Regulation of tradeoffs between plant defenses against pathogens with different lifestyles

By Steven H. Spoel, Jessica S. Johnson, Xinnian Dong. Proceedings of the National Academy of Sciences of the United States of America, 2007

713 citations recorded by the source corpus.

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.

Subfields: Plant Science

View Paper: https://www.semanticscholar.org/paper/b3099f033cfc9b441e3bea5856b8a3ca17996fb8

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Citations in the corpus

Engineered nanomaterials suppress Turnip mosaic virus infection in tobacco (Nicotiana benthamiana) (2018, background): “Both GA and JA are also primary 123 hormones against plant pathogens (Spoel et al., 2007; Navarro et al., 2008).”
Sequence of arrival determines plant‐mediated interactions between herbivores (2011, background): “…interactions between herbivores: The plant’s salicylic acid (SA) response for example down regulates jasmonic acid (JA) dependent defense genes (Spoel et al. , 2007), which may explain the interference of whiteflies with induced resistance (Zarate et al. , 2007) and bacterial colonization…”
Role of plant hormones in plant defence responses (2009, background): “Arabidopsis npr1 plants are compromised in the SA-mediated suppression of JA responsive gene expression indicating that NPR1 plays an important role in SA-JA interaction ( Spoel et al. 2007 ).”
Abiotic and Biotic Stress Response Crosstalk in Plants (2011, background): “tomato treated with SA show compromised resistance to necrotrophic pathogen Alternaria brassicicola, which is sensitive to JA-dependent defenses (Spoel et al., 2007).”
Endophytic fungi promote plant growth and mitigate the adverse effects of stem rot: an example of Penicillium citrinum and Aspergillus terreus (2015, background): “In anti-pathogen defense, crosstalk always occurs between SA and JA (Spoel et al. 2007).”
Hormonal modulation of plant immunity. (2012, background): “For example, induction of the SA pathway by avirulent P. syringae suppressed JA signaling and rendered infected Arabidopsis leaves more susceptible to the necrotrophic fungus Alternaria brassicicola (Spoel et al. 2007).”
Costs and benefits of induced resistance to herbivores and pathogens in plants (2010, background): “syringae, which induces SA-mediated defence, suppressed the JA signalling pathway and consequently rendered Arabidopsis plants more susceptible to the necrotrophic pathogen Alternaria brassicicola [274].”
Growth-defense tradeoffs in plants: a balancing act to optimize fitness. (2014, positive): “For example, elevated SA signaling in response to biotrophic pathogens is often correlated with reduced JA signaling and decreased resistance to necrotrophic pathogens (Spoel et al., 2007).”
Networking by small-molecule hormones in plant immunity. (2009, background): “syringae similarly suppressed JA signaling and rendered infected leaves more susceptible to the necrotrophic fungus Alternaria brassicicola”
Comprehending crystalline β-carotene accumulation by comparing engineered cell models and the natural carotenoid-rich system of citrus (2011, neutral): “SA is an essential signalling molecule that induces SAR and is implicated in resistance to biotrophic pathogens (Spoel et al., 2007; Spoel and Dong, 2008; Leon-Reyes et al., 2009).”
Ecological costs of biotrophic versus necrotrophic pathogen resistance, the hypersensitive response and signal transduction (2008, neutral): “One study found that infection with a virulent biotrophic bacterium led to increased necrotroph virulence if the necrotroph was inoculated 24 h later at a separate site on the same leaf [35].”
Plant Defense Signaling and Responses Against Necrotrophic Fungal Pathogens (2016, neutral): “Even though there are exceptions, mostly pathogens with a hemibiotrophic lifestyle are more sensitive to the SA signalinginduced response, whereas necrotrophic pathogens and herbivorous insects are resisted through JA-mediated defenses (Spoel and others 2007).”
Salicylic Acid, a multifaceted hormone to combat disease. (2009, background): “syringae, but not by preinfection with avirulent strains of the same pathogen that induce a faster, stronger SA response accompanied by an HR (186, 187).”
Systemic acquired resistance: turning local infection into global defense. (2013, neutral): “(123) found that strong crosstalk does not occur in systemic tissue.”
Abiotic Stress Response in Plants - Physiological, Biochemical and Genetic Perspectives (2011, background): “Plants inoculated with virulent strains of Pseudomonas syringae pv. tomato treated with SA show compromised resistance to necrotrophic pathogen Alternaria brassicicola, which is sensitive to JA-dependent defenses (Spoel et al., 2007).”