Gallocatechin biosynthesis via a flavonoid 3′,5′-hydroxylase is a defense response in Norway spruce against infection by the bark beetle-associated sap-staining fungus Endoconidiophora polonica

Abstract

One of the best-studied defense responses to fungal infection in Norway spruce (Picea abies) is the biosynthesis of flavan-3-ols, which accumulate as monomers or polymers known as proanthocyanidins. The individual flavan-3-ol units consist of compounds with a 3',4'-dihydroxylated B ring [2,3-(trans)-(+)-catechin or 2,3-(cis)-(-)-epicatechin] and compounds with a 3',4',5'-trihydroxylated B ring [2,3 (trans)-(+)-gallocatechin or 2,3-(cis)-(-)-epigallocatechin]. While much is known about the biosynthesis and biological activity of catechin in Norway spruce, there is little comparable information about gallocatechin or epigallocatechin. We found that there was a significant increase in the gallocatechin content of Norway spruce bark and wood after inoculation with the bark beetle-associated sap-staining fungus Endoconidiophora polonica. Gallocatechins increased proportionally more than catechins as both monomers and units of polymers. A flavonoid 3',5'-hydroxylase gene identified in Norway spruce was shown by heterologous expression in Nicotiana benthamiana to be involved in the conversion of 2,3 (trans)-(+)-catechin to 2,3 (trans)-(+)-gallocatechin. The formation of the trihydroxylated B ring in Norway spruce occurs at the level of flavan-3-ols, rather than at the level of dihydroflavonols as in many angiosperms. The transcript abundance of the flavonoid 3',5'-hydroxylase gene also increased significantly during fungal infection underlining its importance in gallocatechin biosynthesis. Comparisons of the effect of 2,3 (trans)-(+)-catechin and 2,3 (trans)-(+)-gallocatechin on fungal growth revealed that 2,3 (trans)-(+)-catechin is a stronger inhibitor of fungal growth, while 2,3 (trans)-(+)-gallocatechin is a stronger inhibitor of melanin biosynthesis.

Dual RNA-seq analysis provides new insights into interactions between Norway spruce and necrotrophic pathogen Heterobasidion annosum s.l.

“…The remaining ones are partial models and some of them could be in fact fragments of the same gene, thus the actual number of upregulated terpene synthases could be somewhat lower.

Fig. 2Scheme of the flavonoid biosynthesis pathway with the upstream steps of the phenypropanoid pathway and side branches leading to monolignols and stilbenoids (modified from Mellway et al [75] and Hammerbacher et al [44]). Components of the pathway showing higher transcript abundance in asymptomatic trees are boxed in pink, and the ones with higher abundance in symptomatic trees – in turquoise

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A fungal pathogen induces systemic susceptibility and systemic shifts in wheat metabolome and microbiome composition

“…10). Similarly to lignin precursors, flavonoid compounds as gallocatechin and kaempferol rhamnoside accumulate mainly in the resistant cultivar and are known to act as antimicrobials and antioxidants 25,35,46,47 . Accumulation of HCAAs is associated with resistance to various filamentous plant pathogens 23,24,27,48 .…”

Eyes on the future – evidence for trade‐offs between growth, storage and defense in Norway spruce

“…In Norway spruce, those phenolic (Hammerbacher et al ., , ) and monoterpene compounds (Martin et al ., ) have been shown to play an important role in defence against biotic attack. In addition, phenolic compounds (Neilson et al ., ) and volatile monoterpenes (Vickers et al ., ) are known to have antioxidant properties, therefore maybe required for reducing oxidative damage induced by excess electron transport under low [CO 2 ] (Galvez‐Valdivieso et al ., ).…”

“…growth and reproduction). Often SM fulfil important functions such as detoxification (Neilson et al ., ), anti‐herbivore (Mithöfer & Boland, ) and anti‐pathogen defense (Ullah et al ., ; Hammerbacher et al ., ). The biosynthesis of these compounds may be costly when resources are limited because they divert resources away from other sinks, such as growth.…”