Overexpression of a Cytochrome P450 Monooxygenase Involved in Orobanchol Biosynthesis Increases Susceptibility to Fusarium Head Blight

Valentin Changenet,Catherine Macadré,Marie Dufresne,Kévin Magne,Marion Dalmais,Grégory Mouille,Stéphanie Boutet-Mercey,Abdelhafid Bendahmane,Mélanie Januario

doi:10.3389/fpls.2021.662025

Abstract

Fusarium Head Blight (FHB) is a cereal disease caused primarily by the ascomycete fungus Fusarium graminearum with public health issues due to the production of mycotoxins including deoxynivalenol (DON). Genetic resistance is an efficient protection means and numerous quantitative trait loci have been identified, some of them related to the production of resistance metabolites. In this study, we have functionally characterized the Brachypodium distachyon BdCYP711A29 gene encoding a cytochrome P450 monooxygenase (CYP). We showed that BdCYP711A29 belongs to an oligogenic family of five members. However, following infection by F. graminearum, BdCYP711A29 is the only copy strongly transcriptionally induced in a DON-dependent manner. The BdCYP711A29 protein is homologous to the Arabidopsis thaliana MAX1 and Oryza sativa MAX1-like CYPs representing key components of the strigolactone biosynthesis. We show that BdCYP711A29 is likely involved in orobanchol biosynthesis. Alteration of the BdCYP711A29 sequence or expression alone does not modify plant architecture, most likely because of functional redundancy with the other copies. B. distachyon lines overexpressing BdCYP711A29 exhibit an increased susceptibility to F. graminearum, although no significant changes in defense gene expression were detected. We demonstrate that both orobanchol and exudates of Bd711A29 overexpressing lines stimulate the germination of F. graminearum macroconidia. We therefore hypothesize that orobanchol is a susceptibility factor to FHB.

Highlights

Fusarium Head Blight (FHB) is a major disease of small-grain cereals, including wheat (Dweba et al, 2017; Figueroa et al, 2017; Duba et al, 2018)
The Bradi1g75310 Gene Belongs to an Oligogenic Family Homologous to the Arabidopsis MAX1 Gene and Is Induced Under F. graminearum Infection in a DON-Dependent Manner
A previous study has identified Bradi1g75310 as a gene induced by a DON-producing F. graminearum [FgDON+, 6.93 fold log2 compared to the mock condition 96 hours post inoculation] while it does not respond to a mutant strain unable to produce the mycotoxin [FgDON−, 0.77 fold log2 compared to the mock condition (96 hpi); Pasquet et al, 2014]

Summary

Introduction

Fusarium Head Blight (FHB) is a major disease of small-grain cereals, including wheat (Dweba et al, 2017; Figueroa et al, 2017; Duba et al, 2018). Cereals protection toward FHB has for a long time relied on chemicals mainly belonging to the demethylation inhibitors (DMI) family, none confers full protection against the disease (Yuen and Schoneweis, 2007; Dweba et al, 2017; Chen et al, 2019). Numerous large-scale studies have been performed to decipher the biological functions associated with resistance to FHB These were designed to identify either differentially expressed genes (DEGs; for a review, see Kazan and Gardiner, 2017) or differentially produced metabolites (Kumaraswamy et al, 2011; Gunnaiah et al, 2012; Gauthier et al, 2015) related to quantitative resistance. These results could not be properly compared due to diverse host genetic backgrounds, they allowed the identification of resistancerelated families of secondary metabolites: phenylpropanoids reinforcing cell walls or scavenging reactive oxygen species, lignins, and lignans involved in cell wall thickness, polyamines strengthening physical barriers through their ability to bind cell wall components, terpenoids often having antimicrobial activities, and fatty acids which oxidation products can lead among others to jasmonate (JA) precursors (Bollina et al, 2010, 2011; Kumaraswamy et al, 2011; Kushalappa and Gunnaiah, 2013; Gunnaiah and Kushalappa, 2014; Kage et al, 2017; Karre et al, 2017)

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