Transcriptional Basis of Drought-Induced Susceptibility to the Rice Blast Fungus Magnaporthe oryzae

Abstract

Plants are often facing several stresses simultaneously. Understanding how they react and the way pathogens adapt to such combinational stresses is poorly documented. Here, we developed an experimental system mimicking field intermittent drought on rice followed by inoculation by the pathogenic fungus Magnaporthe oryzae. This experimental system triggers an enhancement of susceptibility that could be correlated with the dampening of several aspects of plant immunity, namely the oxidative burst and the transcription of several pathogenesis-related genes. Quite strikingly, the analysis of fungal transcription by RNASeq analysis under drought reveals that the fungus is greatly modifying its virulence program: genes coding for small secreted proteins were massively repressed in droughted plants compared to unstressed ones whereas genes coding for enzymes involved in degradation of cell-wall were induced. We also show that drought can lead to the partial breakdown of several major resistance genes by affecting R plant gene and/or pathogen effector expression. We propose a model where a yet unknown plant signal can trigger a change in the virulence program of the pathogen to adapt to a plant host that was affected by drought prior to infection.

Global profiling of phytohormone dynamics during combined drought and pathogen stress in Arabidopsis thaliana reveals ABA and JA as major regulators

“…However, the scenario described here varies with different kind of pathogens 24, 62, 63 which can variably influence the outcome of stress interactions under combined stress. Also, recent molecular studies suggest that specific combined stress invokes novel responses in plants and therefore, those cannot be predicted from the study of either stress individually 6, 12, 64–66 .

Figure 4Schematic diagram illustrating the hormonal network under individual drought and host pathogen and their combination. The hormone and transcriptome profile data was integrated to redraw the model from Atkinson and Urwin (2012).

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The role of water in plant–microbe interactions

“…In contrast, drought‐treated rice becomes more susceptible to M. oryzae infection (Bidzinski et al ., ). In this pathosystem, drought stress was found to suppress PTI and ETI (Bidzinski et al ., ). These contrasting findings suggest that severe water limitation (i.e., drought) might differentially affect plant defense and microbial pathogenesis in different pathosystems.…”

“…In addition, drought-stressed chickpea exhibits higher resistance to a xylem-inhabiting bacterial pathogen, Ralstonia solanacearum (Sinha et al, 2016). In contrast, drought-treated rice becomes more susceptible to M. oryzae infection (Bidzinski et al, 2016). In this pathosystem, drought stress was found to suppress PTI and ETI (Bidzinski et al, 2016).…”

Effectors of plant-colonizing fungi and beyond

“…An emerging concept is that adaptation of effector expression is not limited to developmental programs of the pathogen or infection strategies in different hosts or plant organs but also occurs when the host plant is challenged by abiotic stresses. Transcriptomic studies on rice under mild drought stress showed that the hemibiotrophic fungus Magnaporthe oryzae transcriptionally downregulates the majority of its putative effectors despite being more successful in colonizing the stressed plants [ 11 ]. All these examples of adapted effector expression imply that specific environmental signals must be perceived during colonization by the invading microbes.…”