The plant endoplasmic reticulum is both receptive and responsive to pathogen effectors

Abstract

15The endoplasmic reticulum (ER) is the entry point to the secretory pathway and, as such, is 16 critical for adaptive responses to biotic stress, when the demand for de novo synthesis of 17 immunity-related proteins and signalling components increases significantly. Comprised of a 18 network of interconnected tubules and cisternae, the architecture of the ER is highly 19 pleomorphic and dynamic, rapidly remodelling to meet new cellular requirements. During 20 infection with the hemi-biotrophic phytopathogen, Pseudomonas syringae pv. tomato 21 DC3000, the ER in cells immediately adjacent to established bacterial colonies condenses 22 into 'knot-like' structures, reminiscent of fenestrated sheets. Based on known temporal 23 dynamics of pathogen effector delivery and initial bacterial multiplication, the timing of these 24 observed morphological changes is rapid and independent of classical elicitor activation of 25 pathogen-triggered immunity. To further investigate a role for ER reconfiguration in 26 suppression of plant immunity we identified a conserved C-terminal tail-anchor domain in a 27 set of pathogen effectors known to localize to the ER and used this protein topology in an in 28 silico screen to identify putative ER-localised effectors within the effectorome of the oomycete 29 Phytophthora infestans. Subsequent characterization of a subset of 15 candidate tail-30 anchored P. infestans effectors revealed that 11 localised to the ER and/or Golgi. Notably, 31 transient expression of an ER-localised effector from the closely related oomycete, 32 Plasmopara halstedii, reconfigured the ER network, revealing intimate association of labelled 33 ER with perinuclear chloroplasts and clusters of chloroplasts, potentially facilitating retrograde 34 signalling during plant defence. 37As the gateway to the cell's secretory pathway, the endoplasmic reticulum (ER) provides the 38 environment for secretory protein production, folding and quality control. The ER is a highly 39 dynamic, interconnected network of tubules and cisternae (sheets) that extends throughout 40 the cytoplasm, associating with the plasma membrane and other organelles, and adjacent 41 cells via plasmodesmata (Hawes et al., 2015). Hence, the ER is central to the maintenance of 42 cellular homeostasis and can facilitate intra-and intercellular communication.

Potato virus X-mediated constitutive expression of Plutella xylostella PxSDF2L1 gene in Nicotiana benthamiana confers resistance to Phytophthora parasitica var. nicotianae

“…The A. thaliana ethylene-responsive factor 19 gene (AtERF019) mediates plant susceptibility to P. parasitica through suppression of PTI [28]. P. parasitica have developed strategies to suppress PTI through ER-localised effectors during the biotrophic relationship [21]. Transcriptomic analysis of N. tabacum's molecular response to P. parasitica found defence to oomycetes and other essential plant defence mechanisms were suppressed during the interaction [29].…”

“…An effector protein PpRxLR2 has been found to suppress N. benthamiana immunity by targeting a yet unknown plant susceptibility gene [20]. While Breeze et al [21] have shown ER to be an essential target of RxLR-type effectors, which induce a rapid reconfiguration of the organelle coincidently with the suppression of host defences and initial pathogen multiplication.…”

Endomembrane-Targeting Plasmodiophora brassicae Effectors Modulate PAMP Triggered Immune Responses in Plants

“…The interconnected tubular network of the ER can extend throughout the cytoplasm from early endosome to PM, to cell-to-cell junctions, facilitating communication and the regulation of adaptive biotic stress responses. Due to both the receptive and the responsive nature of the ER ( Breeze et al, 2020 ), it is a common subcellular target of pathogen effectors to manipulate host immunity and to hijack the secretory pathway to enable completion of the pathogen life cycle ( McLellan et al, 2013 ; Jing et al, 2016 ; Fan et al, 2018 ; Meisrimler et al, 2019 ; Tsai et al, 2019 ). In oomycetes up to 17% of the effector secretome targets ER localized host proteins, e.g., ER-localized NAC transcription factors and ER luminal binding immunoglobulin proteins (BiPs; Khan et al, 2018a ).…”

The Passage of H2O2 from Chloroplasts to Their Associated Nucleus during Retrograde Signalling: Reflections on the Role of the Nuclear Envelope

“…Stromules may also facilitate the clustering of chloroplasts with the nucleus since they have been shown to move along microtubules and anchored by actin filaments [32]. In addition, pathogen-derived effectors may also achieve the same end without stromules by promoting peri-nuclear clustering of chloroplasts [17,35].…”

“…The outer membrane of the nuclear envelope is continuous with the endoplasmic reticulum membrane (ER; Figure 1) [35] and consequently, the ca. 50 nm wide perinuclear space between the inner and outer nuclear membrane is contiguous with the ER lumen [36].…”