Strigolactone deficiency induces jasmonate, sugar and flavonoid phytoalexin accumulation enhancing rice defense against the blast fungus Pyricularia oryzae

• Published in: The New phytologist 2024-01, Vol.241 (2), p.827-844
• Main Authors: Lahari, Zobaida, Boerdonk, Sarah, Omoboye, Olumide Owolabi, Reichelt, Michael, Höfte, Monica, Gershenzon, Jonathan, Gheysen, Godelieve, Ullah, Chhana
• Format: Article
• Language: English
• Subjects: Accumulation; Biosynthesis; Carotenoids; flavonoid phytoalexins; Flavonoids; Flavonoids - metabolism; Fungi; glucose; Isoleucine; Jasmonic acid; Magnaporthe - physiology; Magnaporthe oryzae; Microorganisms; Mutants; Oryza - metabolism; Oryza sativa; Pathogens; Phytoalexins; Phytohormones; plant defense signaling; Plant Diseases - microbiology; Plant growth; Plant growth substances; Plant hormones; Plants; plant–pathogen interactions; Pyricularia oryzae; rac‐GR24; Rice; Rice blast; RNA-mediated interference; Saccharides; Seedlings; Sucrose; Sugar; Sugars - metabolism; Symbiosis
• ISSN: 0028-646X; 1469-8137
• DOI: 10.1111/nph.19354

Summary Strigolactones (SLs) are carotenoid‐derived phytohormones that regulate plant growth and development. While root‐secreted SLs are well‐known to facilitate plant symbiosis with beneficial microbes, the role of SLs in plant interactions with pathogenic microbes remains largely unexplored. Using genetic and biochemical approaches, we demonstrate a negative role of SLs in rice (Oryza sativa) defense against the blast fungus Pyricularia oryzae (syn. Magnaporthe oryzae). We found that SL biosynthesis and perception mutants, and wild‐type (WT) plants after chemical inhibition of SLs, were less susceptible to P. oryzae. Strigolactone deficiency also resulted in a higher accumulation of jasmonates, soluble sugars and flavonoid phytoalexins in rice leaves. Likewise, in response to P. oryzae infection, SL signaling was downregulated, while jasmonate and sugar content increased markedly. The jar1 mutant unable to synthesize jasmonoyl‐l‐isoleucine, and the coi1‐18 RNAi line perturbed in jasmonate signaling, both accumulated lower levels of sugars. However, when WT seedlings were sprayed with glucose or sucrose, jasmonate accumulation increased, suggesting a reciprocal positive interplay between jasmonates and sugars. Finally, we showed that functional jasmonate signaling is necessary for SL deficiency to induce rice defense against P. oryzae. We conclude that a reduction in rice SL content reduces P. oryzae susceptibility by activating jasmonate and sugar signaling pathways, and flavonoid phytoalexin accumulation.