Spatial Regulation of Root Growth: Placing the Plant TOR Pathway in a Developmental Perspective

Abstract

Plant cells contain specialized structures, such as a cell wall and a large vacuole, which play a major role in cell growth. Roots follow an organized pattern of development, making them the organs of choice for studying the spatio-temporal regulation of cell proliferation and growth in plants. During root growth, cells originate from the initials surrounding the quiescent center, proliferate in the division zone of the meristem, and then increase in length in the elongation zone, reaching their final size and differentiation stage in the mature zone. Phytohormones, especially auxins and cytokinins, control the dynamic balance between cell division and differentiation and therefore organ size. Plant growth is also regulated by metabolites and nutrients, such as the sugars produced by photosynthesis or nitrate assimilated from the soil. Recent literature has shown that the conserved eukaryotic TOR (target of rapamycin) kinase pathway plays an important role in orchestrating plant growth. We will summarize how the regulation of cell proliferation and cell expansion by phytohormones are at the heart of root growth and then discuss recent data indicating that the TOR pathway integrates hormonal and nutritive signals to orchestrate root growth.

Keywords: TOR (target of rapamycin); auxin; cell growth; cytokinin; elongation; environment; meristem; plant; proliferation; root.

Figure 1

Root radial patterning of the model flowering plant Arabidopsis thaliana. Differential interference contrast microscopy picture of the A. thaliana primary root tip. Bar 50 µm. Each color corresponds to a different cell layer.

Figure 2

The cellular mechanims involved in primary root zonation. Photomontage of differential interference contrast microscopy pictures of the A. thaliana primary root. Bar 50 µm. The black contours of cortical cells highlight the increase in cell size. Within the apical meristem new cells are formed by successive division (n x: non-initial cells divide n times in the meristem), each preceded by an increase in size corresponding to cell growth. In the basal meristem most cells have stopped dividing and undergo endoreduplication and vacuolization at the initiation of cell expansion. In the elongation zone all cells have stopped dividing and expand rapidly. In the maturation zone, cells have reached their final length and some specialized epidermal cells go through polarized cell enlargement leading to the formation of root hairs.

Figure 3

Proposed model of the complex interplay between hormones and cellular growth regulators during root growth. In each zone of the root, hormones induce specific regulatory processes that influence cell cycle progression or cell expansion (see main text for details). Bar 50 µm.

Figure 4

Schematic model of hormonal transport and auxin and PLETHORA gradients in the root (see main text for details).

Figure 5

TOR is expressed in the meristem and the QC and regulates meristem size and the zone of CYCB1;1 expression in the apical meristem. Differential interference contrast microscopy pictures of GUS stained A. thaliana primary roots showing the meristem, delimitated by black arrows. (A,B) Expression of TOR:GUS in roots of 4 days-old plants stained for 4 h [97]; (B) Evidence of TOR:GUS expression in the quiescent center; and (C) Effect of asTORis on CYCB1;1-GUS expression in A. thaliana roots. Pictures were taken 2 days after transfer of 3 days-old plants onto medium containing the indicated concentrations of asTORi (µM) (from Montané and Menand, 2013 [1]). Bars, 50 µm (A–C).

Figure 6

Proposed model of TOR involvement in the regulation of proliferation and growth in the primary root. Plane arrows indicate a proven regulation, whereas doted arrows represent hypothesis that have not been verified yet or which are based on experiments made on other tissues (see main text for details). Bar 50 µm.