Transcriptional Dynamics Driving MAMP-Triggered Immunity and Pathogen Effector-Mediated Immunosuppression in Arabidopsis Leaves Following Infection with Pseudomonas syringae pv tomato DC3000

Abstract

Transcriptional reprogramming is integral to effective plant defense. Pathogen effectors act transcriptionally and posttranscriptionally to suppress defense responses. A major challenge to understanding disease and defense responses is discriminating between transcriptional reprogramming associated with microbial-associated molecular pattern (MAMP)-triggered immunity (MTI) and that orchestrated by effectors. A high-resolution time course of genome-wide expression changes following challenge with Pseudomonas syringae pv tomato DC3000 and the nonpathogenic mutant strain DC3000hrpA-allowed us to establish causal links between the activities of pathogen effectors and suppression of MTI and infer with high confidence a range of processes specifically targeted by effectors. Analysis of this information-rich data set with a range of computational tools provided insights into the earliest transcriptional events triggered by effector delivery, regulatory mechanisms recruited, and biological processes targeted. We show that the majority of genes contributing to disease or defense are induced within 6 h postinfection, significantly before pathogen multiplication. Suppression of chloroplast-associated genes is a rapid MAMP-triggered defense response, and suppression of genes involved in chromatin assembly and induction of ubiquitin-related genes coincide with pathogen-induced abscisic acid accumulation. Specific combinations of promoter motifs are engaged in fine-tuning the MTI response and active transcriptional suppression at specific promoter configurations by P. syringae.

Plant-Pathogen Effectors: Cellular Probes Interfering with Plant Defenses in Spatial and Temporal Manners

“…Transcriptome analyses have revealed that 44% of Arabidopsis genes are differentially regulated after inoculation with P. syringae (63). Similarly, U. maydis induces transcriptional reprogramming of up to 21% of maize genes (28).…”

Architecture and Dynamics of the Jasmonic Acid Gene Regulatory Network

“…To go beyond earlier studies that analyzed the JA transcriptional response with a limited number of time points, we generated a high-resolution time series of JA-mediated transcriptional reprogramming in Arabidopsis leaves. Previously, similar types of dense time series experiments with Arabidopsis have been successfully utilized to help decipher gene regulatory networks underpinning a variety of biological processes, such as senescence and responsiveness to infection by Botrytis cinerea and Pseudomonas syringae (Breeze et al, 2011;Windram et al, 2012;Lewis et al, 2015). Here, we used RNA-seq technology to profile whole-genome transcriptional expression in Arabidopsis leaves just before the treatments (t = 0 h), and over 14 consecutive time points within 16 h following application of methyl JA (MeJA; which is readily converted to JA) or a mock solution to the leaves of intact plants (Supplemental Data Set 1).…”

Plastic Transcriptomes Stabilize Immunity to Pathogen Diversity: The Jasmonic Acid and Salicylic Acid Networks within the Arabidopsis/Botrytis Pathosystem

“…In contrast to previous studies that used a single genetic isolate of the pathogen and different time points as source of variation, this analysis is based on natural genetic variation in the pathogen, which allows for a new perspective (Windram et al, 2012;Howard et al, 2013;Lewis et al, 2015). We first calculated the nonparametric Spearman's rank correlation coefficient of model-corrected transcript means for all gene The relationship of camalexin and lesion area measured on leaves from three Arabidopsis genotypes at 72 HPI with 96 B. cinerea isolates was compared using model-corrected means.…”