Dynamic control of lateral root positioning

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Highlights

  • The root cap contains an auxin source that modulates lateral root patterning.

  • Recurrent programmed cell death controls the regular spacing of lateral roots.

  • Periodic release of auxin by dying root cap may trigger prebranch site formation.

  • Tropic responses control the LR sidedness.

In dicot root systems, lateral roots are in general regularly spaced along the longitudinal axis of the primary root to facilitate water and nutrient uptake. Recently, recurrent programmed cell death in the root cap of the growing root has been implicated in lateral root spacing. The root cap contains an auxin source that modulates lateral root patterning. Periodic release of auxin by dying root cap cells seems to trigger lateral root specification at regular intervals. However, it is currently unclear through which molecular mechanisms auxin restricts lateral root specification to specific cells along the longitudinal and radial axes of the root, or how environmental signals impact this process.

Introduction

Plant growth depends on the water and nutrients that a plant can extract from the soil. These resources are both spatially and temporally heterogeneously distributed in soil [1]. Therefore, plants make use of a dual strategy to efficiently exploit water and nutrients. Initially, the growing root tip that traverses unexplored soil maximizes the capacity to find resources by the regular spacing of cells competent to form lateral roots (LRs) in newly formed parts of the main root [2]. This modular organization of the root system subsequently allows the root to show plasticity upon encountering nutrient-rich patches, as environmental cues control the outgrowth, elongation and curving of LRs to enhance nutrient resource capture [1]. The mechanisms that control the regular LR pattern along the main root are mainly studied in the dicot plant Arabidopsis thaliana. In this and other dicot species, LRs originate deep within the root from the pericycle layer (Figure 1c) [3]. In Arabidopsis, LRs can initiate from two opposite poles inside the cylindrical pericycle layer that flank the xylem axis in the underlying vascular bundle (Figure 1b). These poles contain the xylem pole pericycle (XPP) cells. The first anatomical signs of LR initiation are the rounding and coordinated migration of nuclei from several adjacent pairs of XPP cells towards the common cell wall and the concomitant swelling of these XPP cells [4, 5]. Shortly after, these XPP cells divide asymmetrically to initiate the development of a LR primordium that penetrates the surrounding root layers and forms an emerged, functional LR (recently reviewed in [6]). LR initiation and development depend on the activity of the plant hormone auxin (reviewed in [7]).

Here, we review recent insights that reveal how the spatial pattern of LRs along the main root is established, and speculate about molecular mechanisms that might establish the LR pattern along the longitudinal axis of the root during growth. We highlight the vital role of the root cap in this process, and discuss how tropic responses to gravity and water availability impact LR spacing to optimally exploit underground resources.

Section snippets

LR prepattern

Although less obvious as compared to the phyllotaxy of the shoot, the soilborne root system is also organized according to a recurrent pattern reflected by the relative uniform spacing of lateral roots along the main root. This spacing pattern is defined before the first anatomical signs of LR initiation. A growing root can be spatially divided in a meristematic zone, an elongation zone and a differentiation zone. The LR initiation process that occurs in the differentiation zone is spatially

Synchronous cell death of root cap cells positions LRs

Interestingly, the activity of the primary root meristem might be correlated with the size of the root cap [25, 26]. The root cap is the protective outermost tissue of the root meristem and the first plant tissue that experiences environmental conditions while the root traverses the rhizosphere. The root cap is a sensory organ that directs root growth towards or away from environmental cues such as water, gravity, obstacles and nutrients (reviewed in [27]). Lateral root cap cells are connected

Tropic responses affect LR sidedness

The gravitropic response not only accelerates DR5-oscillations, but also affects LR sidedness. When Arabidopsis seedlings are artificially grown on solid plant medium, the primary root grows in a wavy pattern with LRs emerging alternately at the left and right side at the convex side of bends [8]. This wavy growth pattern is due to alternating growth towards gravity and away from the plant medium [39]. Gravity is perceived in the root cap by specialised starch granules (reviewed in [40]). After

Future perspectives

Recently, the root cap has emerged as an essential tissue to control the regular spacing of LRs. Synchronous and periodic PCD in root cap cells might release auxin bursts into the oscillation zone that contributes to the regular spacing of LRs. Interestingly, dying plant tissue was reported to produce auxin in vitro, probably due to the release and subsequent degradation of free tryptophan during protein hydrolysis [45]. This suggests that de novo production of auxin by dying root cap cells

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

The authors thank Maria F. Njo for the original artwork in this review. We are grateful to Laurent Laplaze for helpful discussion and Steffen Vanneste for critical reading of the manuscript. This work was supported by the Omics@vib Marie Curie COFUND fellowship to B.K.M. and by grants from the Interuniversity Attraction Poles Programme (IAP VI/33 and IUAP P7/29 ‘MARS’) initiated by the Belgian Science Policy Office and the Research Foundation-Flanders to T.B. and the Natural Science Foundation

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