Biotrophic plant pathogens

Quite a lot of plant-pathogenic fungi establish a long-term feeding relationship with the living cells of their hosts, rather than killing the host cells as part of the infection process. These pathogens are termed biotrophic [from the Greek: bios = life, trophy = feeding].

Typically, these fungi grow between the host cells and invade only a few of the cells to produce nutrient-absorbing structures termed haustoria. By their feeding acitivities, they create a nutrient sink to the infection site, so that the host is disadvantaged but is not killed. This type of parasitism can result in serious economic losses of crop plants, and in natural environments it can reduce the competitive abilities of the host; indeed, a few biotrophic pathogens have been used successfully as biological control agents of agricultural weeds.

In many ways, this type of parasitism is very sophisticated - keeping the host alive as a long-term source of food. This has led some people to suggest that biotrophic parasitism is evolutionarily advanced. But this is clearly not the case in general, because an almost identical type of parasitism is found in the arbuscular mycorrhizal fungi (see Mycorrhizas) which are thought to have developed on the earliest land plants.

Here we consider the two most important groups of biotrophic plant pathogens:

• the rust fungi (Basidiomycota)
• the powdery mildew fungi (Ascomycota).

A parallel can be made between the behaviour of these fungi and the biotrophic mycoparasites (see Verticillium biguttatum)

Powdery mildew of roses, caused by the fungus Sphaerotheca pannosa.

This is a very common disease, familiar to most gardeners, and it is typical of many powdery mildews, where the fungus forms a powdery coating of white spores on the leaf surface. Other common examples in Britain are powdery mildew of hawthorn (Podosphaera oxyacanthae), gooseberry (Sphaerotheca mors-uvae), and cereals and grasses (Erysiphe graminis).

All these fungi grow superficially on the host, only penetrating the leaf epidermis. But they extract considerable amounts of plant nutrients through their haustoria, and these nutrients are used for sporulation, leading to rapid epidemic spread of these diseases.

Figure A (above) shows many separate, localised lesions of Erysiphe graminis on wheat leaves. The conidia from these lesions (C, D, stained with trypan blue) are produced continuously in chains, maturing at the tip of the chain and being wind-dispersed. They are large enough (about 30 micrometres) to impact onto cereal leaves at normal wind speeds (typically 1-2 metres per second) in field conditions (see Airborne Microbes). Figure B shows similar lesions near the end of the growing season. The small black flecks are the ascocarps. The ascocarps of a different fungus (Podosphaera, the powdery mildew fungus of hawthorn) are seen at higher magnification in Figure E. This type of ascocarp is termed a cleistothecium - a closed body containing one or more asci (each with 8 ascospores inside it). The ascospores are released when the cleistothecium wall is ruptured. (For another example, see Thermoascus)

The haustorium of Erysiphe graminis is highly distinctive (Figure F), consisting of a rounded body with finger-like projections in a wheat epidermal cell. The fungus in this Figure was stained with trypan blue, which also shows the host cell nucleus (n). The haustoria of E. graminis, like those of all biotrophic fungi, are not in direct contact with the host cell contents, because they are surrounded by a membrane - the extrahaustorial membrane - which represents a modified form of the host cell membrane (Fig. G).

From Deacon (1997) Modern Mycology

By digesting the host cell walls with enzymes, it has been possible to isolate "haustorial complexes" consisting of the haustorium and its encasing membrane. Experimental studies on these haustorial complexes of pea powdery mildew have shown that the extrahaustorial membrane lacks ATPase activity (see Figure G) and thus lacks the ability to control the movement of nutrients across this membrane. In contrast, both the haustorial membrane (of the fungus) and the plant cell membrane have normal ATPase activity for driving nutrient uptake.

The consequence is that the fungus can take up nutrients from the host cell, with little or no resistance, while the infected host cell can take up nutrients from its neighbours. So there is a one-way flow of nutrients into the haustorium, and from there to the fungal hyphae on the plant surface, where the fungus uses the nutrients for spore production.

The infection behaviour of rust fungi is broadly similar to that of the powdery mildews, involving nutrient absorption by haustoria to support abundant sporulation for epidemic spread. These fungi also get their name from the characteristic sporing stage - in this case the (usually) rust-coloured uredospores which develop in pustules where the fungus erupts through the plant surface.

Figure H. Wheat leaf infected by the rust fungus, Puccinia graminis var tritici, showing individual lesions (light coloured haloes on the leaf) with pustules of uredospores in their centres. [Image taken by placing an infected leaf on a flat-bed scanner]

For example, Puccinia graminis var. tritici has wheat as its main host and barberry plants (Berberis species) as its alternate host. There is a correspondingly large number of sporing stages - up to 5 in some cases, as shown below.

