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Risk from cooperative interactions

New plant diseases have always threatened world nutrition. The most important groups of pests include biotrophic pathogens. Biotrophy arises from the loss of important metabolic genes, which is countered by suppressing the plant's defenses and the resulting access to plant metabolic products. Successful host colonization requires genetic diversity and thus sexual recombination and interaction with other organisms. In order to understand the development of new diseases, such interactions are analyzed in the natural environment

Threat to world food supply from plant pests

Plant diseases threaten human nutrition, as these diseases lead to severe yield losses or even to the complete destruction of yields. While industrialized nations can limit yield losses through high expenditure on pesticides, developing and emerging countries are at the mercy of epidemics, particularly due to new pathogens.

Despite massive advances in the development of pesticides and plant breeding, new pathogens emerge faster than protective measures can be developed. One example of this is black rust from grain. A new variant of this rust fungus was discovered in Uganda in 1998, which infects all common wheat races, including those that were not considered susceptible and therefore resistant. The fungus is now spreading further east via Iran and threatens India and thus the food base for millions of people [1]. The ecological principles that lead to pathogens, beginning on wild or cultivated plants, subsequently leading to epidemics on agriculturally relevant plants, have so far been only sparsely investigated, although historical examples show their importance. For example, by reducing the barberry stocks in the USA, the black rust infestation could be significantly reduced after the barberry had been identified as an important intermediate host for the sexual reproduction of the fungus [2]. This and other examples show how important it is to understand ecological relationships, in particular the biodiversity and interaction of organisms in their natural surroundings, if one wants to secure food for the still growing world population in the future.

Development of the biotrophic way of life of pathogens

Since rust fungi can only develop and multiply on living plants, in the course of evolution they have developed sophisticated methods of colonizing host plants and overcoming ever new plant protection measures. Due to the dependence on a living host, these pathogens are called obligate biotroph (bios: life, trophé: nutrition) (Fig. 1).

For a long time it was unclear how and, above all, why pathogens adapt to their host plants in such a way that they can ultimately no longer survive without them. The recent sequencing and analysis of numerous genomes of biotrophic pathogens finally revealed this. It turned out that all pathogens that lead such a way of life have lost numerous genes from their genome, which are necessary for important metabolic pathways, such as genes for the production of amino acids or vitamins, but also cell wall-degrading enzymes, which in turn affect those There are fungi that grow on dead plant material.

Since a biotrophic way of life occurs not only in fungi, but also in other organisms such as the Oomycetes, which are related to algae, it was interesting to make comparisons of the genomes of filamentous pests quite independently of their degree of relationship. The evaluation of the genome of downy mildew [3] and the white rust pathogen [4] (Fig. 2) also showed a loss of numerous genes that are important for the metabolism and thus confirm that this is possibly a mechanism that occurs in all biotrophic plant pathogens.

But why does an organism lose important genes from its genome? DeBary [5] discovered 150 years ago that plant pathogens, especially those with a biotrophic lifestyle, develop structures that extend into the plant cell. These highly specialized structures were called haustorien (haurire: to scoop out) (Fig. 3) and it turns out that they probably serve the pathogens to absorb nutrients. How such structures can be formed in the plant cell, however, without dying or effectively fighting this attack, remained unclear for a long time. Only the sequencing of numerous genomes and experimentally determined data showed that biotrophic pathogens have a pronounced repertoire of proteins that are able to suppress the defense of the plant. It was therefore hypothesized that this complex repertoire of proteins also enables the differentiation of structures for the uptake of nutrients. Because: The uptake of nutrients from a living host cell means that substances, which require a lot of energy to generate and thus limit the growth of the pathogen, no longer have to be produced. Genes, which were essential for the production of these nutrients, were no longer needed and were therefore lost over the generations, with the result that the pathogen specifically bound itself to its host [6].

Compromise for sexual recombination

Host-pathogen interactions have so far essentially been reduced to the interaction of two organisms with one another. It is becoming increasingly clear, however, that this reductionist picture can only be implemented to a limited extent, as diverse interactions with other organisms are possible in natural environments [7, 8]. In order to explain the development of new diseases, it is therefore important to understand the ecological context, in particular how they interact with other organisms.

As early as the 1950s it was described that rust fungi are able to suppress the immune defense of their host plant to such an extent that viruses that would otherwise not attack this plant are able to spread after being infected with rust. The same was also observed for initial infections with real powdery mildew fungi. Here it was even shown that they suppress the defense to such an extent that other real powdery mildew fungi, which are usually recognized and killed by the plant's immune system, could now infect and multiply. Since this is not only the case with biotrophic fungi, but also with biotrophic Oomycetes, it must be a general characteristic of this way of life (Fig. 4). Despite their very different origins from fungi, Oomycetes show comparable infection strategies, both in terms of the formation of haustoria and the formation of reproductive structures such as spores [6]. A very efficient suppression of the plant's immune defense could be demonstrated in particular for the white rust that often occurs on cultivated and wild plants. In nature, white rust therefore often occurs together with other oomycetes and fungi. Investigations also showed that white grilles also promote the growth of bacteria on the infected plant.