Metabolic Counteradaptation of Plant Pathogens to Chemical Defenses in Trees

Dr. Almuth Hammerbacher

Plants synthesize many different toxic secondary metabolites as an immune response against fungal and bacterial pathogens. Although this defense strategy is often successful in avoiding plant disease, some pathogens have special adaptations enabling them to overcome the toxic effects of secondary metabolites.
Tree species produce an impressive array of polyphenolics to defend themselves against pathogen attack. These complex aromatic compounds are thought to inhibit microorganism development in many different ways. However, despite increased biosynthesis of some of these toxic defense compounds in response to infection by pathogens, trees are often colonized by disease-causing organisms which seem well adapted to polyphenols.
Our study system focuses on the adaptations of blue stain fungi (order Ophiostomatales) infecting woody hosts. We have already shown that some of these fungi have special metabolic pathways for the degradation of polyphenols produced by their hosts as defense compounds. Our work revealed that degradation of host defense compounds is sometimes a prerequisite for successful colonization of the host and shows a high correlation with pathogenicity in the blue stain fungus Ceratocystis polonica infecting Norway spruce (Picea abies). These observations suggest that the metabolic adaptations of pathogens to their host’s chemistry are much more important in plant-pathogen interactions than has been hitherto recognized.

Blue stain fungi often have a close association with eruptive bark beetle species from the subfamily Scolytinae. These insects, which can devastate large tracts of forest during a single season, transmit blue stain fungi from tree to tree. Although it is thought that the fungus-beetle relationship is mutually beneficial to both partners, it is still unknown how bark beetles benefit from blue stain fungi.
In our research we are using an integrative approach for studying adaptation of blue stain fungi to woody hosts by examining both polyphenol biosynthesis in hosts as well as polyphenol catabolism in blue-stain fungi. We are also investigating how these processes affect the life cycle of a bark beetle species. By understanding the biological system underlying eruptive bark beetle outbreaks we hope to find long-term, sustainable solutions to diminish economic losses suffered in commercial agro-forestry due to bark beetle epidemics.


The evolution of fungal adaptations to host defense compounds

Dr. Almuth Hammerbacher

Blue stain fungal species can infect a wide range of gymnosperm as well as angiosperm tree species from the families Pinaceae, Fabaceae, Myrtaceae, Malvaceae, Juglandaceae Rubiaceae and many others. These host trees synthesize an elaborate array of polyphenolic defense compounds including many different flavonoids, stilbenes, coumarins, phenolic acids, lignans, condensed and hydrolysable tannins. The goal of this research is to study polyphenol biosynthesis in different host species in response to blue stain fungi. Concurrently detoxification and degradation strategies of these phenolics by blue stain fungi will be studied. By understanding how blue stain fungi circumvent host defenses, polyphenol biosynthesis pathways in economically important tree species can be manipulated in order to maximize their efficiency in the defense against these pathogens.

The interaction between blue stain fungi and their associated bark beetle

Dineshkumar Kandasamy

Blue stain fungi often have a close association with eruptive bark beetle species which transmit them from tree to tree. However, not much is known about the biology underlying these associations since transmitting the fungus has no obvious benefit for beetles. The bark beetle-fungus association might therefore be commensal, where the fungus has developed special strategies for attaching itself to the bark beetle life cycle without affecting the bark beetle. An alternative to commensalism might be a mutualistic interaction where both partners benefit from an association. I am exploring both scenarios in C. polonica which is transmitted by the bark beetle Ips typogtaphus using chemical, molecular, proteomic and biochemical tools. As blue-stain fungi live in close proximity to bark beetle larvae in the host, one main goal is to elucidate if fungal degradation of tree defense chemicals leads to an increase in nutritive value of substrates for bark beetles. As many steps in the polyphenol degradation pathways in C. polonica are still unknown, I propose to elucidate these polyphenol degradation pathways of C. polonica by using classical chemical and biochemical methods as well as molecular tools. By studying and comparing the different catabolic strategies for polyphenol degradation in C. polonica as well as the enzymes responsible we will increase our understanding of fungal as well as bark beetle success in woody hosts.

Plant-pathogen interactions between black poplar (Populus nigra) and the biotrophic poplar rust Melampsora larici-populina

Chhana Ullah

Black poplar is a tree species native to Germany which is often infected by the biotrophic poplar rust (Melampsora larici-populina). In their leaves and bark, poplars synthesize high quantities of polyphenolic metabolites, including proanthocyanidins, flavonoids and salicinoids. Although similar compounds are present in many other woody plant species, their benefit in defense against pathogens of different types and their metabolic costs are still poorly understood. We could show that black poplar responds to rust infection by the synthesis of polyphenolic metabolites thought to be important in plant defense against necotrophic fungal pathogens with herbaceous hosts. The goal of this research is therefore to understand (1) the role of polyphenol biosynthesis in poplar defense against rust infection (2) the biosynthetic pathways involved in polyphenol biosynthesis, and (3) the adaptations of poplar rust to polyphenol defenses.

This project is in collaboration with Dr. Sybille Unsicker

Catabolism of flavonols in Arabidopsis thaliana by Sclerotinia sclerotiorum

Jingyuan Chen

Flavonoids are widely distributed in nature and many studies have revealed that some flavonoids have antibiotic activity against fungal plant infection. Fungi can however also produce enzymes that metabolize and detoxify these plant chemical defenses. The phytopathogenic fungus Sclerotinia sclerotiorum is a devastating necrotrophic pathogen that can cause stem rot disease in a vast range of plant species and results in large losses of crop yields worldwide. In order to determine how A. thaliana interacts with S. sclerotiorum, changes in the levels of defense compounds (glucosinolates, flavonoids, camalexin and coumaroyl agmatine) in A. thaliana was investigated. HPLC analyses showed that the concentration of total flavonoids in A. thaliana inoculated with aggressive strains UF-70 decreased significantly 3 days post inoculation when compared with mock inoculated A. thaliana. The result suggested that S. sclerotiorum may have a strategy to block accumulation of flavonoids in host plant. An in vitro growth experiment with artificial medium containing different phenolic compounds showed that S. sclerotiorum can degrade the flavonoids quercetin and kaempferol more quickly than other defense metabolites. Therefore the gene encoding an enzyme involved in degradation of quercetin and kaempferol, in S. sclerotiorum was identified. In order to investigate the role of this gene in fungal virulence, a knock-out mutant was generated based on wild type UF-70. The ability to degrade phenolics in the mutant was impaired but the growth rate of mycelium was not affected. In vitro inoculated Arabidopsis leaves showed that the mutant strain was less virulent than the WT. Defense compound degradation in A. thaliana is now further studied which will allow more insights into the importance of such processes in virulence and survival of S. sclerotiorum.