Figure I. Life cycle of Puccinia graminis var tritici.

• P. graminis produces uredospores from a bed of tissue that erupts through the leaf or stem surface (Figures J, K). These uredospores can reinfect another wheat plant (see Fungal tip growth), leading to multiple cycles of infection during the cropping season. They are binucleate spores, containing nuclei of different mating types, and they germinate to produce hyphae that have 2 nuclei in each hyphal cell. In this condition, the fungus is termed a dikaryon (i.e. with two nuclear types).
• Near the end of the growing season, the same pustules produce a different type of spore - the teliospore, which consists of two cells with heavily thickened and darkly pigmented walls (Figure L). The teliospores also are dikaryons, with two nuclei in each cell.
• The teliospores overwinter, and in spring the nuclear pairs fuse to form diploid nuclei. This is followed immediately by meiosis, then the spore germinates from each cell to form a short hypha that produces 4 uninucleate, haploid basidiospores (see Figure I).

Figures J-L. Puccinia graminis on the cereal host. (J) Pustules of uredospores on a cereal stem. (K) Section of a leaf showing eruption of uredospores through the leaf epidermis (stained with safranin). (L) Section of a leaf later in the season, showing teliospores in place of the uredospores that were produced earlier.

• The basidiospores can only infect a barberry plant. They give rise to haploid hyphae of different mating types, which grow through the barberry leaf. These hyphae produce flask-shaped sexual structures termed spermogonia on the upper surface of the barberry leaf (Figures M and N). Small "male" sexual spores (spermatia) are formed within the spermogonia, and "female" flexuous hyphae project from the neck of the spermogonium, among the stiffer hairs (arrowhead in Figure N).
• Fertilisation of flexuous hyphae by spermatia of a different mating type is brought about by insects. Then the nuclei pair in the hyphae, forming a dikaryon which gives rise to sporing pustules on the lower surface of the barberry leaf (Figures O and P).
• The spores from these pustules are termed aeciospores. They can only infect a cereal host, thereby completing the life cycle.

Figures M-P. Puccinia graminis on the alternate host, barberry. (M) Small lesions on the upper surface of a barberry leaf, with spermogonia in their centres. (N) Section of a spermogonium, showing the minute spermatia (male sexual cells) and the position (arrowhead) where flexuous (female) hyphae arise. (O) Close-up of lower surface of the leaf, showing cup-shaped pustules of aeciospores. (P) Cross section of a leaf showing the aeciospores developing in tightly packed chains from a pad of fungal tissue.

Rust fungi are remarkably common on both crop plants and wild, native plants. On crops they cause serious economic damage, necessitating the use of fungicides. Although Puccinia graminis (black stem rust of cereals) is most important in the USA, Puccinia striiformis (yellow rust) and P. recondita (brown rust) are more important on cereals in Britain.

Several other rusts are common in Britain.

• Phragmidium violaceum produces pustules of violet teliospores on the leaves of blackberry bushes (Rubus fruticosus) (Figures Q, R). The stalked teliospores of this fungus are highly distinctive (R). There is no alternate host in this case, only the main host.
• Puccinia punctiformis (thistle rust) is also commonly seen (Figure S). It grows systemically in the thistle Cirsium arvense, overwintering as mycelium in the rootstock, and producing chocolate-brown aeciospores. This fungus also has no alternate hosts.
• Another common species is birch rust, Melampsoridium betulinum, which forms abundant uredospores (Figure T) and aeciospores on birch leaves. Larch trees are the alternate host of this fungus.
• Further common species include mint rust, groundsel rust (Coleosporium tussilaginis; Figures U, V), dandelion rust, hollyhock (mallow) rust and snapdragon (Antirrhinum) rust.

Figure Q-R. Blackberry rust, showing pustules of aeciospores on the leaf surface (Q) and the stalked, multicellular aeciospores under a microscope (R). Figure S. Thistle rust. Figure T. A mass of uredospores of birch rust, each about 30 micrometers long and easily impacted onto leaf surfaces during wind-dispersal.

Figures U,V. Groundsel (Senecio vulgaris), a common weed of open ground. U, whole plant (about 15 cm tall) with rust infection at the base; V, close-up of base, showing uredospore pustules of Coleosporium tussilaginis on the stem and leaves.

Books:

JW Deacon (1997) Modern Mycology. Blackwell Scientific, Oxford.

Websites:

An excellent site from a public-service disease diagnostic lab in USA: Oklahoma State University Diagnostic Laboratory

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