Genome‐wide transcriptional analysis of the Arabidopsis thaliana interaction with the plant pathogen Pseudomonas syringae pv. tomato DC3000 and the human pathogen Escherichia coli O157:H7

Abstract

Genome-wide transcriptional analysis of the Arabidopsis thaliana interaction with the plant pathogen Pseudomonas syringae pv. tomato DC3000 and the human pathogen Escherichia coli O157:H7 SummaryPseudomonas syringae pv. tomato DC3000 (Pst) is a virulent pathogen that causes disease on tomato and Arabidopsis. The type III secretion system (TTSS) plays a key role in pathogenesis by translocating virulence effectors from the bacteria into the plant host cell, while the phytotoxin coronatine (COR) contributes to virulence and disease symptom development. Recent studies suggest that both the TTSS and COR are involved in the suppression of host basal defenses. However, little is known about the interplay between the host gene expression changes associated with basal defenses and the virulence activities of the TTSS and COR during infection. In this study, we used the Affymetrix full genome chip to determine the Arabidopsis transcriptome associated with basal defense to Pst DC3000 hrp mutants and the human pathogenic bacterium Escherichia coli O157:H7. We then used Pst DC3000 virulence mutants to characterize Arabidopsis transcriptional responses to the action of hrp-regulated virulence factors (e.g. TTSS and COR) during bacterial infection. Additionally, we used bacterial fliC mutants to assess the role of the pathogen-associated molecular pattern flagellin in induction of basal defense-associated transcriptional responses. In total, our global gene expression analysis identified 2800 Arabidopsis genes that are reproducibly regulated in response to bacterial pathogen inoculation. Regulation of these genes provides a molecular signature for Arabidopsis basal defense to plant and human pathogenic bacteria, and illustrates both common and distinct global virulence effects of the TTSS, COR, and possibly other hrp-regulated virulence factors during Pst DC3000 infection.Keywords: coronatine, type III secretion, virulence, effectors, basal defense, PAMP. IntroductionPseudomonas syringae strains collectively infect hundreds of taxonomically diverse plant species and cause disease symptoms ranging from leaf spots to stem cankers (Hirano and Upper, 2000). The P. syringae pv. tomato (Pst) strain DC3000 used in this study causes necrotic lesions that are often surrounded by chlorotic halos in susceptible tomato and Arabidopsis plants (Katagiri et al., 2002;Ma et al., 1991;Whalen et al., 1991). To successfully colonize plants, P. syringae strains have evolved a variety of virulence factors to subvert host defenses or to obtain nutrients. One common virulence mechanism is the hrp-gene-encoded type III protein secretion system (TTSS; He et al., 2004;Jin et al., 2003). The TTSS is used by P. syringae to inject >40 virulence effector proteins into the host cell (Chang et al., 2005;Collmer et al., 2002;Greenberg and Vinatzer, 2003;. Different P. syringae strains also produce a variety of phytotoxins (Bender et al., 1999). Although phytotoxins are generally not required for bacterial pathogenicity, they do enhance pathogen virulence in...

Perturbation of Maize Phenylpropanoid Metabolism by an AvrE Family Type III Effector fromPantoea stewartii

“…P. syringae perturbed the expression of key enzymes of the phenylpropanoid pathway, as well as down-regulated photosynthesis, in Arabidopsis (Thilmony et al, 2006;Truman et al, 2006). In a compatible E. amylovora-apple pathosystem, the induced expression of phenylpropanoid pathway genes is delayed in a T3SS-dependent manner (Venisse et al, 2002).…”

The Pseudomonas syringae Type III Effector AvrRpt2 Promotes Pathogen Virulence via Stimulating Arabidopsis Auxin/Indole Acetic Acid Protein Turnover

“…The ABA signaling pathway is also a target for P. syringae type III effectors (de Torres-Zabala et al, 2007). In addition to type III effectors, other virulence factors, such as the phytotoxin coronatine, could also modulate auxin or other hormone levels or signaling (Thilmony et al, 2006). Thus, the modulation of host hormone physiology is a common virulence strategy among plant pathogens.…”

Regulation of tradeoffs between plant defenses against pathogens with different lifestyles

“…Perhaps in systemic tissues the SA/JA cross-talk is counteracted by the systemic accumulation of the bacterial produced phytotoxin coronatine (40). Coronatine is a mimic of JA that activates a battery of JA-responsive genes (24,25) and has been shown to promote Pst DC3000 virulence by overcoming SA-mediated defense (41). We tested this hypothesis by using the Pst DC3000 cmaA/cfa6 double mutant (42) and found that coronatine deficiency in this double mutant did not affect cross-talk in systemic tissue at the level of gene expression or disease resistance (S.H.S.…”

“…tomato (Pst) DC3000 can simultaneously trigger synthesis of both SA and JA (22). This pathogen produces a JA-mimicking phytotoxin, coronatine, which can induce a set of JA-responsive genes (23)(24)(25). Because coronatine/ JA-insensitive coi1/jai1 mutant plants exhibit elevated expression of SA-responsive PR genes and enhanced resistance to Pst DC3000 (26,27), coronatine is thought to increase pathogen virulence partly by diversion of the plant's SA-dependent defenses.…”