Balanced Nuclear and Cytoplasmic Activities of EDS1 Are Required for a Complete Plant Innate Immune Response

Abstract

An important layer of plant innate immunity to host-adapted pathogens is conferred by intracellular nucleotide-binding/oligomerization domain-leucine rich repeat (NB-LRR) receptors recognizing specific microbial effectors. Signaling from activated receptors of the TIR (Toll/Interleukin-1 Receptor)-NB-LRR class converges on the nucleo-cytoplasmic immune regulator EDS1 (Enhanced Disease Susceptibility1). In this report we show that a receptor-stimulated increase in accumulation of nuclear EDS1 precedes or coincides with the EDS1-dependent induction and repression of defense-related genes. EDS1 is capable of nuclear transport receptor-mediated shuttling between the cytoplasm and nucleus. By enhancing EDS1 export from inside nuclei (through attachment of an additional nuclear export sequence (NES)) or conditionally releasing EDS1 to the nucleus (by fusion to a glucocorticoid receptor (GR)) in transgenic Arabidopsis we establish that the EDS1 nuclear pool is essential for resistance to biotrophic and hemi-biotrophic pathogens and for transcriptional reprogramming. Evidence points to post-transcriptional processes regulating receptor-triggered accumulation of EDS1 in nuclei. Changes in nuclear EDS1 levels become equilibrated with the cytoplasmic EDS1 pool and cytoplasmic EDS1 is needed for complete resistance and restriction of host cell death at infection sites. We propose that coordinated nuclear and cytoplasmic activities of EDS1 enable the plant to mount an appropriately balanced immune response to pathogen attack.

Author Summary

Plants have evolved a multilayered innate immune system to recognize and respond to potentially destructive microbes in the environment. Resistance to invasive biotrophic and hemi-biotrophic pathogens often involves transcriptional mobilization of defenses and programmed death of host cells at infection sites. However, these processes disturb normal metabolism and growth and therefore have to be tightly controlled. In this study, we examine resistance signaling events inside Arabidopsis cells after pathogen activation of intracellular immune receptors. We show that the nucleo-cytoplasmic protein EDS1 acts as an important regulator of transcriptional reprogramming in the immune response by allowing the induction and repression of particular defense-related genes. We provide evidence that EDS1 accomplishes its role as a defense signaling ‘hub’ through coordinated activities in the cytoplasm and nucleus. Maintaining a balance between these two EDS1 pools is probably important for resistance and cell death to a range of infectious microbes and to not ‘overshoot’ defense activation which would be detrimental for the plant.