Implications of reduced root-soil contact for microbial rhizosphere establishment and early plant growth performance

Abstract

Processes at the root-soil interface are essential for plant nutrient and water uptake, but the level of root-soil contact varies depending on root traits and soil properties. Implications of reduced root-soil contact for the rhizosphere, its microbiota and for plant performance remain largely unclear. Here, the consequences of root-soil contact reduction were analyzed in maize microcosm experiments. Either soil porosity was modified by introducing artificial large-sized pores, or the contact area was reduced by a maize mutant (rth3) impaired in root hair development. Microscopic evaluation of roots grown in pores without soil contact revealed strongly reduced prokaryotic surface colonization. Bacterial abundance in the rhizosphere soil of remaining contact areas was also reduced (2.2 × 10¹⁰ vs. 1.0 × 10⁹ 16S rRNA gene copies per g dry soil), including the abundance of nitrogen cycling bacteria. The absence of root hairs decreased bacterial abundance likewise, though not of nitrogen cycling prokaryotes. 16S rRNA gene-based amplicon sequencing revealed bacterial community-compositional alterations in the rhizosphere (PERMANOVA R² = 0.701, p = 0.001) with lower relative abundances of Massilia and Paenibacillus for roots grown in pores. Community shifts in the rhizosphere of rth3 plants showed similar changes. No differences were evident upon root-soil contact reduction in the endosphere bacterial community. Combined manipulations revealed that root hairs improved root-soil contact in pores, whereas lateral roots reduced it, as validated with a maize mutant (lrt1) impaired in lateral root development. Plant growth and biomass allocation in the first three weeks were only weakly affected by root-soil contact reduction. Overall, the level of root-soil contact appears critical for bacterial life in the rhizosphere and rhizoplane, including the establishment of nitrifying bacteria and potential plant-beneficial taxa such as Massilia. Aiming at optimum root-soil contact by soil management and plant breeding strategies has thus the potential to contribute to the establishment of a functional rhizosphere microbiome.