Hidden robbers: the role of fungal haustoria in parasitism of plants.

B iotrophic fungi have developed a range of ‘‘life styles’’ in their relationship with plants from the mutualistic to the parasitic. Vesicular-arbuscular mycorrhizal fungi form mutualistic relationships with the roots of their plant hosts, in which the fungus obtains sugars from the plant and provides phosphates and other minerals in return. At the other extreme, powdery mildew and rust fungi form an obligately parasitic relationship in which the host plant becomes a source for sugars, amino acids, and other nutrients. These parasites develop a specialized organ, the haustorium (Fig. 1) within plant cells for transfer of nutrients from host cell to fungal thallus. The haustorium is assumed to have a key role in the ability of these parasites to compete with the developing plant for photoassimilates and other nutrients but basic questions remain regarding the function of the haustorium. These include: What are the major nutrients transported? What mechanisms are involved in the transport? How do individual components of the haustorium–host cell interface contribute to nutrient flow? And overall, how does haustorial function relate to the biotrophic relationship between host and parasite? The paper by Voegele et al. (1) in this issue of PNAS provides an important advance by characterizing a sugar transporter located at the haustorium–host interface. A haustorium is formed when a specialized fungal hypha penetrates a plant cell wall and expands inside that cell (ref. 2; Fig. 1 A). However, the haustorium is not located directly in plant cell cytoplasm; instead, it is surrounded by an extrahaustorial membrane, a thickened derivative of the plant cell plasma membrane. Lying between the extrahaustorial membrane and fungal haustorial wall is a gel-like layer enriched in carbohydrates called the extrahaustorial matrix. The haustorium itself contains a normal complement of cytoplasm, nuclei, mitochondria, and other organelles (Fig. 1 A). The haustorial cytoplasm is bordered by a plasma membrane and by the haustorial wall (Fig. 1). To move from plant cytoplasm to haustorial cytoplasm, substances must pass sequentially through the extrahaustorial membrane and matrix, the haustorial wall, and the haustorial plasma membrane. The development of the haustorium is the final step of an infection pathway in which the plant host plays a major role. In the case of rust fungi, infection typically begins with the germination of a spore on the leaf surface, followed by the development of an appressorium. The development of the appressorium depends on a thigmotrophic signal triggered by the specific topography of the host plant leaf surface (3). An infection peg formed by the appressorium enters the leaf through a pore (stoma), followed by the development of a substomatal vesicle, an infection hypha, a haustorial mother cell, penetration of a photosynthetic mesophyll cell by a peg and the establishment of a haustorium. Artificial membranes and etched surfaces have been used to mimic the topography of the leaf surface and induce the development of infection structures in vitro (4–6). However, the development is incomplete and haustoria are usually not formed unless carbohydrate is added (7). Uptake studies have demonstrated that sugars and amino acids are transferred from the host plant into biotrophic parasites (8–11) and strongly support the idea that haustoria play a major role. However, because of the intracellular locations of haustoria and the complexities of the haustorium–host interface, it has been