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Biotrophy and Rust Haustoria Physiological and Molecular Plant Pathology (2000) 56, 141±145 doi:10.1006/pmpp.2000.0264, available online at http://www.idealibrary.com on MINI-REVIEW Biotrophy and rust haustoria KURT MENDGEN*, CHRISTINE STRUCK, RALF T. VOEGELE and MATTHIAS HAHN UniversitaÈt Konstanz, Department of Biology, Phytopathology, D-78457 Konstanz, Germany (Accepted for publication March 2000) INTRODUCTION to a haustorial body reaching into the host cell. Around the neck is an iron- and phosphorus-rich neckband which Haustoria produced by biotrophic fungi and Oomycetes bridges the plant and fungal plasma membrane. It seems are extensions into living host cells. However, they are not to serve as a seal against the ¯ow of solutes from the truly intracellular. They breach the cell wall only and a extrahaustorial matrix into the apoplast of the plant [17, newly formed host plasma membrane (the extrahaustorial 20, 22]. The lack of intramembrane particles, as revealed membrane) surrounds them, resulting in a close associ- by freeze fracture electron microscopy and dierent ation of fungal and plant membranes only separated by a cytochemical methods, convincingly demonstrated that thin fungal wall and an extrahaustorial matrix. The the extrahaustorial membrane diers from ``conventional extrahaustorial matrix is mainly of host origin. Heath and membranes'' in plant cells [17]. Although these methods Skalamera [23] suggest that this interface is the site for were unable to reveal the molecular basis of such translocation of nutrients and exchange of information. modi®cations, they proved the existence of a specialized Two more aspects seem to be of utmost importance. First, membrane surrounding the haustorium. In light of the the fungal haustorium must not be recognized as foreign apparent similar tasks that these diverse morphological by the host in order to avoid defence reactions. Second, types of haustoria perform, the question arises whether the fungus should modify the host's metabolite ¯ow to they share common molecular properties. ensure optimal access to these resources. PROBABLE HAUSTORIAL FUNCTIONS THE HAUSTORIUM, A SPECIALIZED HYPHAL BRANCH Haustoria appear to have two main tasks: (1) the regulation of the host±parasite interaction, and (2) the The fungal haustorium may be a short or long simple uptake of nutrients. unbranched projection from an intercellular hypha. Numerous experiments have characterized the host It may be an extensively lobed or branched structure, range of rust fungi which is usually restricted to related or it may be dierentiated as a neck with a haustorial host species [10]. A comparison of haustoria from closely body attached, each with specialized wall structures [9]. related rusts revealed unique structural modi®cations for The morphological spectrum is exempli®ed best by the each species [3, 4]. Also, the same host plant shows rust fungi which have monokaryotic and dikaryotic stages with very dierent morphologies of haustoria. species-speci®c interactions with dierent rusts: Oat plants infected with Puccinia graminis, develop endoplas- The monokaryon produces M-haustoria. Compared to matic reticulum derived membranes with small inter- hyphae, they exhibit only a few structural modi®cations connected tubules, whereas after infection with P. coronata, during growth into host cells [13], yet, the extrahaustorial they form very dierent long and narrow tubular membrane surrounding the M-haustorium is modi®ed extensions [17]. These observations suggest that, apart compared with the plant plasma membrane [1]. In from the signals exchanged between host and parasite contrast, the dikaryon dierentiates the haustorial during development of infection structures [21], for- mother cell in close contact with the plant cell wall, and the haustorium consists of a tubular neck connected mation of the ®ne structure of the haustorial parasite± host interface occurs under the control of species- or even * To whom all correspondence should be addressed. E-mail: race-speci®c signals. Such signals may include suppres- [email protected] sors. Suppressors have been postulated to be involved in 0885-5765/00/040141+05 $35.00/00 *c 2000 Academic Press 142 K. Mendgen et al. maintaining basic compatibility between biotrophic fungi parasites, have been hampered by the close association and their host plants [6]. Evidence for suppressors comes of fungus and plant. Nehls and coworkers [36, 37]have from a phenomenon called induced susceptibility. French cloned the ®rst plasma membrane transporters for sugars bean tissue already infected by Uromyces vignae supported and amino acids from the ectomycorrhizal fungus Amanita additional infections by several nonhost pathogens [8]. muscaria. The authors demonstrated regulation of