Root-bacteria associations boost rhizosheath formation in moderately dry soil through ethylene responses

Abstract

The rhizosheath is a layer of soil around the root that provides a favorable environment for soil microbe enrichment and root growth. Rice (Oryza sativa) roots form rhizosheaths under moderate soil drying (MSD) conditions, but how the rhizosheath forms associations with microbes is unclear. To investigate rice rhizosheath formation under MSD, we employed a multiphasic approach, integrating data from high-throughput sequencing and root-bacteria interactions. Rice roots formed a pronounced rhizosheath under MSD, but not under continuous flooding regimens. Plant growth-promoting rhizobacteria of the Enterobacteriaceae were enriched in rhizosheaths of two different rice varieties, 'Gaoshan 1' (drought tolerant) and 'Nipponbare' (drought sensitive). RNA-sequencing analysis revealed that the ethylene pathway was induced in the rhizosheath-root system under MSD. Enterobacter aerogenes, a bacterium isolated from the rhizosheath, degrades the ethylene precursor 1-aminocyclopropane-1-carboxylate, thereby increasing rhizosheath formation. Furthermore, a 1-aminocyclopropane- 1-carboxylate deaminase-deficient mutant of E. aerogenes failed to enhance rice rhizosheath formation. Our results suggest that root-bacteria associations substantially contribute to rhizosheath formation in rice under MSD conditions by mechanisms that involve the ethylene response. These data inform strategies to reduce water consumption in rice production, one of the most water-intensive human activities.