 & 2 PvRXLR effectors show medium to high expression at the 12 h sampling time and increase in expression from 12 to 96 h by an average of 3.5-fold. Like the 'early' P. sojae effectors, the Group 3 PvRXLR effectors show little or no detectable expression at 12 h and 24 h but increase by 10e79 fold between 24 h and 48 h.Finally, expression profiling of H. arabidopsidis effectors secreted during a compatible interaction indicated that the expression of many of the most highly induced HaRxL effectors peaked at 3 dpi [51].…”

“…Group 3 PvRXLR effectors on the other hand, are only weakly expressed during the initial phase of P. viticola penetration and appear to be induced during the period of rapid haustoria formation [52]. This suggests that Group 3-type P. viticola effectors may have more important roles in the suppression of ETI following haustoria formation or the suppression of salicylic acid-triggered defense pathways which have been shown to be targeted by at least two different HaRXL effectors which are maximally expressed at 3 dpi [45,51].…”

Arabidopsis downy mildew effector HaRxL106 suppresses plant immunity by binding to RADICAL‐INDUCED CELL DEATH1

“…While plant innate immunity fends off the majority of attempted infections, specialized pathogens can subvert host defenses with effector proteins that are translocated into host cells. Many pathogen effectors interfere with cellular processes that are essential for innate immunity, such as formation of cell wall appositions, secretion of antimicrobial compounds, production of reactive oxygen species (ROS), or transcriptional activation of defense genes (DebRoy et al, 2004;Nomura et al, 2006;Bozkurt et al, 2011;Anderson et al, 2012;Gangadharan et al, 2013;Asai et al, 2014). Bacterial pathogens have evolved specialized secretion systems to deliver effectors into host cells .…”