A.C.M. van Wees

Differential Induction of Systemic Resistance in Arabidopsis by Biocontrol Bacteria

Selected nonpathogenic, root-colonizing bacteria are able to elicit induced systemic resistance (ISR) in plants. To elucidate the molecular mechanisms underlying this type of systemic resistance, an Arabidopsis-based model system was developed in which Pseudomonas syringae pv. tomato and Fusarium oxysporum f. sp. raphani were used as challenging pathogens. In Arabidopsis thaliana ecotypes Columbia and Landsberg erecta, colonization of the rhizosphere by P. fluorescens strain WCS417r induced systemic resistance against both pathogens. In contrast, ecotype RLD did not respond to WCS417r treatment, whereas all three ecotypes expressed systemic acquired resistance upon treatment with salicylic acid (SA). P. fluorescens strain WCS374r, previously shown to induce ISR in radish, did not elicit ISR in Arabidopsis. The opposite was found for P. putida strain WCS358r, which induced ISR in Arabidopsis but not in radish. These results demonstrate that rhizosphere pseudomonads are differentially active in eliciting ISR in related plant species. The outer membrane lipopolysaccharide (LPS) of WCS417r is the main ISR-inducing determinant in radish and carnation, and LPS-containing cell walls also elicit ISR in Arabidopsis. However, mutant WCS417rOA-, lacking the O-antigenic side chain of the LPS, induced levels of protection similar to those induced by wild-type WCS417r. This indicates that ISR-inducing bacteria produce more than a single factor that trigger ISR in Arabidopsis. Furthermore, WCS417r and WCS358r induced protection in both wild-type Arabidopsis and SA-nonaccumulating NahG plants without activating pathogenesis-related gene expression. This suggests that elicitation of an SA-independent signaling pathway is a characteristic feature of ISR-inducing biocontrol bacteria.

Rhizobacteria-mediated induced systemic resistance (ISR) in Arabidopsis is not associated with a direct effect on expression of known defense-related genes but stimulates the expression of the jasmonate-inducible gene Atvsp upon challenge.

Selected strains of nonpathogenic rhizobacteria from the genus Pseudomonas are capable of eliciting broad-spectrum induced systemic resistance (ISR) in plants that is phenotypically similar to pathogen-induced systemic acquired resistance (SAR). In Arabidopsis, the ISR pathway functions independently of salicylic acid (SA) but requires responsiveness to jasmonate and ethylene. Here, we demonstrate that known defense-related genes, i.e. the SA-responsive genes PR-1, PR-2, and PR-5, the ethylene-inducible gene Hel, the ethylene- and jasmonate-responsive genes ChiB and Pdf1.2, and the jasmonate-inducible genes Atvsp, Lox1, Lox2, Pal1, and Pin2, are neither induced locally in the roots nor systemically in the leaves upon induction of ISR by Pseudomonas fluorescens WCS417r. In contrast, plants infected with the virulent leaf pathogen Pseudomonas syringae pv. tomato (Pst) or expressing SAR induced by preinfecting lower leaves with the avirulent pathogen Pst(avrRpt2) exhibit elevated expression levels of most of the defense-related genes studied. Upon challenge inoculation with Pst, PR gene transcripts accumulated to a higher level in SAR-expressing plants than in control-treated and ISR-expressing plants, indicating that SAR involves potentiation of SA-responsive PR gene expression. In contrast, pathogen challenge of ISR-expressing plants led to an enhanced level of Atvsp transcript accumulation. The other jasmonate-responsive defense-related genes studied were not potentiated during ISR, indicating that ISR is associated with the potentiation of specific jasmonate-responsive genes.

Plant Immunity: It’s the Hormones Talking, But What Do They Say?

Plants live in complex environments in which they intimately interact with a broad range of other organisms. Besides the plethora of deleterious interactions with pathogens and insect herbivores, relationships with beneficial microorganisms are frequent in nature as well, improving plant growth or helping the plant to overcome stress. The evolutionary arms race between plants and their enemies provided plants with a highly sophisticated defense system that, like the animal innate immune system, recognizes nonself molecules or signals from injured cells, and responds by activating an effective immune response against the invader encountered. Recent advances in plant immunity research underpin the pivotal role of cross-communicating hormones in the regulation of the plant’s defense signaling network (Spoel and Dong, 2008; Pieterse et al., 2009). Their powerful regulatory potential allows the plant to quickly adapt to its hostile environment and to utilize its resources in a cost-efficient manner. Plant enemies on the other hand, can hijack the plant’s defense signaling network for their own benefit by affecting hormone homeostasis to antagonize the host immune response (Grant and Jones, 2009). Similarly, beneficial microbes actively interfere with hormone-regulated immune responses to avoid being recognized as an alien organism (Van Wees et al., 2008). In nature, plants simultaneously or sequentially interact with multiple beneficial and antagonistic organisms with very different lifestyles. However, knowledge on how the hormone-regulated plant immune signaling network functions during multispecies interactions is still in its infancy. Bioinformatic and systems biology approaches will prove essential to crack this tough nut.