Structure and Function of Fungal and Oomycete Haustoria

Haustoria formed by biotrophic or hemibiotrophic rusts, powdery mildews and oomycetes are central to the development of a stable biotrophic relationship between pathogen and plant and are key sites for the absorption of the plant nutrients that are essential for pathogen growth, development and reproduction. For their function, haustoria depend on highly regulated molecular exchange across the haustorium-plant boundary. Before nutrients begin to move from plant to pathogen across this interface, the pathogen must send a likely plethora of signals into the infected plant cell, molecules that not only orchestrate host cell structure and metabolism but also suppress the plant cell's defence response. Given the importance of communication across this haustorium-plant interface, it is not surprising that the area of this boundary is often increased by the development, in the rusts, of up to five lobes (Littlefield 1972) or, in the powdery mildews, of multiple finger-like projections (Gil and Gay 1977) extending from the main body of the haustorium. There is still much to learn about the structure and function of the haustorium-plant interface but integrated cellular and molecular studies are beginning to reveal details of its molecular specialisations.

The composition of both the haustorial cell wall and plasma membrane may differ from that of the cell wall and plasma membrane of hyphae. In flax rust, for example, monoclonal antibodies identify a component of the haustorial wall not found in hyphal walls of this species (Murdoch and Hardham 1998). The same monoclonal antibodies do not react with haustoria from maize rust (Puccinia sorghi) or wheat leaf rust (Puccinia recondita), indicating that the haustorial-specific component may also be species-specific (Murdoch and Hardham 1998). Differentiation of haustorial membranes has been demonstrated in the bean rust fungus (see below) and in the hemibiotrophic oomycete, P. infestans (Avrova et al. 2008). In P. infestans, haustorial membranes, but not membranes of intercellular hyphae, contain the membrane protein, Pihmp1, a protein required for haustoria formation (Avrova et al. 2008).

Haustoria are surrounded by an amorphous, gel-like compartment known as the extrahaustorial matrix, across which molecular exchange between pathogen and plant must occur as shown in Fig. 5 (O'Connell 1987; Hahn and Mendgen 1992; Mendgen and Hahn 2002). The matrix consists of a mixture of components, primarily carbohydrates and glycoproteins, derived from both the fungus and the

Haustoria Formed Fungi

Fig. 5 The plant-haustorium interface. In haustoria-forming biotrophic fungi, the haustorial mother cell (HMC) forms a haustorium (H) surrounded by the extrahaustorial matrix (EHMX), which is a discrete compartment sealed by a neckband (N). Upper inset: A proton gradient generated by ATPases (purple oval) on the haustorial membrane (HM) may facilitate uptake of metabolites into the fungus through proton-driven symporters (green oval). Lower inset: Effectors (blue dots) may cross the extrahaustorial membrane (EHM), a modified host plasma membrane that invaginates around the haustorium, into the host cytoplasm, where they may interact with target proteins, thus leading to host manipulation or resulting in recognition by cognate resistance proteins and the mounting of a defence response. Effectors may also be secreted into the apoplast. PM plant plasma membrane, CW plant cell wall, HCW haustorial cell wall

Fig. 5 The plant-haustorium interface. In haustoria-forming biotrophic fungi, the haustorial mother cell (HMC) forms a haustorium (H) surrounded by the extrahaustorial matrix (EHMX), which is a discrete compartment sealed by a neckband (N). Upper inset: A proton gradient generated by ATPases (purple oval) on the haustorial membrane (HM) may facilitate uptake of metabolites into the fungus through proton-driven symporters (green oval). Lower inset: Effectors (blue dots) may cross the extrahaustorial membrane (EHM), a modified host plasma membrane that invaginates around the haustorium, into the host cytoplasm, where they may interact with target proteins, thus leading to host manipulation or resulting in recognition by cognate resistance proteins and the mounting of a defence response. Effectors may also be secreted into the apoplast. PM plant plasma membrane, CW plant cell wall, HCW haustorial cell wall plant (Harder and Chong 1991). The extrahaustorial matrix is delimited on the pathogen side by the haustorial cell wall and on the host side by an extension of the host plasma membrane known as the extrahaustorial membrane (Harder and Chong 1991). In rust and powdery mildew infections, the extrahaustorial matrix is sealed off from the apoplast by a structure known as the neckband which is thought to act as a selectively permeable barrier, like the Casparian strip at the endodermis of plant roots (Heath 1976; Harder and Chong 1991). Haustoria of hemibiotrophic fungi and oomycetes appear to be less differentiated than those of the rusts and powdery mildews and generally lack neckbands, although some exceptions exist, as in the case of the oomycete Albugo candida which possesses a simple neckband (Soylu 2004; Perfect and Green 2001). In infections by some rust fungi, such as Puccinia hemerocallidis and Puccinia striiformis, tubular beaded elements contiguous with the extrahaustorial matrix extend from the extrahaustorial membrane into the host cytoplasm, perhaps again serving to increase the surface area of this interface (Mendgen et al. 1991; Mims et al. 2002, 2003). These structures were not observed at the host-haustorial interface during P. recondita or Uromyces appendiculatus rust infection (Mendgen et al. 1991). Tubular extensions into the cytoplasm from the extrahaustorial membrane also occur during infections by the oomycete A. candida (Baka 2008).

