Ultrastructural specialization at the host-pathogen interface in rust-infected flax

Abstract

Ultrastructure of the association between the rust fungus, Melampsora lini, and a compatible variety of flax, Linum usitatissimum, was studied to clarify the structural relationships and interactions at the site of host penetration and at the host-parasite interface. Results of freeze-etching as well as a special section-staining procedure consisting of periodate-chromate-phosphotungstate (PACP) are shown with a host-parasite combination for the first time. The host plasma membrane is invaginated by the fungus and forms a continuous boundary around the fungal haustoria which penetrate the host cells. No morphological continuities are observed linking the protoplasts of host and fungus. With both freeze-etching and the PACP stain, the invaginated portion of the host plasma membrane at the host-parasite interface shows distinctive features that are not characteristic of the non-invaginated portion of the membrane. This localized specialization of host plasma membrane in response to the fungus appears as a significant and consistent feature of the host-parasite interaction. The host plasma membrane is separated from the haustorial wall by an amorphous layer of sheath material which covers the body but not the neck of the haustorium. This sheath provides the environment in which the haustorium exists and functions during the course of the host-parasite association. Occasionally, a collar of wall-like material derived from the host cell forms around the haustorial neck. The collar is continuous with the host wall and is distinct and discontinuous from the haustorial sheath. In fewer than 5% of the infected cells this wall material encases entire haustoria. The fungal wall is structurally specialized around the site of host penetration, and it becomes intimately associated with the host wall where the fungus penetrates into the lumen of the host cell. During penetration, the host and fungal walls appear to be fused so that the interface between them is not clearly delineated. The haustorial wall is continuous, via the haustorial neck, with the wall of the haustorial mother cell which lies outside the host cell. Different staining properties reveal this wall continuum to consist of several well-defined regions having different structure or composition. A ring of fungal wall material midway along the haustorial neck stains densely with lead citrate, but is preferentially etched away by periodic acid. The neck ring denotes a transition in the staining reaction of the fungal wall, from that present in the region of host penetration to that of the wall surrounding the haustorium. The findings demonstrate specialization of the fungal wall in the area of host penetration as well as specialization of the host plasma membrane at the host-parasite interface to a degree not previously realized from ultrastructural information.