Interactions between Plants and Parasitic Fungi

The evolution of fungi is mainly dependent on the further development and spread of green plants. The majority of fungal species is saprophytic, some few are parasitic. The latter are at least in certain stages of their life cycle dependent on a particular supply of nutrients (vitamins, for example) that can only be provided by living cells. It is quite striking that fungal diseases are rather rare in nature due to the very effective defence mechanisms of plants that inhibit a spread of parasitic fungi. The solid cell wall including all its introsusceptions and appositions (the cuticle, for example) that inhibits the penetration of the tissues and cell lumina by fungi, bacteria, viruses, etc. is the first line of defence. Additionally, a wide spectrum of secondary defence compounds exists, many of which are fungicides and/ or bactericides. These substances are often not produced until infection occurs (i.e. until their production is induced, example: phytoalexines).

It is remarkable that plant parasites (and this is equally true for fungi, bacteria, and viruses) are strictly host-specific. Some of them depend on an alternation of hosts, so that one stage of the parasite’s development occurs in one host, the following in another that is phylogenetically not closely related to the first host. Parasites cause far larger damages in monocultures (agriculture) than in plant communities rich in species due to their high host specificity. The annual loss of foodstuff caused by them corresponds to an amount large enough to provide 300 million people.

Parasitic fungi have at least three strategies to get hold of plant ingredients:

1. They produce enzymes for the breakdown of cell walls and cuticles.

2. They produce toxins that do either reduce the activity of the host cells or inhibit it completely.

3. They produce plant-specific substances (hormones, for example) thus meshing with the hormonal equilibrium of the plant cell and causing disruptions of the growth and differentiation of the cells and tissues. Gibberella fujikuroi, for example, secretes gibberellins that influence the growth of the host plant (rice). Studies of this fungus lead to the detection of the gibberellins (class of phytohormones).

The literature about parasitic fungi is very extensive. Many studies originate in economic considerations. The majority deals with the classification of the fungi, their life cycles, the symptoms of the plants and their diagnostic, the host range, and the search for the host’s factors of resistance. The plants’ molecular mechanism of action after infection with fungi has by now just been elucidated in a few cases, and these examples can only partially be generalized due to the variety of possible reactions.

The resistance of the hosts is not only based on the general and unspecific defence mechanisms mentioned above, but also on the production of specific, genetically determined substances directed against specific fungi. Genetic analyses showed that the resistance is on one hand caused by the existence of dominant alleles of the respective genes, and on the other hand by resistance genes that are inherited independently of each other.

Some Remarks about the Classification of Parasitic Fungi

It is distinguished between two types of parasitism:

Necrotrophic Parasitism: the infection leads to a destroying of the tissue and thus to the death of the plant. The fungi are often only optionally parasitic, they can just as well proliferate in dead or withering plant material.

Biotrophic Parasitism: In this case, parasite and host live together for longer periods of time. The parasite takes nutrients and growth-regulating substances from the plant, but does not kill it. Most biotrophic fungi are obligatory parasites. They survive only limited saprophytic phases; especially the development of a fruiting body is dependent on the presence of a host. The cultivation of single (vegetative) stages of these fungi in cell-free nutrient medium succeeded only in a few exceptions.

Parasitic fungi can be found in all classes of fungi, the hosts in all systematic groups of plants (and blue-green algae). The kingdom of fungi subdivides into myxomycetes or moulds (slime fungi) and eumycetes, the higher fungi.

One of the economically most important representatives of the parasitic myxomycetes is Plasmodium brassicae, the causative agent of clubroot, a disease whose symptoms can be seen in the roots of numerous species of cruciferes. The changed differentiation pattern of the infected host tissue is caused by a 50- 100 fold increased auxine content, a 10- 100 fold rise of the cytokinin content, and an increased degree of ploidy of the respective tissues’ nuclei (due to the high level of cytokinin maybe?; I. C. TOMMERUP and D. S. INGRAM, 1971).

Spongospora subterraneae is the causative agent of the potato’s powdery scab that can serve as a vector for the potato-mop-top-virus.

