Plant cell wall dynamics and wall-related susceptibility in plant-pathogen interactions

Abstract

The cell wall is a dynamic structure that often determines the outcome of the interactions between plants and pathogens. It is a barrier that pathogens need to breach to colonize the plant tissue. While fungal necrotrophs extensively destroy the integrity of the cell wall through the combined action of degrading enzymes, biotrophic fungi require a more localized and controlled degradation of the cell wall in order to keep the host cells alive and utilize their feeding structures. Also bacteria and nematodes need to degrade the plant cell wall at a certain stage of their infection process, to obtain nutrients for their growth. Plants have developed a system for sensing pathogens and monitoring the cell wall integrity, upon which they activate defense responses that lead to a dynamic cell wall remodeling required to prevent the disease. Pathogens, on the other hand, may exploit the host cell wall metabolism to support the infection. We review here the strategies utilized by both plants and pathogens to prevail in the cell wall battleground.

Keywords: cell wall; cell wall integrity; host cell wall metabolism reprogramming; plant defense; susceptibility factors.

FIGURE 1

Cell wall dynamics during necrotrophs invasion. (A) Necrotrophic fungi secrete a large arsenal of cell wall degrading enzymes (CWDEs) like PGs, hemicellulases and cellulases, assisted by PMEs and AEs in the apoplastic space to degrade cell wall polymers and facilitate the availability of nutrients. PGs and EIXs have been proposed to function as PAMPs recognized by the membrane receptors RBPG1 and Eix1 or 2, respectively. (B) As first line of defense, plants produce a variety of CWDE inhibitors to hinder degradation by microbial CWDEs. For instance, the inhibition of PG degrading activity by PGIPs induces the accumulation of elicitor-active pectin fragments (OGs) perceived by WAK1 receptors. It cannot be excluded the presence of other not yet identified receptors sensing damage of other cell wall components. The perception of cell wall damage triggers specific signaling pathways activating defense responces aimed to reinforce cell wall structure. The more evident defense strategies are callose and lignin deposition, induction of peroxidases/ROS-mediated crosslinks between cell wall structural proteins and polysaccharides. (C) Necrotrophs force plants to cooperate in disease exploiting plant cellulases, expansins, PGs and PMEs as susceptibility factors. PM, plasma membrane; CW, cell wall; Cyt, cytoplasm; OGs, oligogalacturonides; WAK1, wall associated kinase 1; AEs, acetyl esterases; PGs, polygalacturonases; EIXs, ethylen induced xylanases; PME, pectin methylesterases; PMEI, pectin methylesterase inhibitor; FA, ferulic acid; Eix1-2, receptors of ethylene induced xylanases; RBPG1, Responsiveness to Botrytis PolyGalacturonase 1; Ca²⁺, calcium ions; XI, xylanase inhibitor; PRR, pattern recognition receptor; POX, peroxidase; ROS, reactive oxygen species.

FIGURE 2

Cell wall dynamics in plant-biotrophic fungi interaction. (A) Biotrophic fungi use appressorial mechanical pressure and secrete cell wall degrading enzymes to penetrate plant cell wall. (B) Plants perceive fungal biotrophs penetration with not yet identified receptors and respond with “papillae” apposition between cell wall and plasma membrane. Papillae, in addition to new cell wall material are also sites of accumulation of ROS possibly involved in cell wall reinforcement. (C) At a later stage of infection, fungus forms the haustorium feeding organ invaginated into the host membranes and plant cell wall. Biotrophs locally affect cell wall metabolism by induction of susceptibility factors (callose synthase PMR4, O-acetyltransferase PMR5 and pectate lyase PMR6) to modify the extrahaustorial matrix to improve the accessibility of nutrients or to ensure the mechanical stability of the haustorium. PM, plasma membrane; CW, cell wall; Cyt, cytoplasm; PG, polygalacturonase; PME, pectin methylesterase; PRR, pattern recognition receptor; POX, peroxidase; ROS, reactive oxygen species.