A seed-borne endophyte mediates plant drought responses and intergenerational effects on seed characteristics

Global warming is expected to increase drought severity in diverse environments, impacting plant performance. Plants acclimate to drought by mechanisms like stomatal closure and osmotic adjustment. Maternally inherited symbiotic microorganisms with capacity to regulate these mechanisms have the potential to influence intergenerational plant drought responses. We studied how a seedborne endophyte affects maternal drought effects on seed germination water requirements and specialized metabolites. Isotopic analysis of seed cellulose indicated that drought led to improved water use efficiency (WUE; higher δ13C) in endophyte-free mother plants, seemingly without affecting stomatal conductance (non-significant δ18O change). Alternatively, endophyte-symbiotic plants did not exhibit a change in WUE but apparently an increase in stomatal conductance (significant δ18O decrease). Regardless of the symbiosis, drought reduced seed production but not seed size. Endophyte symbiosis improved the seed concentration of mannitol and sorbitol, but this increment was higher under drought. Maternal plant responses to drought did not increase seed germination under reduced water potential but induced dormancy in seeds from endophyte-free but not endophyte-symbiotic plants. Our findings suggest that although differential accumulation of metabolites in seeds results from how endophyte-symbiotic plants perceive and respond to drought, this response may not form part of a mechanism that would enhance seed performance of progeny under drought. •Drought events will increase under global warming, impacting plant performance.•Plant responses to drought involve mechanisms like stomatal closure and osmotic adjustment.•Maternally inherited fungal endophytes influence intergenerational plant drought responses.•Endophyte-symbiotic plants show different water use efficiency and stomatal conductance under drought.•Seedborne endophytes modulate maternal drought effects on seed germination and metabolites.