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Heterosis or hybrid vigor refers to the superior phenotypes of hybrids relative to their parental inbred lines. Recently, soil microbes were identified as an environmental driver of maize heterosis. While manipulation of the soil microbial community consistently altered heterosis, the direction of the effect appeared to be dependent on the microbiome composition, environment, or both. Abiotic factors are well-known modifiers of heterosis expression, however, how the interactive effects between the soil microbial community and abiotic factors contribute to heterosis are poorly understood. To disentangle the proposed mechanisms by which microbes influence heterosis, we characterize the variation in heterosis expression when maize was grown in soil inocula derived from active maize farms or prairies. While we did not observe consistent differences in heterosis among plants grown in these inocula, our observations reaffirm that microbial effects on heterosis are likely specific to the local microbial community. The introduction of a nutrient amendment resulted in greater heterosis expression in the presence of an agricultural inoculum but not a prairie inoculum. We also observed an effect of soil inocula and nutrient treatment on the composition of bacterial and fungal communities in the root endosphere. In addition, the interaction between soil and nutrient treatment significantly affected bacterial community composition, whereas fungal community composition was only marginally affected by this interaction. These results further suggest that the soil microbial community plays a role in maize heterosis expression but that the abiotic environment is likely a larger driver.

Both chronic and acute drought alter the composition and physiology of soil microbiomes, with implications for globally important processes including carbon cycling and plant productivity. When water is scarce, selection favors microbes with thicker peptidoglycan cell walls, sporulation ability, and constitutive osmolyte production (Schimel, Balser, and Wallenstein 2007)-but also the ability to degrade complex plant-derived polysaccharides, suggesting that the success of plants and microbes during drought are inextricably linked. However, communities vary enormously in their drought responses and subsequent interactions with plants. Hypothesized causes of this variation in drought resilience include soil texture, soil chemistry, and historical precipitation patterns that shaped the starting communities and their constituent species (Evans, Allison, and Hawkes 2022). Currently, the physiological and molecular mechanisms of microbial drought responses and microbe-dependent plant drought responses in diverse natural soils are largely unknown (de Vries et al. 2023). Here, we identify numerous microbial taxa, genes, and functions that characterize soil microbiomes with legacies of chronic water limitation. Soil microbiota from historically dry climates buffered plants from the negative effects of subsequent acute drought, but only for a wild grass species native to the same region, and not for domesticated maize. In particular, microbiota with a legacy of chronic water limitation altered the expression of a small subset of host genes in crown roots, which mediated 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 at the metagenomic level, and demonstrate the resulting "legacy effects" on neighboring plants in unprecedented molecular and physiological detail.