Plasma Membrane-Cell Wall Adhesion Is Required for Expression of Plant Defense Responses during Fungal Penetration

Abstract

Fungal pathogens almost invariably trigger cell wall-associated defense responses, such as extracellular hydrogen peroxide generation and callose deposition, when they attempt to penetrate either resistant or susceptible plant cells. In the current study, we provide evidence that the expression of these defenses is dependent on adhesion between the plant cell wall and the plasma membrane. Peptides containing an Arg-Gly-Asp (RGD) motif, which interfered with plasma membrane-cell wall adhesion as shown by the loss of the thin plasma membrane-cell wall connections known as Hechtian strands, reduced the expression of cell wall-associated defense responses during the penetration of nonhost plants by biotrophic fungal pathogens. This reduction was associated with increased fungal penetration efficiency. Neither of these effects was seen after treatment with similar peptides lacking the RGD motif. Disruption of plant microfilaments had no effect on Hechtian strands but mimicked the effect of RGD peptides on wall defenses, suggesting that the expression of cell wall-associated defenses involves communication between the plant cell wall and the cytosol across the plasma membrane. To visualize the state of the plasma membrane-cell wall interaction during fungal penetration, we observed living cells during sucrose-induced plasmolysis. In interactions that were characterized by the early expression of cell wall-associated defenses, there was no change, or an increase, in plasma membrane-cell wall adhesion under the penetration point as the fungus grew through the plant cell wall. In contrast, for rust fungus interactions with host plants, there was a strong correlation between a lack of cell wall-associated defenses and a localized decrease in plasma membrane-cell wall adhesion under the penetration point. Abolition of this localized decreased adhesion by previous inoculation with a fungus that increased plasma membrane-cell wall adhesion resulted in reduced penetration by the rust fungus and induction of cell wall-associated defenses. These results suggest that rust fungi may induce a decrease in plasma membrane-cell wall adhesion as a means of disrupting the expression of nonspecific defense responses during penetration of host cells.

Knocking on the heaven’s wall: pathogenesis of and resistance to biotrophic fungi at the cell wall

“…In fact, the cowpea rust fungus Uromyces vignae elicits essentially no wall-associated defence upon invasion of its host Vigna unguiculata, whereas challenge by the same fungus on nonhost pea plants results in typical CWA formation [49 ]. The lack of wall-associated defence responses in compatible interactions with rust fungi is thought to involve an active suppression mechanism that is linked to a disruption of cell wall-plasma membrane connectivity (as indicated by a reduction in the frequency of Hecht threads beneath attempted penetration sites) [49 ]. Hecht threads are known to bridge the paramural space by physically connecting (unknown) sites in the cell wall and the plasma membrane [50].…”

High affinity recognition of a Phytophthora protein by Arabidopsis via an RGD motif

“…Such recognition is a general strategy that allows microorganisms to modulate infectivity and to regulate toxicity towards host cells [5]. Recent observations report that RGD peptides interfere with the activation of plant defence responses [13][14][15]. Thus, RGD recognition through plant proteins may occur and RGD-containing proteins from phytopathogenic microorganisms may act as pathogenicity factors.…”

“…The importance of plasma membrane-cell wall adhesions during pathogen penetration was highlighted by the study of Mellersh and Heath [15]. When the rust fungus Uromyces vignae attacked its natural host, cowpea, RGD-containing peptides reduced the expression of cell wall-associated defence responses during fungal penetration.…”

“…Integrins are also chosen by pathogens as targets for binding, and the RGD motif is present in surface proteins of several pathogens that attach to mammalian cells [5]. In plants, synthetic peptides containing the RGD motif can disrupt the adhesion between plasma membrane and cell wall [6][7] and can interfere with physiological processes thereby affecting, e.g., development [8][9][10][11], mechano-perception [12] and the interaction with microorganisms [13][14][15]. In particular, expression of cell wall associated defence responses triggered by fungal pathogens is dependent on adhesion between the plasma membrane and the plant cell wall [15].…”

“…In plants, synthetic peptides containing the RGD motif can disrupt the adhesion between plasma membrane and cell wall [6][7] and can interfere with physiological processes thereby affecting, e.g., development [8][9][10][11], mechano-perception [12] and the interaction with microorganisms [13][14][15]. In particular, expression of cell wall associated defence responses triggered by fungal pathogens is dependent on adhesion between the plasma membrane and the plant cell wall [15]. The fact that these adhesions can be disrupted by RGD containing peptides suggests similarities between plant cell wall-plasma membrane interactions, and mammalian ECM-membranecytoskeleton continuum [16].…”