the Similarly, haustoria of Erysiphe graminis, the powdery corresponding genes in response to dierent metabolites mildew pathogen, can induce such susceptibility [29]. in mycelium grown in vitro and performed a biochemical However, experimental evidence for suppressors from characterization of the transporters expressed in yeast. these fungi is still weak [2, 34]. However, the roles of these transporters in fungal Evidence for the uptake of de®ned host metabolites, nutrition and symbiosis remain speculative since no such as sugars and amino acids, by rust haustoria is scarce data regarding the localization and distribution of these and mostly indirect. Studies with radioisotopes started transporters in planta are available. Harrison and van more than three decades ago [25]. They have the Buuren [19] have cloned a phosphate transporter from disadvantage that any labelled substrate fed to infected the VA-mycorrhizal fungus Glomus versiforme by expression host plants is metabolized to a certain extent on its path in yeast. By means of RT-PCR, they localized transcripts to the fungus. In addition, depending on the isotope used, of the transporter in external hyphae of symbiotically 14 3 CO2 or H2O may develop as products and obscure the growing G. versiforme. These data provided the ®rst piece results. Eorts to dierentiate between uptake by haus- of molecular evidence for the postulated nutrient ¯uxes in toria or by intercellular hyphae revealed some trends, but VA-mycorrhizae. were not able to trace the fate of single compounds from the plant cell into the haustorium [33]. In powdery mildews, the role of haustoria in nutrient uptake is more TRANSPORT PROTEINS IN HAUSTORIA evident, because they are the only fungal structures with- in the host tissue. Feeding experiments with radiolabelled Based on the screening of a rust haustorium-speci®c sugars seemed to indicate that glucose, and not sucrose, cDNA-library, genes encoding three amino acid trans- is the main carbohydrate obtained from epidermal porters (AAT1, AAT2, AAT3) were isolated. AAT2 cells [46]. (formerly PIG2)andAAT3 are amino acid transporters On the basis of inhibitor studies with haustoria of based on sequence homology [15, 16, M. Hahn, unpub- E. graminis,Gayet al.[11] and Manners [32] suggested lished]. AAT1 (formerly PIG27) was expressed in amino that the extrahaustorial membrane loses control of acid uptake de®cient yeast cells, enabling the trans- solute export and that ATPase activity of the haustorial formants to take up histidine and lysine (M. Hahn, plasma membrane would support a high ¯ux of solutes unpublished). Antibodies raised against synthetic across the haustorial interface. However, the lead peptides from the predicted sequence of AAT2p demon- precipitation technique used to detect meaningful mem- strated that the putative amino acid transporter is local- brane ATPase activity on the host or the fungal side has ized to the plasma membrane of the haustorial body. In given inconsistent results [1, 48]. This technique has addition, a hexose transporter gene (HXT1) was isolated been debated since its development [27, 39, 42], and (R. Voegele, unpublished). Preliminary results with immunocytological data are urgently needed to clarify antibodies raised against portions of HXT1p indicate the localization of the plasma membrane ATPase. that this protein has a similar localization as AAT2p. In agreement with homologous transporters from other organisms, heterologous expression and characterization in yeast mutants or Xenopus oocytes classi®ed the trans- porters found so far in U. fabae as H/solute symporters ENZYMES INVOLVED IN SUBSTRATE (C. Struck, unpublished). UPTAKE BY FUNGAL HYPHAE Plasma membrane H-ATPase plays a key role in Wild Saccharomyces cerevisiae has become one of the active nutrient uptake. The ®rst biochemical evidence for model organisms for the characterization of structure the existence of this enzyme was obtained using and function of plasma membrane transport proteins microsomal vesicles of isolated haustoria of U. fabae. [38, 40], surprisingly little is known about the molecular Compared with ungerminated urediospores and germ aspects of transport processes across the cytoplasmic tubes, the hydrolytic activity of the haustorial H- membrane of ®lamentous fungi. In Neurospora crassa,one ATPase is several-fold higher, suggesting that the enzyme of the best studied species, facilitators and secondary plays an important role in rust haustoria [44]. Molecular transporters have been found with speci®cities for amino analysis revealed a single copy gene, PMA1, encoding the acids, hexoses and ions [5, 26]. Studies with symbionts, U. fabae plasma membrane H-ATPase. Little changes in such as mycorrhizal fungi or obligately biotrophic transcript
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