Myxostelida - resting spores splitting open to release myxamoebae - Trichiales - young sporangia of Trichia decipiens - Trichiales - plasmodiocarp of Hemitrichia serpula
© Bryce KENDRICK

Eumycetes.

Phytophthora-species need among a few others Solanaceae (species of the potato family) as hosts. Phytophthora infestans is the causative agent of late blight of potato. The early destruction of the foliage and the reduction of the rate of photosynthesis caused by it leads to heavy crop failure. The host spectrum is - in contrast to some other Phytophthora-species (potato, tomato, and a few others) - very restricted. The fungus was the cause of a big famine in Ireland in the middle of the 19^th century (1845/ 47). A huge migration into the USA was the consequence.

Four kinds of Ascus exist. They do not look alike. They come in two basic kinds, called unitunicate and bitunicate. The picture illustrates the bitunicate type. © Bryce KENDRICK

Ascomycetes. Numerous species like Taphrina insititae (host: plums and others), T. betula (birch), T. cerasi (cherry), T. deformans (peach) and others that cause leaf curls in different hosts belong to the ascomycetes. Most of these species develop haustoria (exception: T. deformans), i.e. processes into the inner of the host cell lumen. The most important precondition for the development of a haustorium is a local perforation of the plant cell wall. The growing haustorium widens into a vesicle-like structure after having penetrated the cell lumen. The host cell’s plasmalemma is not penetrated. Haustoria do therefore not grow into the plasma of the host cells. Electron microscopic studies of different types of haustoria showed that the plasmalemma changed structurally, though. It folds up and a lot of electron-dense material is incorporated into the membrane. These observations point to an active defence reaction of the cells. Leaf curls are caused by an increased, but uneven growth of single leaf areas. Experimental data suggest that the leaves’ content of cytokinins and IAA is increased.

The species causing witches’ broom in numerous host trees belongs to the Taphrina family, too. The symptom is produced by an increased number of vegetative points that are the reason for an irregular, tuft-shaped branching pattern of the infected plant parts.

The order Erysiphales consists of the family Erysiphaceae (mildew). Mildew is the collective name for a variety of Erysiphacae-species that live parasitically on a number of angiosperms: Erysiphe graminis (corn mildew), E. communis (on pumpkin), and E. polygoni (on peas, clover, and other Leguminosae). The fungal mycelium spreads usually on the upper or the undersurface of the leaf. A few epidermal cells are penetrated by occasional haustoria.

Numerous subspecies of Erysiphe graminis have specialized on cereals. Some species, for example, grow on wheat but not on barley, while the opposite is true for others.

   

Erysiphales - SEM of conidial chains and mother cells of the Oidium anamorph of Erysiphe on a host leaf (picture to the left) - dichotomously branched ascomatal appendage of Microsphaera - ascoma of Microsphaera, with dichotomously branched appendages
© Bryce KENDRICK

Ceratocystis ulmi and related species cause the Dutch elm disease. The disease was discovered in Britain in 1927, where 10% of all elms were infected between 1930 and 1940. In the dry summer of 1947, it spread epidemically in Germany, too.

Botrytis cinerea (grey mould) is a not much specialized parasite. It infects lettuce leaves as well as a variety of juicy fruits (tomatoes, strawberries, etc.) if the weather is humid enough.

Basidium of a sequestrate basidiomycete, Gastrocybe, in which the basidiospores are symmetrically mounted, and are not forcibly discharged © Bryce KENDRICK

Basidiomycetes. Two important orders of parasitic fungi belong to the basidiomycetes: Ustilaginales (smuts) and Uredinales (rusts). The order Agaricales consists mainly of the already discussed mycorrhizal fungi, only few species are parasitic (honey fungus, for example). More than 1000 species of Ustilaginales live parasitically on hosts of more than 75 angiosperm families. They produce dark, powder-like traces consisting of fruiting bodies strung together on leaves, shoots, flowers, and fruits. They develop usually no haustoria. Their extensive mycelium spreads through the intercellular spaces of the host plants. Uredinales include about 4,000 species in 100 genera. They are characterized by the red-brownish colour (rusts !) of their spores. Smuts develop haustoria and infect a range of angiosperms, gymnosperms, and pteridophytes. Puccinia graminis is the classic example of a fungus with an alteration of hosts. Its haploid (monocariontic) mycelium grows on Berberis (barberry), its dicariontic mycelium on different grasses. P. graminis is characterized by a complex alternation of generations. Up to five different types of spores can be generated during its course. P. graminis can live on grasses for an infinite time in its dicariontic state, if barberry is not present.

