Abstract
MicroRNAs (miRNAs) play a pivotal role in regulating gene expression during plant development. Although a substantial fraction of plant miRNAs has proven responsive to pathogen infection, their role in disease resistance remains largely unknown, especially during fungal infections. In this study, we screened Arabidopsis thaliana lines in which miRNA activity has been reduced using artificial miRNA target mimics (MIM lines) for their response to fungal pathogens. Reduced activity of miR396 (MIM396 plants) was found to confer broad resistance to necrotrophic and hemibiotrophic fungal pathogens. MiR396 levels gradually decreased during fungal infection, thus, enabling its GRF (GROWTH-REGULATING FACTOR) transcription factor target genes to trigger host reprogramming. Pathogen resistance in MIM396 plants is based on a superactivation of defense responses consistent with a priming event during pathogen infection. Notably, low levels of miR396 are not translated in developmental defects in absence of pathogen challenge. Our findings support a role of miR396 in regulating plant immunity, and broaden our knowledge about the molecular players and processes that sustain defense priming. That miR396 modulates innate immunity without growth costs also suggests fine-tuning of miR396 levels as an effective biotechnological means for protection against pathogen infection.
Highlights
MicroRNAs play a pivotal role in regulating gene expression during plant development
We have provided evidence that a gradual decrease of miR396 activity, and a concomitant increase of its transcription factor targets, play a central role in immune responses against necrotrophic and hemibiotrophic fungal pathogens
We have demonstrated that reduced miR396 activity results in superactivation of defense responses that enables a more successful immune response without interfering with normal growth or development
Summary
MicroRNAs (miRNAs) play a pivotal role in regulating gene expression during plant development. MiR396 levels gradually decreased during fungal infection, enabling its GRF (GROWTH-REGULATING FACTOR) transcription factor target genes to trigger host reprogramming. The enhanced H2O2 accumulation, callose deposition and transcriptional reprogramming after P. cucumerina treatment suggest a potentiated induction of defense responses in MIM396 plants, or “sensitization” that confers an improved reaction to pathogen infection. Such superactivation of defense responses is in agreement with a priming event[29]. Our results suggest that reduced levels of miR396 improve resistance to fungal pathogens through potentiation of defense mechanisms without major penalties for host growth and development. This study broadens our knowledge about the molecular players participating in defense priming by adding miR396 and its transcription factor targets to the palette of elements involved
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