Regulation of tradeoffs between plant defenses against pathogens with different lifestyles

Abstract

Plants activate distinct defense responses depending on the lifestyle of the attacker encountered. In these responses, salicylic acid (SA) and jasmonic acid (JA) play important signaling roles. SA induces defense against biotrophic pathogens that feed and reproduce on live host cells, whereas JA activates defense against necrotrophic pathogens that kill host cells for nutrition and reproduction. Cross-talk between these defense signaling pathways has been shown to optimize the response against a single attacker. However, its role in defense against multiple pathogens with distinct lifestyles is unknown. Here we show that infection with biotrophic Pseudomonas syringae, which induces SA-mediated defense, rendered plants more susceptible to the necrotrophic pathogen Alternaria brassicicola by suppression of the JA signaling pathway. This process was partly dependent on the cross-talk modulator NPR1. Surprisingly, this tradeoff was restricted to tissues adjacent to the site of initial infection; A. brassicicola infection in systemic tissue was not affected. Even more surprisingly, tradeoff occurred only with the virulent Pseudomonas strain. Avirulent strains that induced programmed cell death (PCD), an effective plant-resistance mechanism against biotrophs, did not cause suppression of JA-dependent defense. This result might be advantageous to the plant by preventing necrotrophic pathogen growth in tissues undergoing PCD. Our findings show that plants tightly control cross-talk between SA-and JA-dependent defenses in a previously unrecognized spatial and pathogen type-specific fashion. This process allows them to prevent unfavorable signal interactions and maximize their ability to concomitantly fend off multiple pathogens.biotroph ͉ cross-talk ͉ jasmonic acid ͉ necrotroph ͉ salicylic acid

Arabidopsis MYC Transcription Factors Are the Target of Hormonal Salicylic Acid/Jasmonic Acid Cross Talk in Response to Pieris brassicae Egg Extract

“…SA suppressed JA-dependent defense responses in tomato (Solanum lycopersicum; Doares et al, 1995), tobacco (Nicotiana tabacum; Niki et al, 1998), and Arabidopsis (Arabidopsis thaliana; Spoel et al, 2003). Consequently, stimulation of the SA pathway diminished plant response to a necrotrophic fungus (Spoel et al, 2007) and a generalist herbivore (Cipollini et al, 2004). In Arabidopsis, treatments with SA or pathogens that enhance SA levels inhibited expression of herbivore-induced VSP2 and necrotroph-induced PDF1.2 (Koornneef et al, 2008;Leon-Reyes et al, 2009).…”

MYB72 Is Required in Early Signaling Steps of Rhizobacteria-Induced Systemic Resistance in Arabidopsis

“…To test the effectiveness of ISR against A. brassicicola, ISR bioassays were performed in the genetic background of the camalexin-deficient mutant pad3-1. In contrast to wild-type Col-0 plants, pad3-1 is susceptible to A. brassicicola infection and is routinely used in assays to test for induced resistance against this pathogen (Thomma et al, 1999;Ton et al, 2002b;Spoel et al, 2007). Figure 3B shows that induction of ISR in pad3-1 significantly reduced disease symptoms caused by A. brassicicola infection, whereas the pad3-1/ myb72-1 double mutant failed to mount ISR against this pathogen.…”

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

“…ceptible to the necrotrophic fungus Alternaria brassicicola (Spoel et al, 2007). Similarly, prior inoculation with the biotrophic downy mildew pathogen Hyaloperonospora arabidopsidis suppressed JA-mediated defenses that were activated upon feeding by caterpillars of the small cabbage white butterfly (Pieris rapae; .…”

“…Cross talk between ABA-mediated drought stress and JAdependent defense against necrotrophic pathogens in Arabidopsis was recently shown to be regulated by the transcription factor OVEREXPRESSOR OF CATIONIC PEROXIDASE3 (Ramirez et al, 2009). Interestingly, SA was shown to antagonize both adaptive responses (Spoel et al, 2007;Yasuda et al, 2008). However, in the adaptive response of Arabidopsis to heat stress, SA and JA seem to act together (Clarke et al, 2009), highlighting the complexity of the regulatory processes involved in the adaptive response of plants to their continuously changing environment.…”