Persistent legacy effects on soil microbiota facilitate plant adaptive responses to drought.

Abstract

Both chronic and acute drought alter the composition and physiology of the soil microbiota, favoring the selection of microbes with functional traits that preserve fitness in these challenging conditions 1 . This drought-adapted microbiota may influence water-use efficiency mechanisms in host plants. Currently, it is largely unknown how this soil microbial drought legacy manifests at the molecular and physiological levels and how it influences microbe-dependent plant responses to drought in diverse natural soils. Here, to infer how drought legacy affects soil microbiota composition and function, we collected soils spanning two distinct and geographically distant precipitation gradients. By controlling for variation in numerous other soil properties including porosity and elemental profiles, we identified a group of bacterial taxa that are highly sensitive to water availability and critical for the formation of soil drought memory. Next, by imposing an acute experimental drought we show that this microbial drought legacy is robust to short-term perturbations. Furthermore, we reveal that soil microbiota from historically dry climates buffered a wild grass species native to the precipitation gradient, but not the domesticated crop species maize, from the negative effects of subsequent acute drought. In particular, microbiota with a legacy of chronic water limitation altered the expression of a small subset of host genes that mediate the effect of acute drought on transpiration and intrinsic water use efficiency. Our results reveal how long-term exposure to water stress alters soil microbial communities and demonstrate the resulting "legacy effects" on the drought responses of neighboring plants.