Effect of water retention caused drought and the loss of root hairs on maize root gene expression

Background and Aims: We have a limited understanding of the complex interactions occurring in the plant-soil-microbiome continuum, and how root hairs interact with microbes to maintain rhizosphere processes. Here, we investigate how water limitation propagates in a plant-soil-microbiome system upon stopping irrigation. We use two maize genotypes (rth3 and wildtype B73), differing in root hair formation, to elucidate the effect of rhizosphere extension under water limitation.Methods: For 22 days, WT and rth3 were grown in a climate chamber, with irrigation stopped for drought treatment during the last 7 days. Soil water status, evapotranspiration and gas exchange were measured daily. At final harvest, root exudates, biomass, relative water content, osmolality, nutrients, root morphological traits, transcriptomics, microbial beta-diversity and enzyme kinetics were determined.Key Results: In line with a larger plant size, the number of differentially expressed genes was higher, and drought stress developed more rapidly in the WT compared to rth3. Under drought, root exudation rates were increased and soil enzyme activities were more strongly decreased in the rhizosphere of WT compared to rth3. Water level significantly affected microbial beta-diversity in the bulk soil, with a stronger impact on fungi than bacteria/archaea. A significant genotype effect was observed only for bacteria/archaea and was more pronounced in the rhizosphere. The effect of drought on enzymatic rates was more pronounced in the rhizosphere of WT than rth3.Conclusions: With our interdisciplinary study, we have drawn a picture of how a defined short drought stress is expressed in a plant-soil-microbiome system. Water limitation was the driving force for alterations of microbial (fungal) diversity more distant from the root surface, while genotype-specific stress-induced increases in exudation mainly modified microbial activity in root proximity. Furthermore, plant-mediated microbial responses to drought resulted in a retarded growth, an increased affinity of drought-sensitive enzymes, and a reduced contribution of plant-originated enzymes to P-turnover in the rhizosphere. The less intense drought response of the rth3 mutant was confirmed at all levels of investigation and may be due at least in part to the slightly smaller plant size of this genotype.