A Common Fungal Associate of the Spruce Bark Beetle Metabolizes the Stilbene Defenses of Norway Spruce

Hammerbacher, Almuth; Schmidt, Axel; Wadke, Namita; Wright, Louwrance P.; Schneider, Bernd; Bohlmann, Jöerg; Brand, Willi A.; Fenning, T. M.; Gershenzon, Jonathan; Paetz, Christian

doi:10.1104/pp.113.218610

Cited by 139 publications

(142 citation statements)

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“…Thus, salicinoids are not likely to be deployed by poplar for pathogen defense. They might decline because of their metabolism by the fungus as a potential food source; the sugar moiety, in particular, could be cleaved and assimilated by the pathogen (Hammerbacher et al, 2013). A more likely explanation, however, is that lower levels of salicinoids in rust-infected leaves result from elevated flavan-3-ol biosynthesis, which was shown previously to reduce salicinoid biosynthesis.…”

Section: Discussionmentioning

confidence: 97%

Flavan-3-ols Are an Effective Chemical Defense against Rust Infection

et al. 2017

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Phenolic secondary metabolites are often thought to protect plants against attack by microbes, but their role in defense against pathogen infection in woody plants has not been investigated comprehensively. We studied the biosynthesis, occurrence, and antifungal activity of flavan-3-ols in black poplar (Populus nigra), which include both monomers, such as catechin, and oligomers, known as proanthocyanidins (PAs). We identified and biochemically characterized three leucoanthocyanidin reductases and two anthocyanidin reductases from P. nigra involved in catalyzing the last steps of flavan-3-ol biosynthesis, leading to the formation of catechin [2,3-trans-(+)-flavan-3-ol] and epicatechin [2,3-cis-(2)-flavan-3-ol], respectively. Poplar trees that were inoculated with the biotrophic rust fungus (Melampsora larici-populina) accumulated higher amounts of catechin and PAs than uninfected trees. The de novo-synthesized catechin and PAs in the rust-infected poplar leaves accumulated significantly at the site of fungal infection in the lower epidermis. In planta concentrations of these compounds strongly inhibited rust spore germination and reduced hyphal growth. Poplar genotypes with constitutively higher levels of catechin and PAs as well as hybrid aspen (Populus tremula 3 Populus alba) overexpressing the MYB134 transcription factor were more resistant to rust infection. Silencing PnMYB134, on the other hand, decreased flavan-3-ol biosynthesis and increased susceptibility to rust infection. Taken together, our data indicate that catechin and PAs are effective antifungal defenses in poplar against foliar rust infection.

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Section: Discussionmentioning

confidence: 97%

Flavan-3-ols Are an Effective Chemical Defense against Rust Infection

et al. 2017

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“…Stilbenes are assumed to provide protection against a wide variety of environmental stressors (Franceschi et al, 2005;Witzell and Martin, 2008;Chong et al, 2009). Stilbenes appear to contribute to antifungal defense in spruce (Hammerbacher et al, 2011(Hammerbacher et al, , 2013. The fungal inoculation of spruce bark with the blue-stain fungus Endoconidiophora polonica (previously named Ceratocystis polonica; de Beer et al, 2014) causes astringin levels to decrease, in parallel with increasing dimeric stilbene glucoside levels in the LMD-isolated axial phloem parenchyma (Li et al, 2012) or increasing levels of corresponding aglycons in bulk tissue (Viiri et al, 2001).…”

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In planta localization of stilbenes within Picea abies phloem

