Hordedane diterpenoid phytoalexins restrict Fusarium graminearum infection but enhance the colonization by Bipolaris sorkiniana of barley roots

Abstract

Plant immunity is a multi-layered process that includes recognition of patterns or effectors from pathogens to elicit defense responses. These include the induction of a cocktail of defense metabolites that typically restrict pathogen virulence. Here, we investigate the interaction between barley roots and the fungal pathogens Bipolaris sorokiniana (Bs) and Fusarium graminearum (Fg) at the metabolite level. We identify hordedanes, a previously undescribed set of labdane- related diterpenoids with antimicrobial properties, as critical players in these interactions. Infection of barley roots by Bs and Fg elicits hordedane synthesis from a 600-kb gene cluster. Heterologous reconstruction of the biosynthesis pathway in yeast and Nicotiana benthamiana produced several hordedanes, including one of the most functionally decorated products 19-β-hydroxy- hordetrienoic acid (19-OH-HTA). Barley mutants in the diterpene synthase genes of the cluster are unable to produce hordedanes but, unexpectedly, show reduced Bs colonization. By contrast, colonization by Fusarium graminearum, another fungal pathogen of barley and wheat, is four-fold higher in mutants completely lacking hordedanes. Accordingly, 19-OH-HTA enhances both germination and growth of Bs, while it inhibits other pathogenic fungi, including Fg. Microscopy and transcriptomics suggest hordedanes delay the necrotrophic phase of Bs. Our data show that adapted pathogens such as Bs can subvert plant metabolic defenses to facilitate root colonization.