Drought response of the maize plant-soil-microbiome system is influenced by plant size and presence of root hairs

We have abundant knowledge on drought responses of plants or soil microorganisms individually. However, there is a severe lack of knowledge regarding interactions in the plant-soil-microbiome continuum, and specifically root-soil interface traits including the role of root hairs. Here, we investigated how water limitation propagates in a plant-soil-microbiome system upon stopping irrigation. We used two Zea mays genotypes (rth3 and its isogenic wildtype B73), differing in root hair formation, to elucidate the effect of rhizosphere extension under water limitation. For 22 days, WT and rth3 were grown in a climate chamber, with irrigation stopped for drought treatment during the last 7 days. Daily measurements included soil water status, plant evapotranspiration and gas exchange. At harvest, root exudates, shoot relative water content, osmolality and nutrients, root morphological traits and transcriptomics, and soil microbial β-diversity and enzyme activity were determined. In line with a larger plant size, drought stress developed more rapidly and the number of differentially expressed genes was higher in the WT compared to rth3. Under water limitation, root exudation rates increased and soil enzyme activities decreased more strongly in the WT rhizosphere. In both genotypes, water level significantly altered microbial β-diversity in the bulk soil, particularly affecting fungi more than bacteria/archaea. The genotype affected only bacteria/archaea and was more pronounced in rhizosphere than in bulk soil. This interdisciplinary study assessed how a short drought stress manifested in a plant-soil-microbiome system. Water limitation altered microbial (fungal) diversity more distant from the root surface. Genotype-specific stress-induced increases in exudation rates modified microbial activity in root proximity, possibly pointing to root hair functions under water limitation. Less intense drought responses of rth3 were confirmed at all levels of investigation and may be due at least in part to its smaller plant size.