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Abstract

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 comprehensively investigated. We studied the biosynthesis, occurrence and anti-fungal activity of flavan-3-ols in black poplar (Populus nigra L.), which include both monomers, such as catechin, and oligomers known as proanthocyanidins (PAs). We identified and biochemically characterized three leucoanthocyanidin reductases (LAR) and two anthocyanidin reductases (ANR) 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-(-)-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 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 anti-fungal defenses in poplar against foliar rust infection.