Mortierella alleviates the poor growth and the compositional changes of root exudates of root hairless maize mutant

The rhizospheric and endophytic microbiota, recognized as the plant's second genome, have gained increasing attention. Root hairs, as pivotal structures for nutrient uptake and exudate secretion, are essential regulators of plant-microbe interactions. However, how root microbiota respond to root hair traits and their potential compensatory mechanisms remains poorly understood. Here, the maize inbred line B73 and its root hairless mutant were compared based on a field experiment. This study integrated rhizosphere and root endosphere microbial community characterization with transcriptomic sequencing and untargeted metabolomic analysis to detect genes with distinct expression patterns and differential metabolites in mutant versus wild-type maize. The findings revealed that root hair absence significantly impairs maize growth, resulting in pronounced differences in the endophytic and rhizospheric microbial communities. Notably, the absence of root hairs particularly impacted endophytic nitrogen-fixing bacteria and even the amino acid composition in root exudates. The change pattern of endophytic nitrogen-fixing bacteria was highly consistent with ferredoxin nitrate reductase genes, further corroborated by RNA-seq, indicating these bacteria partially compensate for the insufficient nitrogen absorption caused by the loss of root hair. Mortierella abundance declined by over 80% in the rhizosphere of hairless root mutant, which strongly associated with many downregulated root exudates. Exogenous inoculation with Mortierella efficiently restored these root metabolites. Mortierella inoculation effectively mitigated the poor growth of the mutant. This study highlights the compensatory role of rhizosphere microorganisms in alleviating the adverse effects of plant gene mutations and highlights the significant influence of specific rhizosphere microorganisms on crop growth. • Root hair deficiency triggered notable variations in maize rhizosphere microbes. • Nitrogen assimilation genes in root linked with endogenous nitrogen fixing bacteria. • Rhizosphere Mortierella was depleted in the root hairless mutant of maize. • The inoculation of Mortierella effectively restored the growth of the maize mutant.