Joint Transcriptomic and Metabolomic Analyses Reveal Changes in the Primary Metabolism and Imbalances in the Subgenome Orchestration in the Bread Wheat Molecular Response toFusarium graminearum

Abstract

Fusarium head blight is a prevalent disease of bread wheat (Triticum aestivum L.), which leads to considerable losses in yield and quality. Quantitative resistance to the causative fungus Fusarium graminearum is poorly understood. We integrated transcriptomics and metabolomics data to dissect the molecular response to the fungus and its main virulence factor, the toxin deoxynivalenol in near-isogenic lines segregating for two resistance quantitative trait loci, Fhb1 and Qfhs.ifa-5A. The data sets portrait rearrangements in the primary metabolism and the translational machinery to counter the fungus and the effects of the toxin and highlight distinct changes in the metabolism of glutamate in lines carrying Qfhs.ifa-5A. These observations are possibly due to the activity of two amino acid permeases located in the quantitative trait locus confidence interval, which may contribute to increased pathogen endurance. Mapping to the highly resolved region of Fhb1 reduced the list of candidates to few genes that are specifically expressed in presence of the quantitative trait loci and in response to the pathogen, which include a receptor-like protein kinase, a protein kinase, and an E3 ubiquitin-protein ligase. On a genome-scale level, the individual subgenomes of hexaploid wheat contribute differentially to defense. In particular, the D subgenome exhibited a pronounced response to the pathogen and contributed significantly to the overall defense response.

The defence‐associated transcriptome of hexaploid wheat displays homoeolog expression and induction bias

“…Global observation of expression patterns revealed that homoeolog expression bias underpins a substantial proportion of the wheat transcriptome under both basal growth conditions and increasingly so during infection. Recent work has demonstrated the D subgenome contributes disproportionately to the transcriptional response during infection by Fusarium graminearum suggesting the D genome may play a predominant role in responding to this pathogen (Nussbaumer et al ., ). Contribution of homoeolog expression was found to be significantly biased towards B and D subgenomes under both mock and infection conditions consistent with previous findings.…”

Time‐course expression QTL‐atlas of the global transcriptional response of wheat to Fusarium graminearum

“…We could confirm this in detail by comparing our findings to the published data from Nussbaumer et al . (): Wherein photosynthesis‐related genes (GO:0015979) are less expressed in response to the pathogen compared to mock, while this effect was stronger in the susceptible genotypes.…”

“…The spectrum of resistant responses is mainly categorized in resistance against initial penetration of the pathogen (type I) and resistance against spreading of the disease (type II) (Schroeder and Christensen, ). The complex nature of the underlying resistance mechanisms has been investigated in transcriptomic studies in near‐isogenic material (Hofstad et al ., ; Nussbaumer et al ., ) but not on the population level: After infection F. graminearum commences with a biotrophic life style but switches to necrotrophy after roughly 48 h. This switch is set off or followed by the production of high amounts of the trichothecene toxin deoxynivalenol (DON) that elicits oxidative stress and shuts down ribosomal peptidyltransferase activity (Pestka, ). These dynamic changes are countered by massive reprogramming of the host transcriptional response (Nussbaumer et al ., ).…”

“…The complex nature of the underlying resistance mechanisms has been investigated in transcriptomic studies in near‐isogenic material (Hofstad et al ., ; Nussbaumer et al ., ) but not on the population level: After infection F. graminearum commences with a biotrophic life style but switches to necrotrophy after roughly 48 h. This switch is set off or followed by the production of high amounts of the trichothecene toxin deoxynivalenol (DON) that elicits oxidative stress and shuts down ribosomal peptidyltransferase activity (Pestka, ). These dynamic changes are countered by massive reprogramming of the host transcriptional response (Nussbaumer et al ., ). The outcome of these interactions is much determined by the plants correct response at the right time to counteract the multifaceted effects of DON (Audenaert et al ., ).…”

Regulation and cell biology of secondary metabolite production in Fusarium graminearum and Fusarium pseudograminearum

“…Similar, asparagine (fusatin production inducer) levels were increased in DON treated wheat plants (Nussbaumer et al, 2015), but increased asparagine levels could also be detected in resistant wheat cultivars in comparison to susceptible cultivars constitutively but also induced by F. graminearum infection (Paranidharan et al, 2008). Hence, the concentrations of different nitrogen sources changes in infected plants, probably both due to defence responses of the plants as well as due to host manipulation by the fungus.…”