Salt stress reverses root circumnutation, -skewing and -growth direction in Arabidopsis

Plant roots exhibit remarkable developmental plasticity, resulting in the adaptation of growth direction and architecture upon environmental changes. Previously, we demonstrated that inorganic phosphate (Pi) triggers Arabidopsis roots to skew to the left when grown on tilted agar plates. This so-called 'phosphate-dependent skewing' (PDS) is caused by a right-handed (clockwise, CW) circumnutation of the root tip, which is driven by a left-handed (counterclockwise, CCW) cell file rotation (CFR) of epidermal cells in the root elongation zone, and involves the cortical microtubule cytoskeleton (Sheng et al., 2024). In the present study, we demonstrate that NaCl triggers a skewing response in the opposite direction and that all other helical movements are also reversed. Thus, 'Salt-Induced Rightward Skewing' (SIRS) is accompanied by a right-handed (CW) epidermal CFR, a left-handed (CCW) circumnutation of the root tip, and hence, a left-handed (CCW) helical root growth. Comparing different Na+- and Cl- salts revealed that SIRS is predominantly caused by cations, and can be induced by K+ and osmotic stress as well, although Na+ is most efficient. To get further insight into the mechanism underlying this response, we tested candidate genes from an earlier GWAS on root responses to salt stress (Deolu-Ajayi et al., 2019) for their potential involvement. This identified GLT1 and DOB1 as being involved in the root skewing response to Pi and NaCl, respectively. Our findings reveal that Pi and salinity elicit opposing effects on root circumnutation, and hence root skewing and growth direction. Understanding the molecular machinery driving this helical behaviour may help explain adaptive mechanisms, including changes in the spatial architecture of roots, and may facilitate the optimization of crop yield under abiotic stress conditions through breeding or crop management strategies. Our results also shed new light on halotropism, which is typically measured as a change in root growth direction to the right, which in the present study has been identified to represent SIRS.