Fusarium graminearum Infection Strategy in Wheat Involves a Highly Conserved Genetic Program That Controls the Expression of a Core Effectome.

Florian Rocher,Géraldine Philippe,Ludovic Bonhomme,Tarek Alouane,Philippe Label,Marie-Laure Martin,Thierry Langin

doi:10.3390/ijms23031914

Abstract

Fusarium graminearum, the main causal agent of Fusarium Head Blight (FHB), is one of the most damaging pathogens in wheat. Because of the complex organization of wheat resistance to FHB, this pathosystem represents a relevant model to elucidate the molecular mechanisms underlying plant susceptibility and to identify their main drivers, the pathogen’s effectors. Although the F. graminearum catalog of effectors has been well characterized at the genome scale, in planta studies are needed to confirm their effective accumulation in host tissues and to identify their role during the infection process. Taking advantage of the genetic variability from both species, a RNAseq-based profiling of gene expression was performed during an infection time course using an aggressive F. graminearum strain facing five wheat cultivars of contrasting susceptibility as well as using three strains of contrasting aggressiveness infecting a single susceptible host. Genes coding for secreted proteins and exhibiting significant expression changes along infection progress were selected to identify the effector gene candidates. During its interaction with the five wheat cultivars, 476 effector genes were expressed by the aggressive strain, among which 91% were found in all the infected hosts. Considering three different strains infecting a single susceptible host, 761 effector genes were identified, among which 90% were systematically expressed in the three strains. We revealed a robust F. graminearum core effectome of 357 genes expressed in all the hosts and by all the strains that exhibited conserved expression patterns over time. Several wheat compartments were predicted to be targeted by these putative effectors including apoplast, nucleus, chloroplast and mitochondria. Taken together, our results shed light on a highly conserved parasite strategy. They led to the identification of reliable key fungal genes putatively involved in wheat susceptibility to F. graminearum, and provided valuable information about their putative targets.

Highlights

Introduction distributed under the terms andFusarium Head Blight (FHB), mainly caused by the Ascomycota fungus Fusarium graminearum, is one of the most prevalent diseases of small grain cereals, especially in wheat [1,2]
In the Pathogen Variability (PathoV) experiment, it corresponded to 3.5%, 8.6% and 22.6% of the assigned pairs at 48, 72 and 96 hpi, respectively (Supplementary Table S1B)
Taking advantage of different F. graminearum strains and wheat host cultivars, this study identified the in planta expression of 840 unique fungal genes harboring effectorassociated features, including nine new accessions not included in the reference

Summary

Introduction

Introduction distributed under the terms andFusarium Head Blight (FHB), mainly caused by the Ascomycota fungus Fusarium graminearum, is one of the most prevalent diseases of small grain cereals, especially in wheat [1,2]. For the last twenty years, the multiple evidences of the role of a plant’s susceptibility factors in promoting pathogen infection have opened new opportunities to identify such pivotal determinants of plant diseases, and a number of studies already reported that mutation or loss of susceptibility genes can be used in resistance breeding [16,17]. With the increasing evidences of the role of wheat’s susceptibility factors in FHB development [18,19,20,21,22,23], elucidating the mechanisms of wheat susceptibility to F. graminearum appears as a promising approach to improve FHB resistance [17,24,25,26]

Methods

Results

Discussion

Conclusion