Comparative Genomics of Eight Fusarium graminearum Strains with Contrasting Aggressiveness Reveals an Expanded Open Pangenome and Extended Effector Content Signatures

Abstract

Fusarium graminearum, the primary cause of Fusarium head blight (FHB) in small-grain cereals, demonstrates remarkably variable levels of aggressiveness in its host, producing different infection dynamics and contrasted symptom severity. While the secreted proteins, including effectors, are thought to be one of the essential components of aggressiveness, our knowledge of the intra-species genomic diversity of F. graminearum is still limited. In this work, we sequenced eight European F. graminearum strains of contrasting aggressiveness to characterize their respective genome structure, their gene content and to delineate their specificities. By combining the available sequences of 12 other F. graminearum strains, we outlined a reference pangenome that expands the repertoire of the known genes in the reference PH-1 genome by 32%, including nearly 21,000 non-redundant sequences and gathering a common base of 9250 conserved core-genes. More than 1000 genes with high non-synonymous mutation rates may be under diverse selection, especially regarding the trichothecene biosynthesis gene cluster. About 900 secreted protein clusters (SPCs) have been described. Mostly localized in the fast sub-genome of F. graminearum supposed to evolve rapidly to promote adaptation and rapid responses to the host’s infection, these SPCs gather a range of putative proteinaceous effectors systematically found in the core secretome, with the chloroplast and the plant nucleus as the main predicted targets in the host cell. This work describes new knowledge on the intra-species diversity in F. graminearum and emphasizes putative determinants of aggressiveness, providing a wealth of new candidate genes potentially involved in the Fusarium head blight disease.

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

“…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 (i.e., genes encoding secreted proteins and differentially expressed during the FHB infection), including nine new accessions not included in the reference PH-1 genome. These represent almost 5% of F. graminearum pangenome and more than 35% of its putative pansecretome [49].…”

“…Because previous comparative genomic studies demonstrated that F. graminearum putative pathogenicity-related genes were located in variable regions of the genome [49,54,55], the distribution of our core effectome on F. graminearum genome was studied (Supplementary Table S4). At both inter-and intrachromosomal level, spatial distribution of the core effector genes was uneven (Figure S3).…”

“…In Fusarium graminearum, genomics variability has been well characterized and the first pangenome of the species, built from 20 strains, was published in 2021 [49]. If the in silico characterization of F. graminearum secretome [49,50] is now available, our knowledge about the effective in planta effectome remains fragmented and needs to be clarified.…”

“…In Fusarium graminearum, genomics variability has been well characterized and the first pangenome of the species, built from 20 strains, was published in 2021 [49]. If the in silico characterization of F. graminearum secretome [49,50] is now available, our knowledge about the effective in planta effectome remains fragmented and needs to be clarified. Several in planta studies outlined a highly dynamic and complex molecular dialogue between wheat and F. graminearum, involving a stage-specific delivery of the effectors [19,25,51,52].…”

Distribution, Function, and Evolution of a Gene Essential for Trichothecene Toxin Biosynthesis in Trichoderma

“…The results of the current study also provide evidence for positive selection of the ancestral Trichoderma tri5 during its divergence from tri5 in other fungi ( Figures 4 , 5 ). There is evidence for positive selection of other secondary metabolite biosynthetic genes in fungi ( Massonnet et al, 2018 ; Alouane et al, 2021 ). In these other fungi, the selection was attributed to adaptation to environmental changes.…”