et al. 2016

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Phenolic stilbene glucosides (astringin, isorhapontin, and piceid) and their aglycons commonly accumulate in the phloem of Norway spruce (Picea abies). However, current knowledge about the localization and accumulation of stilbenes within plant tissues and cells remains limited. Here, we used an innovative combination of novel microanalytical techniques to evaluate stilbenes in a frozen-hydrated condition (i.e. in planta) and a freeze-dried condition across phloem tissues. Semiquantitative time-of-flight secondary ion-mass spectrometry imaging in planta revealed that stilbenes were localized in axial parenchyma cells. Quantitative gas chromatography analysis showed the highest stilbene content in the middle of collapsed phloem with decreases toward the outer phloem. The same trend was detected for soluble sugar and water contents. The specimen water content may affect stilbene composition; the glucoside-to-aglycon ratio decreased slightly with decreases in water content. Phloem chemistry was correlated with three-dimensional structures of phloem as analyzed by microtomography. The outer phloem was characterized by a high volume of empty parenchyma, reduced ray volume, and a large number of axial parenchyma with porous vacuolar contents. Increasing porosity from the inner to the outer phloem was related to decreasing compactness of stilbenes and possible secondary oxidation or polymerization. Our results indicate that aging-dependent changes in phloem may reduce cell functioning, which affects the capacity of the phloem to store water and sugar, and may reduce the defense potential of stilbenes in the axial parenchyma. Our results highlight the power of using a combination of techniques to evaluate tissue-and cell-level mechanisms involved in plant secondary metabolite formation and metabolism.

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“…Both terpenoids and phenolics are present at high concentrations in healthy spruce bark and also are synthesized de novo upon mechanical damage and fungal infection (Martin et al, 2002;Hammerbacher et al, 2011Hammerbacher et al, , 2014. Recently, astringin, a stilbene glycoside present in the concentric rows of phloem parenchyma cells, was shown to be catabolized by Endoconidiophora polonica (Hammerbacher et al, 2013). E. polonica (formerly known as Ceratocystis polonica; de Beer et al, 2014) is the most virulent blue-stain fungus transmitted by I. typographus (Krokene and Solheim, 1998).…”

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“…E. polonica (formerly known as Ceratocystis polonica; de Beer et al, 2014) is the most virulent blue-stain fungus transmitted by I. typographus (Krokene and Solheim, 1998). Although spruce trees still actively synthesize astringin in fungus-infected bark, a net loss of this compound occurs within the fungal lesions (Hammerbacher et al, 2013). This reduction in astringin was attributed to fungal biotransformation processes, including the formation of astringin dimers, aglycones, and ring-cleavage products with muconoid carbon skeletons, but specific genes or enzymes involved in these processes were not identified.…”

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Catechol dioxygenases catalyzing the first step in Norway spruce phenolic degradation are key virulence factors in the bark beetle-vectored fungus Endoconidiophora polonica

et al. 2016

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Norway spruce (Picea abies) is periodically attacked by the bark beetle Ips typographus and its fungal associate, Endoconidiophora polonica, whose infection is thought to be required for successful beetle attack. Norway spruce produces terpenoid resins and phenolics in response to fungal and bark beetle invasion. However, how the fungal associate copes with these chemical defenses is still unclear. In this study, we investigated changes in the phenolic content of Norway spruce bark upon E. polonica infection and the biochemical factors mediating these changes. Although genes encoding the rate-limiting enzymes in Norway spruce stilbene and flavonoid biosynthesis were actively transcribed during fungal infection, there was a significant time-dependent decline of the corresponding metabolites in fungal lesions. In vitro feeding experiments with pure phenolics revealed that E. polonica transforms both stilbenes and flavonoids to muconoid-type ring-cleavage products, which are likely the first steps in the degradation of spruce defenses to substrates that can enter the tricarboxylic acid cycle. Four genes were identified in E. polonica that encode catechol dioxygenases carrying out these reactions. These enzymes catalyze the cleavage of phenolic rings with a vicinal dihydroxyl group to muconoid products accepting a wide range of Norway spruce-produced phenolics as substrates. The expression of these genes and E. polonica utilization of the most abundant spruce phenolics as carbon sources both correlated positively with fungal virulence in several strains. Thus, the pathways for the degradation of phenolic compounds in E. polonica, initiated by catechol dioxygenase action, are important to the infection, growth, and survival of this bark beetle-vectored fungus and may play a major role in the ability of I. typographus to colonize spruce trees.

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A Common Fungal Associate of the Spruce Bark Beetle Metabolizes the Stilbene Defenses of Norway Spruce

Cited by 139 publications

References 51 publications

Flavan-3-ols Are an Effective Chemical Defense against Rust Infection

Flavan-3-ols Are an Effective Chemical Defense against Rust Infection

In planta localization of stilbenes within Picea abies phloem

Catechol dioxygenases catalyzing the first step in Norway spruce phenolic degradation are key virulence factors in the bark beetle-vectored fungus Endoconidiophora polonica

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