Commentary Hidden robbers: The role of fungal haustoria in parasitism of plants Les J. Szabo* and William R. Bushnell Cereal Disease Laboratory, Agricultural Research Service, U.S. Department of Agriculture, and Department of Plant Pathology, University of Minnesota, St. Paul, MN 55108 iotrophic fungi have developed a Brange of ‘‘life styles’’ in their relation- ship with plants from the mutualistic to the parasitic. Vesicular-arbuscular mycor- rhizal 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 min- erals 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 nu- trients but basic questions remain regard- ing the function of the haustorium. These include: What are the major nutrients Fig. 1. Haustorial complex, a specialized feeding organ of biotrophic fungal parasites of plants. To move transported? What mechanisms are in- from host cell to fungus, nutrients must traverse the extrahaustorial membrane, the extrahaustorial matrix, the haustorial wall, and the haustorial plasma membrane. A neckband seals the extrahaustorial volved in the transport? How do individ- matrix from the plant cell wall region so that the matrix becomes a unique, isolated, apoplast-like ual components of the haustorium–host compartment. The haustorium connects to intercellular fungal hyphae by way of a haustorial mother cell. cell interface contribute to nutrient flow? Evidence from Voegele et al. (1) indicates that a proton symport system in the haustorial plasma And overall, how does haustorial function membrane drives sugar transport from plant to parasite. (A) Transmission electron micrograph of a flax relate to the biotrophic relationship be- rust haustorium [Reproduced with permission from ref. 2 (Copyright 1972, NRC Research Press)]. (Bar, 1 tween host and parasite? The paper by ␮m.) (B) Drawing showing key features of the fungal haustorium. Voegele et al. (1) in this issue of PNAS provides an important advance by charac- terizing a sugar transporter located at the rial cytoplasm, substances must pass se- a peg and the establishment of a hausto- haustorium–host interface. quentially through the extrahaustorial rium. Artificial membranes and etched surfaces have been used to mimic the A haustorium is formed when a special- membrane and matrix, the haustorial wall, topography of the leaf surface and induce ized fungal hypha penetrates a plant cell and the haustorial plasma membrane. the development of infection structures in wall and expands inside that cell (ref. 2; The development of the haustorium is vitro (4–6). However, the development is Fig. 1A). However, the haustorium is not the final step of an infection pathway in incomplete and haustoria are usually not located directly in plant cell cytoplasm; which the plant host plays a major role. In formed unless carbohydrate is added (7). instead, it is surrounded by an extrahaus- the case of rust fungi, infection typically Uptake studies have demonstrated that torial membrane, a thickened derivative of begins with the germination of a spore on sugars and amino acids are transferred the plant cell plasma membrane. Lying the leaf surface, followed by the develop- ment of an appressorium. The develop- from the host plant into biotrophic para- between the extrahaustorial membrane sites (8–11) and strongly support the idea and fungal haustorial wall is a gel-like ment of the appressorium depends on a thigmotrophic signal triggered by the spe- that haustoria play a major role. However, layer enriched in carbohydrates called the because of the intracellular locations of cific topography of the host plant leaf extrahaustorial matrix. The haustorium haustoria and the complexities of the surface (3). An infection peg formed by itself contains a normal complement of haustorium–host interface, it has been cytoplasm, nuclei, mitochondria, and the appressorium enters the leaf through a other organelles (Fig. 1A). The haustorial pore (stoma), followed by the develop- cytoplasm is bordered by a plasma mem- ment of a substomatal vesicle, an infection See companion article on page 8133. brane and by the haustorial wall (Fig. 1). hypha, a haustorial mother cell, penetra- *To whom reprint requests should be addressed. E-mail: To move from plant cytoplasm to hausto- tion of a photosynthetic mesophyll cell by [email protected]. 7654–7655 ͉ PNAS ͉ July 3, 2001 ͉ vol. 98 ͉ no. 14 www.pnas.org͞cgi͞doi͞10.1073͞pnas.151262398 Downloaded by guest on September 29, 2021 this gene was expressed in haustoria iso- ATPase (17) and an amino acid trans- lated from leaves, but not in other infec- porter (18) have been isolated. tion structures induced in vitro. Further, The work of Voegele et al. (1) has the authors demonstrated that this sugar provided an important piece of the puzzle transporter is localized in the haustorial regarding the nutrient transport pathway membrane and not in membranes of in- across the host–parasite interface in obli- tercellular hyphae, thus providing the first gate parasitic fungi. However, many ques- direct evidence that sugar uptake occurs tions remain. Does sucrose diffuse out of in the haustorium and suggesting that the the host plant cell into the extrahaustorial haustorium may be the sole site. matrix, or is it first cleaved in the host Sucrose is the primary sugar that is cytosol into glucose and fructose? What transported in plants and, therefore, it has enzyme breaks down the sucrose? Is it been speculated that the haustoria may invertase, which is known to increase in infected leaf tissue (19, 20), or alterna- import sucrose directly. Recent studies tively, sucrose synthase? Once glucose is with the powdery mildew fungus indicate transported into the haustorium, what that glucose, rather than sucrose, may be sugar is then transported into intercellular the sugar imported (14, 15). The data of hyphae? It has been speculated that man- Voegele et al. (1) demonstrate that the nitol may play this role (21). Further, HXT1 sugar transporter has a specificity photosynthetic mesophyll cells, usually for D-glucose and D-fructose, confirming producers of sucrose, which is actively that glucose/fructose and not sucrose are exported, become net importers when col- the primary sugars imported by haustoria. onized by rust fungi. How does the obli- Fig. 2. Proton symport model for nutrient trans- In addition, the authors showed that glu- gate parasite manipulate the host to port across the haustorial plasma membrane, sup- cose transport occurs through a proton change the flow of sugars? Are there gene plying glucose and amino acids to biotrophic fungi. symport mechanism. These results sup- regulators that are secreted by the fungal 1, Protons are supplied by haustorial plasma mem- port a proton symport model for nutrient ϩ haustorium into the plant cell that alter brane H -ATPase (15); 2, Amino acid transporter transport at the haustorial interface (ref. these pathways? What other compounds (16); 3, Glucose/fructose transporter described by 16; Fig. 2). A membrane Hϩ-ATPase gen- traverse this interface? What methods are Voegele et al. (1). Redrawn from Hahn et al. (16). erates a proton gradient across the haus- used by the fungus to elude or suppress torial plasma membrane, which provides the defense mechanisms of the host? difficult to determine what transfer pro- the energy for transport of nutrients (glu- The results of Voegele et al. (1) elegantly cesses are involved and where they are cose/fructose, amino acids) from the ex- demonstrate that multifaceted experi- located. In the last several years a differ- trahaustorial matrix into the haustorium. mental approaches can provide answers ent approach has been taken, in which The establishment of a proton gradient is to the roles of haustoria in host–parasite cDNAs for developmentally expressed possible because the extrahaustorial ma- interactions. COMMENTARY genes in infection structures and haustoria trix is a sealed compartment, bounded by have been isolated (12, 13). Voegele et al. the extrahaustorial membrane on the We thank Jacki Morrison for preparation of the figures, and Kurt Leonard and Richard Staples (1) demonstrated that one of the most plant side, the haustorial membrane on for their comments on the manuscript. This abundantly expressed genes in the rust the fungal side, and the neck band, which paper was supported by the Agricultural Re- haustorium encodes a sugar transporter seals it from the apoplast. In support of search Service of the U.S. Department of ϩ (HTX1). 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