Growth-induced hormone dilution can explain the dynamics of plant root cell elongation

Abstract

In the elongation zone of the Arabidopsis thaliana plant root, cells undergo rapid elongation, increasing their length by ∼10-fold over 5 h while maintaining a constant radius. Although progress is being made in understanding how this growth is regulated, little consideration has been given as to how cell elongation affects the distribution of the key regulating hormones. Using a multiscale mathematical model and measurements of growth dynamics, we investigate the distribution of the hormone gibberellin in the root elongation zone. The model quantifies how rapid cell expansion causes gibberellin to dilute, creating a significant gradient in gibberellin levels. By incorporating the gibberellin signaling network, we simulate how gibberellin dilution affects the downstream components, including the growth-repressing DELLA proteins. We predict a gradient in DELLA that provides an explanation of the reduction in growth exhibited as cells move toward the end of the elongation zone. These results are validated at the molecular level by comparing predicted mRNA levels with transcriptomic data. To explore the dynamics further, we simulate perturbed systems in which gibberellin levels are reduced, considering both genetically modified and chemically treated roots. By modeling these cases, we predict how these perturbations affect gibberellin and DELLA levels and thereby provide insight into their altered growth dynamics.H ormone distributions within plant tissues affect plant growth and development (1). Although many studies have investigated the influence of nonuniform distributions of the hormone auxin, gradients in other hormones also govern plant growth (2, 3). In some regions of the plant, cells undergo rapid expansion that dilutes their contents, including hormones. In these regions, organ-scale hormone gradients can arise due to the interplay between dilution, diffusion, production, decay, and receptor binding. Such complex dynamics govern in particular the distribution of the plant hormone gibberellin, which is involved in a diverse range of developmental processes including germination, organ development, and growth (4).A well-studied context for gibberellin growth regulation is provided by the primary root of the model species Arabidopsis thaliana (3, 5, 6). At the organ level, the Arabidopsis primary root classically presents three distinct morphological zones (ref. 7; Fig. 1A): Cells divide in the meristem, which is located close to the root tip; after a number of divisions, cells then move through the elongation zone, where they rapidly increase in length with negligible change in radius; finally, cells stop growing on entering the mature zone. Gibberellin has been described as a key hormone in regulating both cell division in the root meristem (6) and cell elongation in the elongation zone (5).Gibberellin regulates cell elongation and division by mediating the destabilization of DELLA proteins (8, 9). Gibberellin first binds with its receptor GID1, forming gibberellin-GID1 complexes that can then interact wi...

Mathematical Modelling Plant Signalling Networks

“…A recent analysis in this vein was performed on gibberellin perception in [86]. The authors embedded the model developed in [78] in a multi-scale spatial framework to analyse the interplay between GA signalling and root growth.…”

Gradients in Wall Mechanics and Polysaccharides along Growing Inflorescence Stems

“…Spatial gradients in growth hormones (auxin and GA) were proposed (Went and Thimann, 1937;Sánchez-Bravo et al, 1992;Band et al, 2012), but hormones are several steps removed from the biochemical and biophysical processes that drive cell growth (e.g. cell wall loosening and stress relaxation, leading to water uptake and concomitant expansion of the cell wall; Cosgrove, 2016).…”

Modelling Plant Hormone Gradients

“…The combination of experimental and modelling analysis enables the study of plant hormone gradients as an integrated system, in which the causal relationships of all components can be established. To date, this approach has led to an improved understanding of, for example, how PIN proteins play a key role in auxin patterning and root growth (Grieneisen et al, 2007); how asymmetric auxin gradients link to gravitropsim (Band et al 2012; see also doi: 10.1002/9780470015902.a0025267);…”

“…It has also been shown that growth-induced hormone dilution can explain the dynamics of plant root cell elongation (Band et al, 2012).…”