Plant endomembranes and cytoskeleton: moving targets in immunity

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Pathogens attack plant cells to divert resources toward pathogen proliferation. To resist pathogens, plant cells rely on multilayered signaling pathways that hinge upon the secretory pathway for the synthesis and trafficking of pathogen sensors and defense molecules. In recent years, significant strides have been made in the understanding of the functional relationship between pathogen response and membrane traffic. Here we discuss how the plant cytoskeleton and endomembranes are targeted by pathogen effectors and highlight an emerging role of membrane contact sites in biotic stress responses.

Introduction

Balancing resource allocation to either growth or defense against pathogens is a challenge that plants face on a regular basis. Upon pathogen perception, plant endomembranes and the associated cytoskeleton components that are normally engaged in growth under unstressed conditions need to be massively redeployed to counteract pathogen attack. The endomembrane system is composed of organelles with unique microenvironments (e.g. pH, enzymes, functions) [1]. These are essential for the production, sorting, and transport of a large part of the cellular proteome as well as of proteins anchored to the cell surface and present in the apoplast, such as membrane-anchored receptors and antimicrobial proteins, respectively (e.g. PATHOGENESIS-RELATED 1 (PR1)) [2,3]. The plant endomembranes are closely associated with the cytoskeleton, a dynamic protein network that undergoes continuous remodeling, enabling traffic of biosynthetic cargo, cell development, and deployment of defense molecules [4]. The plant cytoskeleton comprises actin and microtubules (MT) and acts as a propelling mesh for a timely and directional movement of endomembranes and other organelles within the cell [5,6]. A close association of actin with endomembrane organelles, such as the endoplasmic reticulum (ER), Golgi apparatus and plasma membrane (PM), has been documented [7], and an engagement of MT in secretory organelle biogenesis, positioning, and movement is emerging in plants [8••,9,10].

Beyond physical barriers such as the cuticle and a cellulosic cell wall that act as a biological shield, plant innate immunity is understood to operate on a neatly arranged two-tier system [11]. The first tier, known as Pattern-Triggered Immunity (PTI), is initiated and actuated upon activation of PM-localized Pattern-Recognition Receptors (PRRs), which detect conserved microbial patterns, such as bacterial flagellin or peptido-glycans (Figure 1). Certain pathogens overcome PTI by secreting proteinaceous virulence factors (effectors) into the apoplast or cytoplasm (Figure 1). Pseudomonas syringae (Pst), a bacterial pathogen, uses a needle-like structure called the type III secretion system to deliver effectors into host cell, while fungi use specialized infection structures known as haustoria [12]. Once inside the cell, pathogen effectors target various cellular components and processes, including transcription factors, cytoskeleton, hormonal pathways, and protein trafficking [13]. Recognition of effectors by intracellular immune receptors, which largely belong to the nucleotide binding leucine-rich repeat (NLR) class, results in the activation of the second tier of immunity, known as Effector-Triggered Immunity (ETI) (Figure 1) [11]. PTI and ETI employ overlapping signaling components and defense gene expression, with ETI being characterized by quick and sustained transcriptional reprogramming and, in some cases, by localized cell death [14,15,16].

The plant immune system has to be ready to respond appropriately upon receptor-mediated activation of PTI, ETI, or possibly both, and defuse a false alarm. Sophisticated alarm systems are in place to ensure that PRR-mediated signaling is not perpetually active [17]. During plant–pathogen coevolution, pathogens have adopted multiple strategies to evade detection and maintain a virulent advantage, as supported by the evidence that pathogen effectors target diverse host proteins and organelles [13,18]. The importance of trafficking during immunity supports that the endomembranes and cytoskeleton are obvious targets for pathogen effectors. In this review we highlight recent insights on the role of endomembranes and cytoskeleton in immunity and how these are targeted by pathogens drawing largely from the well-studied model plant–pathogen system Arabidopsis thaliana and Pst.

Section snippets

Plasma membrane: at the plant–microbe interface

The PM acts as a barrier between phytopathogens and the host cell machinery (e.g. endomembranes, cytoskeleton). The PM is also home to integral membrane PRRs that can be internalized by endocytosis [19]. During immunity, the internalization of activated signaling complexes at the PM relies on receptor-mediated endocytosis, and clathrin-mediated endocytosis plays a major role in the internalization of receptors, including FLAGELLIN SENSING 2 (FLS2), ELONGATION FACTOR-TU (EFR) and PEP RECEPTOR 1

Endomembrane trafficking in biotic stress

The endomembrane system plays a key role in transporting proteins and anti-bacterial compounds during pathogen attack. Pathogens target these trafficking components to subvert immunity and hijack the trafficking pathways to their advantage (Figure 2). The Pst effectors HopM1 and AvrE help establish an aqueous environment in the apoplast to enhance Pst growth [25]. HopM1 interacts with the TGN/EE-localized ADP-RIBOSYLATION FACTOR-GUANINE NUCLEOTIDE EXCHANGE FACTOR (ARF-GEF), HopM1 INTERACTOR 7

Plant cytoskeleton: highways of defense

Actin and MT are targeted by different pathogen effectors [13,37,38] (Table 1). A role of actin in plant immunity is underscored by the evidence that activation of PTI leads to increased accumulation of actin at the site of infection [5]. Furthermore, ACTIN DEPOLYMERIZING FACTOR (ADF) proteins, which are important for actin turnover, also play diverse roles in immunity. For example, ADF4 is required for RESISTANCE TO PSEUDOMONAS SYRINGAE 5 (RPS5)-mediated ETI against the Pst effector AvrPphB [39

Extracellular vesicles

Extracellular vesicles (EV), small, membrane-enclosed structures akin to multi-vesicular bodies that are released from a cell into the surrounding environment, are new emerging players in the battle between plants and pathogens. Although the biogenesis and transport mechanisms of EV are not yet known, a co-localization of late endosomes and EV at the site of EV secretion and the presence of compounds of different origin in EV suggest that they pass through or encounter, multiple trafficking

Membrane contact sites

In highly vacuolated plant cells, the cytoplasm and all the other organelles are sandwiched at the cell cortex between the tonoplast and the PM. In this crowded environment, organelles contact each other at membrane contact sites (MCS) [54,55]. Although the membranes of contacting organelles do not fuse, studies on yeast MCS have revealed critical roles in membrane dynamics, lipid transport between membranes, and endosomal cargo sorting [54]. Lipids and fatty acids, and their metabolic

Conclusions

Contributions from different research avenues such as genomics, proteomics, and cell biology have broadened our understanding of the myriad interactions, such as gene regulation, protein production and transport, and host virulence targets, during an immune response. A major tipping point in the past decade has been the appreciation of finer spatio-temporal aspects of immunity that have led to building of newer models upon the classic ‘zig-zag model’ [11], such as the ‘invasion model’ which

Conflict of interest statement

Nothing declared.

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

We apologize to those colleagues whose work was not cited due to manuscript length restrictions. This work was funded primarily by the Michigan State University Foundation with contributing support of the DOE Great Lakes Bioenergy Research Center (DOE BER Office of Science DE-FC02-07ER64494 and DE-SC0018409), the Chemical Sciences, Geosciences and Biosciences Division, Office of Basic Energy Sciences, Office of Science, US Department of Energy (award number DE-FG02-91ER20021), National Science

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