Summary Arbuscular mycorrhizal (AM) fungi can form mutualistic endosymbiosis with > 70% of land plants for obtaining fatty acids and sugars, in return, AM fungi promote plant nutrients and water acquisition to enhance plant fitness. However, how AM fungi orchestrate its own signaling components in response to drought stress remains elusive. Here, we identify a transcription factor containing C2H2 zinc finger domains, RiMsn2 from Rhizophagus irregularis. To characterize the RiMsn2, we combined heterologous expression, subcellular localization in yeasts, and biochemical and molecular studies with reverse genetics approaches during the in planta phase. The results indicate that RiMsn2 is highly conserved across AM fungal species and induced during the early stages of symbiosis. It is significantly upregulated in mycorrhizal roots under severe drought conditions. The nucleus‐localized RiMsn2 regulates osmotic homeostasis and trehalose contents of yeasts. Importantly, gene silencing analyses indicate that RiMsn2 is essential for arbuscule formation and enhances plant tolerance to drought stress. Results from yeasts and biochemical experiments suggest that the RiHog1‐RiMsn2‐STREs module controls the drought stress‐responsive genes in AM fungal symbiont. In conclusion, our findings reveal that a module centered on the transcriptional activator RiMsn2 from AM fungus regulates drought stress tolerance in host plant.

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