Uredinales. Teleutosorus. The stalked, two-celled winter spores (teleutospores) develop on cereals after the change of the host in summer and hibernate on the ground. These probasidia develop into the original, septate basidiospores (photo: W. KASPRIK).

The preconditions for this change, however, are mild winters, since the dicariontic, asexual uredospores (summer spores) cannot survive long and cold winters. Wind can on the other hand disperse fungus spores thousands of kilometres so that a local extermination of barberry provides no lasting protection against Puccinia. This species consists of a number of subspecies, too. One has specialized on wheat, another on oat, a third on rye, etc. Puccinia graminis belongs to the few parasitic fungi that can be cultivated cell-free on agar (under addition of yeast extract).

      

Uredinales - uredinia of Puccinia graminis tritici erupting through epidermis of wheat (Triticum). - - vertical section through a uredinial sorus of Puccinia graminis tritici in a wheat leaf. - vertical section through an aecium of Puccinia graminis tritici.

Dacrymycetales - "tuning fork" basidia of Dacrymyces at various stages of development
© Bryce KENDRICK

Fungi imperfecti. This is the collective name for fungus species that do not develop fruiting bodies and that are therefore rather difficult to classify. Because of ultrastructural studies, it is assumed today that most of them belong to the ascomycetes. Several species have been used as test objects for studying molecular processes occurring during the infection of plants. We will therefore discuss them two subchapters later.

Parasitic aquatic fungi are rather unknown to the public, since they are of no economic importance. Only few scientists have studied them intensely.

More than 200 filamentous marine fungi have been described. Between a quarter or a third of them live parasitically on algae. Most of them belong to the ascomycetes. Brown, red, and green algae as well as diatoms serve as their hosts. Lagenisma coscinodisca, a diatom parasite, has been especially well documented with the help of the electron microscope.

Most parasites of freshwater algae belong to the chytrids that were discovered by A. BRAUN (Berlin) in 1856. He described them as follows:

" The whole little plant consists of a simple, vesicle-like cell that does often penetrate the cells of the nutritive organism with a root-like excrescence."

Chytrids develop no hyphae, but a non-cellular and partially rather extensive system of rhizoids that seizes the host cells and can even enclose them. Nearly every known species of algae has its own specific parasite. The fungus infections should not be underestimated. Infections of nearly all algal cell-colonies have often been observed towards the end of a ‘water bloom’, i.e. the massive growth of an algal species.

Chytrids infect both blue-green algae (Cyanophyceae) and Volvocales, as well as Chlorococcales. These three groups of algae differ in the chemical composition of their cell walls so that the respective parasites have to have the most diverse enzyme systems at their disposal. The destruction of a cell occurs only after a cell-to-cell contact has been established, i.e. the fungus secretes no lytic substance into the adjacent medium that destroys all cells of a colony that are surrounded by a gelatinous coat.

Years of research into the population dynamics of diatom and cyanophycean parasites showed, that the fungus infection is able to reduce the number of individuals drastically, especially at the beginning of a population’s growth, and to accelerate the decline of a population lastingly. The studies took place in South England’s Lake District. A reduction in the number of individuals of an algal species is usually compensated by an increase in the population size of another species (H. M. CANTER, Freshwater Biological Association, Ambleside). Such quantitative analyses and a larger attention to the consequences of the fungus infection offer possible explanations for the fact that a species of algae is dominant in one year and does scarcely, or not at all occur in the following year.

The infection of algal colonies with chytrids is not the only reason for the disintegration of a water bloom. Other reasons, like the lack of nutrients (especially of phosphate) or weather-caused changes are often decisive, especially if the fungus infection is limited and only few cells of a colonyare destroyed (as was shown e.g. for the end of a bloom of the blue-green alga Microcystis aeruginosa)