Salicylic acid activates poplar defense against the biotrophic rust fungus Melampsora larici-populina via increased biosynthesis of catechin and proanthocyanidins

• Published in: The New phytologist 2019-01, Vol.221 (2), p.960-975
• Main Authors: Ullah, Chhana, Tsai, Chung-Jui, Unsicker, Sybille B., Xue, Liangjiao, Reichelt, Michael, Gershenzon, Jonathan, Hammerbacher, Almuth
• Format: Article
• Language: English
• Subjects: abscisic acid; Basidiomycota - physiology; benzothiadiazole (BTH); biosynthesis; catechin; Catechin - metabolism; chemical defense; condensed tannins; Cyclopentanes - metabolism; drought; drought stress; flavan-3-ols; Flavonoids - metabolism; Gene Expression Regulation, Plant; genes; genetic engineering; genetically modified organisms; hormones; immunity; jasmonic acid; leaf rust; leaves; Melampsora larici-populina; metabolites; Oxylipins - metabolism; phytohormones; Plant Diseases - immunology; Plant Diseases - microbiology; Plant Growth Regulators - metabolism; Plant Leaves - genetics; Plant Leaves - metabolism; Plant Leaves - microbiology; plant pathogenic fungi; Plant Sciences; Populus - genetics; Populus - immunology; Populus - microbiology; Populus nigra; proanthocyanidins; Proanthocyanidins - metabolism; salicylic acid; Salicylic Acid - metabolism; Signal Transduction; transcriptional activation; trees
• ISSN: 0028-646X; 1469-8137
• DOI: 10.1111/nph.15396

• Poplar trees synthesize flavan-3-ols (catechin and proanthocyanidins) as a defense against foliar rust fungi, but the regulation of this defense response is poorly understood. Here, we investigated the role of hormones in regulating flavan-3-ol accumulation in poplar during rust infection. • We profiled levels of defense hormones, signaling genes, and flavan-3-ol metabolites in black poplar leaves at different stages of rust infection. Hormone levels were manipulated by external sprays, genetic engineering, and drought to reveal their role in rust fungal defenses. • Levels of salicylic acid (SA), jasmonic acid, and abscisic acid increased in rust-infected leaves and activated downstream signaling, with SA levels correlating closely with those of flavan-3-ols. Pretreatment with the SA analog benzothiadiazole increased flavan-3-ol accumulation by activating the MYB–bHLH–WD40 complex and reduced rust proliferation. Furthermore, transgenic poplar lines overproducing SA exhibited higher amounts of flavan-3-ols constitutively via the same transcriptional activation mechanism. These findings suggest a strong association among SA, flavan-3-ol biosynthesis, and rust resistance in poplars. Abscisic acid also promoted poplar defense against rust infection, but likely through stomatal immunity independent of flavan-3-ols. Jasmonic acid did not confer any apparent defense responses to the fungal pathogen. • We conclude that SA activates flavan-3-ol biosynthesis in poplar against rust infection.