Suboptimal pre-anthesis water status mitigates wheat susceptibility to fusarium head blight and triggers specific metabolic responses

Abstract

The impact of abiotic challenges on plant physiology reshapes plant-pathogen interactions by modulating the plant immune responses. In wheat, the development of Fusarium Head Blight (FHB) is heavily influenced by environmental conditions, especially during the pre-anthesis stage, just before fungal infection occurs. The early stages of infection are thus likely conditioned by prior environmental changes with consequences on the disease outcome that require further characterization. In this study, we aimed to assess the impact of pre-anthesis water depletion followed by rapid rehydration at inoculation on the expression of FHB-related molecular determinants with emphasis on susceptibility factors and metabolism-related processes. Water depletion altered plant physiology and its effects remained detectable after three days after rehydration, leading to significantly reduced FHB symptoms. Dual-transcriptomics, combined with untargeted metabolomics, revealed two key findings including (i) extensive metabolic changes specific to prior water stress, and (ii) the strong conservation of previously identified candidate susceptibility genes regulation. Considering the combined stress effects, a unique response signature emerged, highlighting that immune responses are strongly interwoven with physiological adjustments. Our findings provide new insights into the trade-offs that plants make under multiple challenges and identify original wheat metabolic determinants that may improve FHB resistance even in suboptimal physiological conditions.

Keywords: Bread wheat; FHB susceptibility; Multi-stress genomics; Specialized metabolism; Water stress.

Fig. 1

Experimental design and contrasts of interest that were considered in the statistic model for transcriptomic and metabolomic data analysis. FHB stands for Fusarium head blight.

Fig. 2

Characterization of water depletion and FHB development during experimentation. (a) Mean field capacity loading measured during the twelve days preceding mid-anthesis and over the 7 following days. Values are represented with standard errors for well-watered condition (dark blue lines) and for water limited condition (light blue lines). (b) Box plot of photosystem II yields measured in flag leaves at mid-day for mock (dark lines) and F. graminearum infected (grey lines) plants. Values are shown at 3 days post inoculation for plants submitted to both water regimes. P-value originates from Tukey’s Honestly Significant Difference test. (c) Evolution of mean symptom scores and their standard errors following infection with the MDC_Fg1 strain under well-watered conditions and pre-anthesis water limited conditions.

Fig. 3

Upset plots showing the number of differentially-expressed genes (DEG) and differentially-accumulated metabolites (DAM) observed following pre-anthesis water depletion in healthy plants (PWD effect), Fusarium Head Blight infection of well-watered plants (FHB effect after WW), FHB infection effect after pre-anthesis water depletion (FHB effect after PWD) and effects of cumulative PWD and FHB effects compared to well-watered healthy plants (cumulative effect). (a) Plots are given for all differentially expressed genes and for a narrowed set of genes annotated to GO:0008152 “metabolic process” and daughter GeneOntology (GO) terms as well as for (b) metabolomic features. Upset plots were created according to the intersections between DEGs of focal contrasts.

Fig. 4

Heat maps of the expression patterns of differentially expressed metabolism-related genes (DEmGs) and differentially accumulated metabolites (DAMs). (a) Elements responding generically to Fusarium Head Blight (FHB), i.e. evidenced in FHB effect after well watered (WW) conditions, in FHB effect after pre-anthesis water depletion (PWD) and in cumulative effect; (b) responding specifically to FHB after WW; (c) responding specifically to FHB after PWD and (d) responding specifically to cumulative effects of PWD and FHB infection. Colors represent z-scores of normalized counts from DiCoExpress. Red dot on the top right of each heat map refer to the groups of the Upset plots in Fig. 3.

Fig. 5

Bar plots representing distribution of functional annotations of pre-anthesis water depletion (PWD) and Fusarium Head Blight (FHB) responsive elements. (a) GeneOntology (GO) annotations of differentially expressed metabolism-related genes (DEmGs) and (b) metabolite annotation to NP Classifier pathways of the former identified differentially accumulated metabolites (DAMs). Visual representations correspond to the number of FHB generic (black bar) and specific responsive elements (FHB effect after WW, FHB effect after PWD (grey bars) and for cumulative effects of PWD and FHB).

Fig. 6

Heat maps of the expression patterns of genes related to Fusarium Head Blight (FHB) susceptibility retrieved from the study of Rocher et al.. (a) Known FHB susceptibility factors and (b) master regulators of FHB response network.