Stress memory and phyllosphere/soil legacy underlie tolerance and plasticity of Leymus chinensis to periodic drought risk

Abstract Periodic drought is one of the most frequent stressors for grassland plants under climate change, potentially inhibiting ecosystem productivity and stability through its legacy effects. Recent findings on plant stress memory and microbial legacy effects provide some unique perspectives on this issue. However, the mechanisms underlying intra- and inter-generational adaptation to drought in grassland plants are currently unclear. Here, we conducted a set of experiments using the perennial rhizome grass Leymus chinensis, the dominant species in the eastern Eurasian grasslands, aiming to examine the roles of (1) stress memory in intra-generational adaptation and clonal trans-generational plasticity and (2) phyllosphere/soil legacy effects in inter-generational adaptation to repeated drought events. We found that L. chinensis experiencing repeated drought had increased proline content, photosynthetic rate, and water retention capacity than those that did not experience repeated drought. This supports the hypothesis that stress memory is a key mechanism underlying within-generation physiological adaptation of plants. Moreover, clonal offspring of drought-exposed L. chinensis had poor growth but showed higher levels of tolerance to drought relative to the control group. Inoculation with drought-conditioned phyllosphere communities increased proline content but decreased the photosynthetic rate of L. chinensis. In contrast, drought-associated soil aided plant growth through legacy effects but did not affect proline content under repeated drought events. Overall, drought resilience enhances the ability of clonal L. chinensis to cope with repeated drought via intra-generational stress memory. Our findings highlight the importance of stress memory and the potential complementary effect of soil and phyllosphere legacy effects on plant growth and tolerance to repeated drought under climate change.