New insights into root gravitropic signalling

Abstract

An important feature of plants is the ability to adapt their growth towards or away from external stimuli such as light, water, temperature, and gravity. These responsive plant growth movements are called tropisms and they contribute to the plant's survival and reproduction. Roots modulate their growth towards gravity to exploit the soil for water and nutrient uptake, and to provide anchorage. The physiological process of root gravitropism comprises gravity perception, signal transmission, growth response, and the re-establishment of normal growth. Gravity perception is best explained by the starch-statolith hypothesis that states that dense starch-filled amyloplasts or statoliths within columella cells sediment in the direction of gravity, resulting in the generation of a signal that causes asymmetric growth. Though little is known about the gravity receptor(s), the role of auxin linking gravity sensing to the response is well established. Auxin influx and efflux carriers facilitate creation of a differential auxin gradient between the upper and lower side of gravistimulated roots. This asymmetric auxin gradient causes differential growth responses in the graviresponding tissue of the elongation zone, leading to root curvature. Cell biological and mathematical modelling approaches suggest that the root gravitropic response begins within minutes of a gravity stimulus, triggering genomic and non-genomic responses. This review discusses recent advances in our understanding of root gravitropism in Arabidopsis thaliana and identifies current challenges and future perspectives.

Keywords: Arabidopsis thaliana; auxin; calcium; differential growth; gravitropic response; root growth; tropism..

Fig. 1.

Gravitropic bending of an Arabidopsis thaliana root. Sequential imaging of a bending root with colour codes at different time points.

Fig. 2.

Gravity perception in Arabidopsis thaliana. At time point 0, roots grow vertically. After a 90 ° turn, the following series of events take place: (1) At 10 s, statoliths are still at the old bottom of the cell. After 3min, statoliths move towards the new bottom of the cell to be uniformly distributed at 5min (Leitz et al., 2009). (2) PIN3 and PIN7 relocalization is achieved 2min after the gravity stimulus and, in consequence, a lateral auxin gradient is generated between the upper and lower side of the root (thin and thick orange arrows respectively) (Friml et al., 2002b ). (3) Development of differential extracellular pH levels between the upper (acidic) and lower (alkaline) side of the gravistimulated root (Monshaussen et al., 2011).

Fig. 3.

Gravity signal transduction and transmission. Auxin transport and redistribution upon a gravity stimulus. AUX1 and PIN2 channel auxin from the shoot to the root tip (black arrows). Auxin efflux is distributed through the vascular tissue to the columella cells by PIN4 (blue arrows). PIN3 and PIN7 set up the auxin flow (green arrows), with an accumulation on the lower side of the root. PIN2 and AUX1 transport auxin through the lateral root cap to the epidermal cells in the elongation zone (orange arrows) where the actual growth response will occur.

Fig. 4.

Gravity response. The pH and several molecules, such as Ca²⁺, reactive oxygen species (ROS), nitric oxide (NO), and inositol 1,4,5-triphosphate (InsP₃), serve as signals in the non-genomic phase of root bending. Following this initial phase, a change in the expression of auxin-regulated genes is seen within 15min (adapted from Band et al., 2012a ).

Fig. 5.

Restoration of the symmetrical auxin flow and of vertical growth. When the root reaches 40° (~100min after the initial gravistimulus), the auxin symmetry is restored (Band et al., 2012a ) and the root continues to bend until it ultimately regains growth along the gravity vector.

Fig. 6.

Arabidopsis thaliana root system. Overview of the A. root system redrawn from a 7-day-old seedling, showing the orientation of primary and lateral roots.