Host–pathogen warfare at the plant cell wall
Introduction
The plant cell wall is an exoskeleton surrounding the cell protoplast, and is composed of a highly integrated and structurally complex network of polysaccharides, including cellulose, hemicelluloses and pectin (for comprehensive reviews of the cell wall structure see [1]). In brief, cell wall synthesis begins when a pectin rich middle lamella is deposited at the cell plate during cytokinesis. Then, the primary cell wall is synthesized and remodelled following cell growth. Finally, a thicker secondary cell wall is deposited once the cell has reached its final size. Growth and cell shape are largely determined by the balance between expansion driven by turgor and constraint provided by the plant cell wall. The cell wall is also a highly dynamic structure that is constantly remodelled during growth and development and in response to environmental cues. For example, upon pathogen attack, plants often deposit callose rich cell wall appositions (i.e. papillae) at sites of attempted pathogen penetration, accumulate phenolic compounds and various toxins in the wall and synthesize lignin-like polymers to reinforce the wall [2•]. Thus, much like the ramparts or fortress walls of ancient cities, the plant cell wall can be an important defensive structure that many pathogens encounter first before confronting intracellular plant defences [3, 4]. Pathogens use mechanical force or release cell wall degrading enzymes to break down this barrier. At the cell wall, they also release pathogen-associated molecular patterns (PAMPs) either inadvertently or as a consequence of plant degradative enzymes (e.g. the release of chitin oligomers by plant chitinases). Plants, in turn, appear to sense these PAMPs and damage to their cell walls and activate a variety of defences, including the production of reactive oxygen species (ROS), the production and export of anti-microbial compounds and fortification of their cell walls. In addition, sensing PAMPs may activate intracellular defences like the salicylic acid pathway, perhaps priming the plant for the next stage of warfare.
In this commentary, we suggest that in addition to its structural role, the plant cell wall also relays information about the environment to the cell cytoplasm via signal transduction pathway(s) that are patterned after PAMP signalling pathways. In the case of microbe attack, cell wall fragments generated by either the plant or the microbe activate plant defences, reinforcing the protection provided by plant cell wall. Experimental results supporting this model are discussed in detail below. Roles for the plant cuticle in defence are not addressed in this article.
Section snippets
Pathogens use different invasion strategies but similar weapons.
There are a variety of pathogen lifestyles from biotrophs to necrotrophs, which influence the kinds of interactions that occur at the plant cell wall. Necrotrophs release copious amounts of cell wall degrading enzymes, presumably in an attempt to lyse plant cells before they can mount an effective defence. Biotrophs, however, appear to operate by stealth, minimizing damage to the host cell wall. This difference in lifestyle is partially reflected in the repertoire of cell wall degrading enzymes
Plant surveillance of pathogen invasion: elicitors inform about enemies
Plants possess different mechanisms to detect pathogen invasion. They can directly detect pathogen presence by non-self recognition of PAMPs or they can monitor the integrity of their own cell wall (i.e. ‘intact self’ or ‘degraded self’). The cellular responses to PAMPs such as flg22 or chitin and cell wall perturbation are very similar (e.g. induction of ROS, overproduction of callose and lignin). Thus, PAMP signalling can be used to study the less characterized cell wall integrity signalling.
Plasma membrane-anchored receptors: the embrasures of the fortress battlements
One can assume that perception of plant cell wall damage involves plasma membrane-anchored proteins, like the RLK (Figure 2). These RLKs may sense damage to the plant cell wall directly via their extracellular domain or may interact with a cell wall based receptor to form a complex.
Wall-associated kinases (WAK) were the first cell wall binding receptor kinases to be described [39]. WAK1 possesses an extracellular domain containing an epidermal growth factor (EGF)-like motif and appears to be
Signalling pathways
As noted above, cell wall damage is sensed by plants and leads to the activation of various kinds of signalling pathways. Deficiencies in cellulose, whether found in mutants or in plants treated with cellulose synthesis inhibitors, lead to the activation of the ET and JA signalling pathways [10, 11, 12••], and in some cases, to the activation of the SA or ABA pathways [12••, 13•]. A deficiency in wound and pathogen-induced callose deposition is associated with hyper-activation of the SA
Conclusions
The induction of defence-related pathways by plant cell wall damage or change supports the role of the cell wall as not only a physical barrier but also as an important sensory component for downstream signalling pathways. As the cell wall is an important barrier or shield for plant cells, monitoring its integrity allows plants to quickly activate pathways to minimize pathogen entry and reduce the spread of disease. Although a number of plant responses to cell wall damage have been described, a
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgments
We thank Bill Underwood, Shundai Li and Ying Gu for their critical reading and suggestions on this manuscript. Financial support was provided partly by the National Science Foundation (0519898) and the Carnegie Institute of Science. C.C. was supported partly by graduate student funding from the University of California at Berkeley.
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