Cellular interactions between biotrophic fungal pathogens and host or nonhost plants

Abstract

Biotrophic fungi, such as the rust fungi and the powdery mildew fungi, represent a distinct and economically important group of plant pathogens. Studies of nonhost interactions with Uromyces vignae (cowpea rust fungus, monokaryotic stage) or Erysiphe cichoracearum (plantain powdery mildew fungus) suggest that for both types of biotrophs, penetration through the epidermal wall commonly fails in association with wall-associated defense responses, in part elicited by breakdown products of the plant cell wall. Data suggest that extracellular hydrogen peroxide plays a primary role in this penetration failure, acting either as a signaling agent or as a necessary adjunct to some other defense response within the wall. Protoplast involvement, but not necessarily transcription or translation, is necessary for these wall-associated responses, and they can be reduced by reducing the adhesion between the plant cell wall and the plasma membrane. The latter observation suggests that this adhesion is important for at least some types of defensive signaling between the wall and the cell contents. In host or nonhost plants, Erysiphe species increase this adhesion and wall-associated responses occur even in susceptible plants. However, in its host species, U. vignae locally reduces this adhesion around the penetration site and, as an apparent consequence, no wall-associated responses can be detected. Thus, this latter system is ideal for studying postpenetration cellular and molecular changes in resistant or susceptible host cells without the confounding effect of responses to the trauma of cell wall penetration. Such studies indicate that not only is penetration failure in nonhost plants determined while the fungus is growing through the epidermal cell wall, but that it is at this stage of infection in host species that cellular responses are initiated that determine whether the plant cell will become susceptible to infection or exhibit the hypersensitive response.