Although contiguous with the plant plasma membrane, from which it is thought to be derived, the extrahaustorial membrane exhibits distinct molecular properties

(Hardham 2007). Differences include a reduced glycolipid content, differential staining by phosphotungstic acid and a reduced level of ATPase activity compared to the rest of the host plasma membrane (Baka et al. 1995; Perfect and Green 2001). The extrahaustorial membrane formed during infection of pea plants by the pea powdery mildew, Erysiphe pisi, contains a large (200 kDa) glycoprotein that does not occur elsewhere in the plasma membrane of infected cells (Micali et al. 2008; Roberts et al. 1993). Similarly, the plant resistance protein RPW8.2 is specifically targeted to the extrahaustorial membrane of Arabidopsis leaf cells infected by powdery mildew, Golovinomyces orontii (Micali et al. 2010). During infections of Arabidopsis by G. orontii and another powdery mildew, Erysiphe cichoracearum, host plasma membrane proteins are specifically excluded from the extrahaustorial membrane (Koh et al. 2005; Micali et al. 2010).

Haustoria have been difficult to analyse at a molecular level because they are only formed in planta. However, methods to isolate haustoria either by differential centrifugation or affinity purification have been developed (Gil and Gay 1977; Tiburzy et al. 1992; Hahn and Mendgen 1992; Micali et al. 2010) and in recent years have facilitated studies of haustorial proteins and transcriptomes (Hahn et al. 1997; Murdoch and Hardham 1998; Catanzariti et al. 2006; Micali et al. 2010). Early studies led to the proposal that haustoria were specialised feeding structures that played a key role in nutrient acquisition, but definitive evidence was difficult to obtain. Strong evidence to support this hypothesis has come from transcriptome analyses of genes that are preferentially expressed in haustoria of the bean rust fungus, U. fabae (Hahn and Mendgen 1997). This study identified two cDNA sequences, AAT1 and AAT2, which have homology to genes encoding amino acid transporters (Hahn and Mendgen 1997). AAT1 is a broad-specificity amino acid transporter (Struck et al. 2002). AAT2 was shown by immunolocalisation to occur specifically in the haustorial membrane, although no amino acid transport activity has yet been described for this protein (Mendgen et al. 2000). Further evidence for a role of U. fabae haustoria in nutrient acquisition comes from studies of a haustorially expressed sugar uptake transporter, HXT1p, which transports monosaccharides through a proton symport process when expressed in Xenopus oocytes (Voegele et al. 2001; Voegele and Mendgen 2003). Given that ATPases, which are required for the pumping of protons across membranes, are reduced on the extrahaustorial membrane but enriched on the fungal haustorial membrane (Baka et al. 1995; Struck et al. 1996, 1998), this finding suggests that during infection, a proton gradient is generated between the extrahaustorial matrix and the haustorium that is used to drive active transport of nutrients towards the pathogen (Fig. 5 inset; Szabo and Bushnell 2001; Baka et al. 1995; Aist and Bushnell 1991).

In addition to this role in nutrient acquisition, it has also emerged that the secretion of pathogen proteins, known as effectors (described in greater detail below), from haustoria is important in establishing biotrophy by allowing manipulation of host metabolism and defence responses. In agreement with this scenario, compatibility between the host and the pathogen appears to be determined at the onset of haustorial development since spore germination, germ tube growth, appressorium formation and growth of primary infection hyphae develop on a similar time scale in both susceptible and resistant host plants (Dickinson and Lucas 1982).

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  • bruna
    How is haustoria formed in fungi?
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    What is the function of huastoria in fungi?
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    Where are haustoria found?
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    What is haustorium and it's function?
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    What is the main function of a haustoria?
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