Plant-microbe interactions in the apoplast: Communication at the plant cell wall

Abstract

The apoplast is a continuous plant compartment that connects cells between tissues and organs and is one of the first sites of interaction between plants and microbes. The plant cell wall occupies most of the apoplast and is composed of polysaccharides and associated proteins and ions. This dynamic part of the cell constitutes an essential physical barrier and a source of nutrients for the microbe. At the same time, the plant cell wall serves important functions in the interkingdom detection, recognition, and response to other organisms. Thus, both plant and microbe modify the plant cell wall and its environment in versatile ways to benefit from the interaction. We discuss here crucial processes occurring at the plant cell wall during the contact and communication between microbe and plant. Finally, we argue that these local and dynamic changes need to be considered to fully understand plant-microbe interactions.

Figure 1

A structural model of the primary CW. Based on atomic force microscopic images of onion epidermal CWs (Cosgrove, 2014): cellulose microfibrils (blue fibrils) are shown embedded in a matrix of pectins (yellow chains), hemicellulose (green chains), arabinogalactan proteins (linear protein backbones are shown in pink with glycosylated hydroxyproline residues in orange), and other plant CW proteins (pink). Limited areas, called biomechanical hotspots (red shadows), are thought to contribute to CW mechanics disproportionately, and likely include sites of contact between cellulose and other molecules. The cellulose microfibrils are synthesized at the plasma membrane by cellulose synthase complexes tracking along microtubules, while the other polysaccharides are synthesized in the Golgi and assembled at the apoplast. A, Xylan is shown binding to the hydrophilic face of cellulose microfibrils via hydrogen bonding, in the same conformation as the glucan chains within cellulose. B, Xyloglucan binds to the hydrophobic face of cellulose based on molecular dynamics simulations, though details of this interaction require further investigation. This interaction is modified by EXP and XTH/XETs. EXPs are nonhydrolytic proteins that cause CW loosening through an unknown mechanism, most probably by separating hemicelluloses and cellulose that are interacting. An XTH has transglycosylated a xyloglucan chain onto a glucan chain of cellulose, forming a new covalent bond, highlighted in red. XTHs can also make xyloglucan–xyloglucan links, or hydrolyse xyloglucan, also (data not shown). C, HG is demethylated by PMEs that are inhibited by PMEIs, regulating the methylation status of the pectin. PME-demethylated regions of HG bind Ca²⁺ (fuchsia circles), forming dimerized egg-box structures, either intra- or intermolecularly. Ca²⁺-bound pectin seems to associate with cellulose, though the details of this interaction are not well understood. The size of demethylated HG is reduced by the cleavage of pectate and PLs and PGs. D, The glucuronic acid residues of arabinogalactan proteins can bind Ca²⁺, and this may enable dimerization.

Figure 2

Modification of the plant CW environment upon microbial colonization. The polysaccharides of the primary CW represented in Figure 1 have been loosened and degraded by microbial CWDE and CW-modifying enzymes (red), and the CW ionic environment has been modified (A–E). The plant responds by synthesizing new CW material (F–G). For elements present in Figure 1, refer to its key. A, Plant CW polysaccharides become digested upon microbial enzymatic activities. Some of the resulting oligosaccharide fragments are detected as DAMPs by plasma membrane localized receptors that induce signaling cascades leading to defense reactions. Shown are confirmed DAMPs, such as cellobiose and OGs, and potential DAMPs, such as xyloglucan- and xylan-polysaccharides. B, Microbial xyloglucanases (GH12) and EXP cut the xyloglucan and loosen the Figure 2 (Continued) xyloglucan–cellulose interactions, respectively. This may reduce cross-linking between microfibrils enabling separation/sliding of the cellulose microfibrils, which could be important for CW loosening. Other hemicelluloses are targeted by CWDEs from different CaZY families, not shown. C, Microbial PMEs remove methyl groups from HG, while pectate and PLs and PGs cut this polymer into smaller fragments. At low pH, or potentially small HG size, the HG loses the ability to bind Ca²⁺ ions, possibly reducing the interaction between HG and cellulose. D, Apoplast acidification through hyperactivation of the plant plasma membrane proton ATPases (AHAs) in response to F. oxysporum contact, leads to the depletion of cellulose synthase complexes from the plasma membrane and cortical microtubule depolymerization. This leads to a halt in cellulose synthesis and, may be a general response to pathogen infection, though has, thus far, only been observed in F. oxysporum. E, A drop in apoplastic pH leads to a release of Ca²⁺ ions from arabinogalactan proteins and HG, which could contribute importantly to the cytosolic Ca²⁺ peak detected in response to microbes. The liberated Ca²⁺ can be sequestered by bacterial extracellular polysaccharides, affecting the Ca²⁺ dynamics that are important for activating plant immunity. F, In response to some microbial attacks, the plant cell forms a papillae composed of cellulose, callose (purple chains), PRs, and secondary metabolites with antimicrobial properties. The papillae polysaccharides interact in unknown ways, though calllose modifies the extensibility of cellulose gels in vitro. G, The plant cell reinforces its CW by lignification (light brown chains) through the activity of PRXs and LACs. PRXs binding to demethylated HG, which might help localize lignin formation at sites of CW damage. Some microbes get trapped in the newly formed lignin-network. Microbes can scavenge ROS through their extracellular polymeric substances. Many of the models shown are speculative, based on research in related contexts (C, D, F, and G) or the known activities of well-described enzymes (E and F).