H₂O₂ plays different roles in determining penetration failure in three diverse plant–fungal interactions

Abstract

Fungal plant pathogens that attempt to penetrate and feed on living cells frequently trigger a localized plant defence response that results in fungal penetration failure. In the current study we demonstrate that breakdown products of the cell wall released by the localized application of hemicellulase elicit localized responses including, sequentially, extracellular H2O2 generation; accumulation of phenolic compounds; and cross-linking of proteins in the cell wall. In a detailed time-course study of three plant-fungus interactions that result in a high frequency of penetration failure, only one plant-fungus combination displayed a similar profile of responses to that induced by localized cell-wall degradation. The additional generation of extracellular O2- in one interaction, and the absence of phenolic compounds in the cell wall in another, demonstrate that plant responses to the penetration process may be influenced by activities of the penetrating fungus. Significantly, H2O2 generation was the only response detected in all three plant-fungal combinations at the correct time and place to account for penetration failure, and in all three combinations the enzymatic removal of H2O2 resulted in increased penetration success. Pharmacological studies suggest that in two of the three interactions, H2O2 generation required cytoskeletal involvement but was independent of transcription or translation, although inhibition of the latter processes increased fungal penetration. In at least one of these two interactions, the data suggest that H2O2 generation and new gene expression act within the same penetration-inhibiting pathway, possibly through the involvement of phenolic materials. However, enzymatic removal of H2O2 from the third interaction almost completely eliminated penetration failure, while interference with cytoplasmic processes had no effect, suggesting that H2O2 generation in this system did not require protoplast involvement and, alone, was necessary and sufficient to account for fungal penetration failure.

Changes of antioxidant enzymes of mung bean [Vigna radiata (L.) R. Wilczek] in response to host and non-host bacterial pathogens

“…It has been showed that an accumulation of ROS plays a central role in a number of non-host interactions like barley/Blumeria graminis f. sp. tritici (Hück-elhoven et al 2001), cowpea/Erysiphe cichoracearum (Mellersh et al 2002); and pepper/Blumeria graminis f. sp. tritici pathosystems (Hao et al 2011).…”

Mitochondrial complex II has a key role in mitochondrial-derived reactive oxygen species influence on plant stress gene regulation and defense

“…mROS may contribute to plant defense by either directly acting against the pathogen or acting as a signaling molecule in plant defenses. For a fungal pathogen like R. solani AG8, which is unable to penetrate the roots of WT plants (16), mROS could contribute to the oxidative cross-linking of the cell wall to help prevent fungal penetration (31,32). Moreover, some evidence suggests that signaling may be the primary role of ROS in R. solani resistance because resistant transgenic cotton seedlings exhibited a rapid induction of ROS and downstream defense-related genes (33).…”

Microdochium nivale (Fr., Samuels & Hallett): cytological analysis of the infection process in triticale (×Triticosecale Wittm.)

“…Beside a direct antimicrobial effect (review by Heath 2002), H 2 O 2 stimulates peroxysomes, activates defence genes, and stimulates numerous modifications of plant cell walls, i.e. oxidative cross-linking of phenolic compounds in the process of lignification (Baker and Orlandi 1995;Hammond-Kossack and Jones 1996;Mellersh et al 2002). As phenolic compound accumulation was detected in our study at the site of pathogenic hyphae penetration, this reaction seems to belong to triticale defense system against M. nivale.…”