Environmental legacy effects impact maize growth and microbiome assembly under drought stress

Background and Aims As the climate changes, plants and their associated microbiomes face greater water limitation and increased frequency of drought. Historical environmental patterns can leave a legacy effect on soil and root-associated microbiomes, but the impact of this conditioning on future drought performance is poorly understood. Precipitation gradients provide a means to assess these legacy effects. Methods We collected soil microbiomes from four native prairies across a steep precipitation gradient in Kansas, USA. Seedlings of two Zea mays genotypes were inoculated with each soil microbiome in a factorial drought experiment. We investigated plant phenotypic and root microbiome responses to drought and modeled relationships between plant growth metrics and climatic conditions from the soil microbiome origin sites. Results Drought caused plants to accumulate shoot mass more slowly and achieve greater root/shoot mass ratios. Drought restructured the bacterial root-associated microbiome via depletion of Pseudomonadota and enrichment of Actinomycetota, whereas the fungal microbiome was largely unaffected. An environmental legacy effect on prairie soil microbiomes influenced plants’ drought responses: counterintuitively, prairie soil inocula from historically wetter locations increased shoot biomass under drought more than inocula from historically drier prairie soils. Conclusion We demonstrated links between soil microbiome legacy effects and plant performance under drought, suggesting that future drying climates may condition soils to negatively impact plant performance. ### Competing Interest Statement The authors have declared no competing interest. Raw sequencing data is available on NCBI SRA under BioProject ID PRJNA913622 and SRA accessions SAMN32302538-SAMN32303072 for root-associated samples and SAMN33863891-SAMN33864082 for soil and inoculum samples. Code to reproduce the analysis and figures are available on GitHub at [https://github.com/Kenizzer/Maize\_Drought\_Microbiome][1]. [1]: https://github.com/Kenizzer/Maize_Drought_Microbiome