Plant immunity: the EDS1 regulatory node
Introduction
Individual plant cells perceive an enormous range of external cues. Plant survival depends on integrating this information and responding appropriately in terms of metabolism, growth and defense. In the natural environment (and indeed the cleanest growth chamber!) plants are rarely able to grow without attempted pathogen colonization and have evolved an elaborate, multi-layered system of innate immunity. Unraveling these layers and comprehending how the most aggressive pathogens overcome or subvert defenses to cause disease is of major interest. Some of the most effective barriers to disease are expressed at the plant cell wall and plasma membrane, preventing pathogen penetration and accounting for the majority of aborted infections in non-host (species-level) resistance. Necrotrophs commonly take advantage of wound sites or dead cells to invade. By contrast, biotrophic and hemi-biotrophic pathogens have evolved specialized structures and effector molecules that allow invasive growth on particular host genotypes and, in the case of obligate biotrophs, limit the disruption of host cell integrity.
The contrasting modes of infection of necrotrophs at one extreme and obligate biotrophs at the other require ingenuity in plant defense signaling. What emerges from genetic analyses, mainly of Arabidopsis, is a complex circuitry that balances the activation of various basal defenses. Pathways involving the hormones jasmonic acid (JA), JA-related oxygenated lipids and ethylene (ET) are principally effective against necrotrophic pathogens and chewing insects, whereas those involving salicylic acid (SA) are effective against biotrophs [1]. The expression of basal resistance to invasive pathogens is a crucial protective layer. Without it, plants become super-susceptible to even mild infections and are less likely to survive in a competitive environment. A large catalogue of Arabidopsis mutants that are compromised in basal defenses to virulent pathogens points to the involvement of many genes in maintaining this resistance layer and to the existence of numerous potential targets that the pathogen might disable to promote disease [2]. A further layer of resistance to invading pathogens is mediated by Resistance (R) genes that encode proteins that recognize the presence of specific pathogen effector molecules. Recognition triggers dramatic cellular reprogramming that stops pathogen growth, and often involves a localized burst of reactive oxygen intermediates (ROI) and strictly delimited programmed plant cell death. The local response also serves to prime uninfected tissues against subsequent attack in a process called systemic acquired resistance [3•]. Several key plant defense regulators have been cloned and characterized. In this review, we discuss ENHANCED DISEASE SUSCEPTIBILITY 1 (EDS1), a positive regulator of basal resistance to invasive biotrophs and hemi-biotrophs that is also indispensable for Toll-Interleukin-1 receptor (TIR)-type nucleotide binding-leucine rich repeat (NB-LRR) protein-triggered resistance. We highlight several recent studies that suggest that EDS1 and its partners are positioned as a pivotal node in signal relay against pathogens and in certain abiotic stress responses.
Section snippets
Positioning EDS1 and its partner PAD4 in the defense signaling network
EDS1 was originally identified in a screen for mutants that are defective in RPP1- and RPP5-specified resistance to isolates of the obligate biotrophic oomycete pathogen Peronospora parasitica [4]. Further inspection of eds1 mutants revealed defects in basal resistance to virulent isolates of P. parasitica and Erysiphe (an obligate biotrophic fungus) and to strains of the bacterial pathogen Pseudomonas syringae (notably P. syringae tomato [Pst] DC3000 and P. syringae maculicola [Psm] ES4326],
EDS1 and redox stress signal relay
Accumulation of evidence of more fundamental activities of EDS1 and PAD4 in transducing redox signals has gathered some momentum. Rustérucci et al. [14] revealed the existence of an ROI- and SA-stimulated propagative loop that requires EDS1 and PAD4 in lsd1-conditioned runaway cell death. Further work by Karpinski and colleagues [24•] shows that lsd1 mutants fail to acclimate to excess excitation energy (EEE) generated by photosynthesis in high light, causing ROI overload and ultimately cell
Additional players in EDS1 defense relay
Arabidopsis EDS1 and PAD4 interact in soluble cell extracts of healthy (pathogen unchallenged) leaves, indicating the presence of a pre-existing EDS1–PAD4 complex, although the co-immunoprecipitable amounts of EDS1 and PAD4 increased upon pathogen challenge [7]. The molecular interactions and biochemical activities of EDS1 and PAD4 need to be defined more precisely. Using an affinity-purification approach coupled to Quadropole-Time-of-flight (Q-TOF) mass spectrometry, an additional EDS1
The lipid link
Various studies have shown that EDS1 and PAD4 do more than simply regulate SA in R-protein-triggered and basal resistance [7, 24•, 38, 39], but the nature of the signals that they transduce and their precise biochemical activities remain unclear. Although EDS1 and PAD4 (and less convincingly, SAG101) have homology to acyl hydrolases, no enzymatic activity has been measured to date for any of these proteins in our assays (S Rietz, J Parker, unpublished). Still, the idea that they could process
Conclusions
The emerging importance of EDS1 as a central regulatory protein in biotic and oxidative stress signaling (Figure 1) prompts us to explore the structures, interaction dynamics and biochemical activities of EDS1 and its partners in more depth. Although the lipase homologies might be a scientific ‘falsche Fährte’ (‘red herring’) in terms of catalytic activity, conservation of these domains in all of the plant EDS1 and PAD4 orthologs examined suggests they are needed, perhaps as structural rather
References and recommended reading
Papers of particular interest, published within the annual period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgements
We thank all colleagues who provided unpublished data for this review. Work in the Parker laboratory is funded by The Max-Planck Society, The Alexander von Humboldt Foundation and grants from The Deutsche Forschungsgemeinschaft and The Bundesministerium für Bildung und Forschung. We thank our colleagues Steffen Rietz and Stefan Malonek for stimulating discussion while writing this review.
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