Guiding gravitropism: root coiling in response to growth-promoting bacteria is mediated by root cap transcription factors

Abstract

Darwin showed that the root cap was important for sensing gravity (Darwin, 1881). Today, we know that starch-filled granules in the root cap cells act as statoliths that sink in response to gravity. This triggers a signaling process leading to differential cell elongation in the root elongation zone to adapt root growth to the direction of gravity (Su et al., 2017). The root cap is not only involved in gravitropism, but also in many other processes, including sensing nutrients, salt, water, and modulating rhizosphere microbiota (Ganesh et al., 2022).

In the highlighted publication, Kirán Rubí Jiménez-Vázquez and colleagues show how two root cap transcription factors could act to integrate contact with rhizosphere microbes with root gravitropism. For his PhD project, Jiménez-Vázquez was involved in a biodiversity study of bacteria that inhabited an exceptional ecosystem, a salty pool in the middle of the Chihuahua desert. The researchers were surprised that some grasses could grow well despite the high salt content, amidst a film of salt crystals, and they also saw some mesquite trees that looked healthy. Therefore, they sampled the rhizosphere of a mesquite tree and built a collection of culturable bacteria. They then inoculated Arabidopsis thaliana seedlings with the pure cultures to analyze the root phenotype and biomass production (Jiménez-Vázquez et al., 2020). Interestingly, the rhizobacterium Achromobacter sp. 5B1 not only promoted primary root growth and lateral root formation in Arabidopsis but also induced root waving and coiling once the bacteria spread over the primary root (Figure 1). This caught the attention of the researchers because it was the only reported bacterium that caused disruption of the gravitropic response (Jiménez-Vázquez et al., 2020).

They wondered how Achromobacter sp. 5B1 modifies developmental processes in the roots, in particular gravitropism (Jiménez-Vázquez et al., 2025). They analyzed primary root growth on agar plates under different conditions: (1) roots in direct contact with the bacterial streak; (2) roots and bacteria on opposite sides of divided Petri dishes, allowing only volatile compounds to be sensed; and (3) the bacterial streak placed near, but not touching, the root cap, enabling interaction through diffusible molecules like metabolites and phytohormones. In all cases, the bacterium promoted primary and lateral root growth, but the roots only coiled and showed disrupted gravitropism when the root was in direct contact with the inoculum. This reaction was specific to Achromobacter sp. 5B1 and was not observed for other plant growth-promoting bacteria (i.e., Bacillus sp. LC390B or Micrococcus luteus LS570). Roots with no root cap did not coil after contact with the bacterium, suggesting that the root cap is responsible for sensing the bacterium and directing the root growth response.

The NAC domain transcription factors FEZ and SOMBRERO (SMB) are key in controlling root cap formation (Willemsen et al., 2008). FEZ expression decreased after contact with Achromobacter sp. 5B1, while the expression of SMB increased. Interestingly, Achromobacter sp. 5B1 promoted root growth in both fez-2 and smb-3 mutants, but in smb-3 mutants the roots did not coil, while fez-2 roots coiled more often than wild-type roots (Figure 1).

The agravitropic root growth in response to Achromobacter sp 5B1 was associated with differential cell growth at the root elongation zone: coiled roots had longer cells on the convex side, and this was more pronounced in fez-2 mutants. The authors previously showed that in response to Achromobacter sp 5B1, higher expression of the auxin-responsive reporter DR5 could be detected toward the concave side of the roots (Jiménez-Vázquez et al., 2020). In root caps, they observed an enhanced auxin signal at the center, with redistribution toward the lateral root cap and epidermal cells toward the concave side of the roots upon root contact with Achromobacter sp 5B1. DR5 expression in fez-2 root caps was lower than in wild-type, but auxin could still be mobilized toward the concave side when roots were co-cultivated with Achromobacter sp. 5B1. smb-3 mutants showed elevated DR5 expression levels regardless of bacterial presence, and no asymmetric auxin gradient could be established in response to the bacterium. Together, this suggests that auxin distribution is critical to deviate root growth in response to Achromobacter sp. 5B1.

Auxin transport is facilitated by the auxin efflux carriers PINFORMED (PINs) (Blilou et al., 2005). In the fez-2 mutant, levels of the PIN1, PIN3, and PIN4 proteins were reduced, while PIN2 and PIN7 levels remained unchanged. Co-cultivation with Achromobacter sp. 5B1 reduced the levels of all PINs in fez-2 even further. In the smb-3 mutant, levels of all PIN exporters (except PIN7) were lower than in wild-type. Upon bacterial inoculation, PIN levels were further reduced, except for PIN4 and PIN7 levels, which increased in columella cells. This could interfere with the establishment of the asymmetric auxin gradient in the smb-3 mutant, preventing the root coiling in response to Achromobacter sp. 5B1.

In summary, Jiménez-Vázquez and colleagues found that Achromobacter sp. 5B1 regulates root growth behavior through the root cap-specific transcription factors FEZ and SMB, which modulate the directional auxin flow through regulation of PIN protein levels. Here, SMB plays a key role in creating an asymmetric distribution of auxin in the root cap, which initiates directional root growth.

What could be the advantage of inducing agravitropic behavior in roots? While the authors can only speculate, the agravitropic root response triggered by Achromobacter sp. 5B appears to promote lateral root formation. This could enable roots to temporarily avoid or better tolerate environmental stresses by redirecting growth away from the primary root tip and expanding into new soil regions. As a result, plants could improve soil exploration and enhance their ability to access water and nutrients, which would create a favorable niche for the bacteria to live and receive fixed carbon via root exudation.