Proteomics-Based Data Integration of Wheat Cultivars Facing Fusarium graminearum Strains Revealed a Core-Responsive Pattern Controlling Fusarium Head Blight

Abstract

Fusarium head blight (FHB), mainly occurring upon Fusarium graminearum infection in a wide variety of small-grain cereals, is supposed to be controlled by a range of processes diverted by the fungal pathogen, the so-called susceptibility factors. As a mean to provide relevant information about the molecular events involved in FHB susceptibility in bread wheat, we studied an extensive proteome of more than 7,900 identified wheat proteins in three cultivars of contrasting susceptibilities during their interaction with three F. graminearum strains of different aggressiveness. No cultivar-specific proteins discriminated the three wheat genotypes, demonstrating the establishment of a core proteome regardless of unequivocal FHB susceptibility differences. Quantitative protein analysis revealed that most of the FHB-induced molecular adjustments were shared by wheat cultivars and occurred independently of the F. graminearum strain aggressiveness. Although subtle abundance changes evidenced genotype-dependent responses to FHB, cultivar distinction was found to be mainly due to basal abundance differences, especially regarding the chloroplast functions. Integrating these data with previous proteome mapping of the three F. graminearum strains facing the three same wheat cultivars, we demonstrated strong correlations between the wheat protein abundance changes and the adjustments of fungal proteins supposed to interfere with host molecular functions. Together, these results provide a resourceful dataset that expands our understanding of the specific molecular events taking place during the wheat–F. graminearum interaction.

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

“…The prediction of their subcellular localization in the host cell demonstrated that the chloroplast could be a primary target of F. graminearum effectors, followed by the plant nucleus. Although functional characterizations of these proteins might be necessary to identify their intracellular localization and their role in the infection process, this clearly corroborates previous dual-proteomics on the FHB disease in bread wheat that identified a close relationship between chloroplast adjustments and the accumulation of F. graminearum proteins harboring the features of a chloroplast transit peptide [17,56,78]. Among SPCs with known functions, more than 70% are closely linked to plant/pathogen interaction and pathogenicity, including CAZymes, proteases and PHI genes.…”

“…These represented a total of 18 spikelets per plant (90 measurements per strain) that were individually scored for the symptom dynamics at 72 h after the inoculation (hpi). This duration was chosen on the basis of our previous studies [17,56,78] demonstrating a turning point in the FHB progress at this time, enabling to discriminate strains of contrasted aggressiveness. Along with the forty infected plants, five additional ones were inoculated with water and were used as a control, and no symptoms were observed on these plants.…”

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

“…The search for localization signals within the F. graminearum secreted protein sequences revealed that putative effectors can target host apoplast, as well as different subcellular compartments including nucleus, chloroplast and mitochondria at several infection stages (Figure 7). Along with the relatively high diversity of predicted functions (66 GO terms and 140 Pfam), this supports that the infection success is based on a wide array of manipulated host pathways and echoes previous studies that evidenced the diverse nature of processes involved in FHB susceptibility [19,20,23].…”

“…The inhibition of the defense mechanisms through the manipulation of chloroplast [76] and mitochondrial [77] processes was already evidenced in several plant-fungi interactions and proved here to be part of the F. graminearum infection strategy. In the case of the chloroplast, its central role has already been described in previous FHB studies [19,20,23]. Finally, effectors with multiple host targets were also detected, suggesting that one effector can achieve completely different functions during the infection progress.…”

“…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].…”