Unifying model of shoot gravitropism reveals proprioception as a central feature of posture control in plants

Abstract

Gravitropism, the slow reorientation of plant growth in response to gravity, is a key determinant of the form and posture of land plants. Shoot gravitropism is triggered when statocysts sense the local angle of the growing organ relative to the gravitational field. Lateral transport of the hormone auxin to the lower side is then enhanced, resulting in differential gene expression and cell elongation causing the organ to bend. However, little is known about the dynamics, regulation, and diversity of the entire bending and straightening process. Here, we modeled the bending and straightening of a rod-like organ and compared it with the gravitropism kinematics of different organs from 11 angiosperms. We show that gravitropic straightening shares common traits across species, organs, and orders of magnitude. The minimal dynamic model accounting for these traits is not the widely cited gravisensing law but one that also takes into account the sensing of local curvature, what we describe here as a graviproprioceptive law. In our model, the entire dynamics of the bending/straightening response is described by a single dimensionless "bending number" B that reflects the ratio between graviceptive and proprioceptive sensitivities. The parameter B defines both the final shape of the organ at equilibrium and the timing of curving and straightening. B can be estimated from simple experiments, and the model can then explain most of the diversity observed in experiments. Proprioceptive sensing is thus as important as gravisensing in gravitropic control, and the B ratio can be measured as phenotype in genetic studies.perception | signaling | movement | morphogenesis

The foundations of plant intelligence

“…Temperature (higher or lower than ambient) institute radical shifts in behaviour, often not perceived but easily detected experimentally [2]. There are numerous kinds of mechanical signals such as touch, bending, wind [45] or even weight itself and proprioreception [46]; stress institutes different phenotypic effects to strain [47]. Soil obstacles initiate marked root phenotypic change [48].…”

On the growth and form of shoots

“…The simplest of these, Sachs' law, states that the local rate of curvature of the growth zone responds to the orientation of the shoot, leading to a response that is strongest at regions which are horizontal and weakest where it is vertical. However, this does not suffice to build a regulatory framework for stem straightening; indeed, it leads to oscillations [11] similar to those in undamped feedback control systems. Separately, evidence shows that plants and fungi have a proprioceptive sense known as autotropism that causes them to grow straight in the absence of any stimuli [3,[17][18][19][20].…”

“…In the minimal setting considered in [11,26], effects such as elasticity and gravity acting on soft stems, and maturation/lignification are neglected, and this implicitly raises the natural question of how to modify the theory to explain the various complex spatio-temporal morphologies of plant shoots summarized earlier.…”

“…For example, Impatiens glandulifera [11][12][13] can have shoots that display oscillatory curving and de-curving before converging to a vertically upward steady orientation, Cerastium tomentosum (figure 1c) and Toxicodendron radicans (figure 1d) have shoots that first grow vertically downwards before turning upwards effectively switching from being positively gravitropic to negatively gravitropic as the plant develops, Salix alba (figure 1e) exhibits an apparent positive gravitropic behaviour by growing in the direction of gravity, and Trandescantia fluminensis and Oplismenus hirtellus [14,15] also display a 'gravitropic sign reversal' suggesting a time-dependent preferential orientation.…”

Beyond the sine law of plant gravitropism

“…Unlike models based solely on Sachs' sine law, the gravitropic/autotropic model put forward by the authors explains why the universal gravitropic response in plant stems proceeds from an initial overall bending of the stem followed by basipetal straightening (3,18). As shown in their paper (3), a stem placed horizontally will rapidly converge to a steady-state solution where the stem angle (A) decreases exponentially over the length (L gz ) of the growth zone:…”