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Synergies and trade-offs between insect and pathogen resistance in maize leaves and roots

2011, Erb, Matthias, Balmer, Yves, de Lange, Elvira S., von Merey, Georg, Planchamp, Chantal, Robert, Christelle Aurélie Maud, Röder, Gregory, Sobhy, Islam, Zwahlen, Claudia, Mauch-Mani, Brigitte, Turlings, Ted

Determining links between plant defence strategies is important to understand plant evolution and to optimize crop breeding strategies. Although several examples of synergies and trade-offs between defence traits are known for plants that are under attack by multiple organisms, few studies have attempted to measure correlations of defensive strategies using specific single attackers. Such links are hard to detect in natural populations because they are inherently confounded by the evolutionary history of different ecotypes. We therefore used a range of 20 maize inbred lines with considerable differences in resistance traits to determine if correlations exist between leaf and root resistance against pathogens and insects. Aboveground resistance against insects was positively correlated with the plant's capacity to produce volatiles in response to insect attack. Resistance to herbivores and resistance to a pathogen, on the other hand, were negatively correlated. Our results also give first insights into the intraspecific variability of root volatiles release in maize and its positive correlation with leaf volatile production. We show that the breeding history of the different genotypes (dent versus flint) has influenced several defensive parameters. Taken together, our study demonstrates the importance of genetically determined synergies and trade-offs for plant resistance against insects and pathogens.

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Fungal Infection Reduces Herbivore-Induced Plant Volatiles of Maize but does not Affect Naïve Parasitoids

2006, Rostás, Michael, Ton, Jurriaan, Mauch-Mani, Brigitte, Turlings, Ted

Plants attacked by insects release volatile compounds that attract the herbivores' natural enemies. This so-called indirect defense is plastic and may be affected by an array of biotic and abiotic factors. We investigated the effect of fungal infection as a biotic stress agent on the emission of herbivore-induced volatiles and the possible consequences for the attraction of two parasitoid species. Maize seedlings that were simultaneously attacked by the fungus Setosphaeria turcica and larvae of Spodoptera littoralis emitted a blend of volatiles that was qualitatively similar to the blend emitted by maize that was damaged by only the herbivore, but there was a clear quantitative difference. When simultaneously challenged by fungus and herbivore, the maize plants emitted in total 47% less of the volatiles. Emissions of green leaf volatiles were unaffected. In a six-arm olfactometer, the parasitoids Cotesia marginiventris and Microplitis rufiventris responded equally well to odors of herbivore-damaged and fungus- and herbivore-damaged maize plants. Healthy and fungus-infected plants were not attractive. An additional experiment showed that the performance of S. littoralis caterpillars was not affected by the presence of the pathogen, nor was there an effect on larvae of M. rufiventris developing inside the caterpillars. Our results confirm previous indications that naïve wasps may respond primarily to the green leaf volatiles.

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Above- and belowground antifungal resistance in maize: aspects of organ-specific defense

, Balmer, Dirk, Mauch-Mani, Brigitte

The hemibiotrophic fungus Colletotrichum graminicola causes devastating anthracnose on maize (Zea mays) and is responsible for annual losses of up to 1 billion dollars in the U.S. A key factor for its success is the capability to infect different plant organs. The predominant symptoms are leaf blight and stalk rot, but C. graminicola also infects roots. The vast majority of phytopathological studies were conducted on aerial disease stages, and only little is known about belowground defense responses. Moreover, most studies on antifungal resistance focus on either above- or belowground immune systems. Thus, this thesis investigated the local and systemic organ-specific interactions of maize and C. graminicola.
Firstly, a soil-free plant growth system was developed, allowing non-destructive in vivo observations of C. graminicola infection strategies on maize roots. This system consists of pouches containing nutrient-soaked filter paperwhich supplies the plants with nutrients adapted to the host.
Secondly, local and systemic molecular and chemical changes upon C. graminicola attack on maize leaves and roots were investigated. Distinct gene expression patterns in leaves and roots were found, in agreement with different dynamics of phytohormone induction. In roots defense-related genes were induced faster than in leaves, and roots also exhibited higher hormone levels upon infection. Local leaf and root infections triggered leaf-leaf and root-leaf systemic transcriptional and hormonal adaptations, including the induction of defense-related genes and hormones. Interestingly, local leaf and root infection also resulted in a systemic resistance against C. graminicola in distal leaves. Performing metabolomic fingerprinting, several local and systemic organ-specific compounds were identified, which could serve as chemical arsenal during antifungal immunity in maize.
Thirdly, the organ-specific microRNA (miRNA) transcriptome of maize during C. graminicola infection was examined. Several miRNAs were identified which are specifically induced or downregulated in fungal infected shoots or roots, but not upon challenge with the herbivore Spodoptera frugiperda. Some of those miRNAs target defense-related genes, thus miRNAs might play an important role in organ-specific antifungal defense.
In conclusion, exploiting organ-specific plant defense might be a prominent target for future crop enhancing programs.