Root cap transcription factors control directional root growth in Arabidopsis seedlings in response to the plant growth-promoting rhizobacterium Achromobacter sp. 5B1

Abstract

The root cap protects the meristem as the root grows and senses stimuli such as gravity and nutrient availability. Although it enables tight interaction with the rhizosphere, a role in perceiving microorganisms is unknown. Here, through Arabidopsis direct root inoculation with the plant growth promoting rhizobacterium Achromobacter sp. 5B1, we unveiled a critical, opposite role of two transcription factors, FEZ and SOMBRERO, in mediating growth, waving, and coiling of primary roots as a response to the bacterium. In Arabidopsis seedlings with mutations in FEZ, the rhizobacterium had increased formation of coils, whereas in seedlings harboring mutations in SOMBRERO, the formation of coils did not occur and the root maintains normal gravity response. This correlated with the elongation of the cells on the right or convex side, an aspect that is increased in fez-2 mutants but does not manifest itself in smb-3 mutants. Interaction with Achromobacter sp. 5B1 increased the size of the root cap, which coincided with decreased or increased detection in vivo of FEZ:FEZ:GFP and SMB:SMB:GFP, respectively, and with the phenotype of smb-3 mutants, which develop roots with a huge cap irrespective of bacterization. Expression of auxin transporters PIN1, PIN2, PIN3, PIN4, and PIN7 overall decreased in the WT, fez-2, and smb-3 upon bacterial inoculation, suggesting that the agravitropic behavior of roots may be linked to disturbance of auxin distribution within the root tip. Our data indicate that the root cap senses the rhizobacterium Achromobacter sp. 5B1 through FEZ and SOMBRERO for the directional growth and soil exploration.