Developmental timing in plants

Abstract

Plants exhibit reproducible timing of developmental events at multiple scales, from switches in cell identity to maturation of the whole plant. Control of developmental timing likely evolved for similar reasons that humans invented clocks: to coordinate events. However, whereas clocks are designed to run independently of conditions, plant developmental timing is strongly dependent on growth and environment. Using simplified models to convey key concepts, we review how growth-dependent and inherent timing mechanisms interact with the environment to control cyclical and progressive developmental transitions in plants.

Fig. 1. Cell division according to two rules.

a Cell growing and dividing to form a filament. b As (a) but shown as a continuum, with a snapshot of cells in their final state at the bottom. c, d Effect of reducing growth rate. If cells divide with a fixed cycle duration (c), cell size decreases with time and final cell number remains unchanged. If a cell divides at a fixed threshold size (d), cell cycle duration increases and final cell number decreases. e Growth-dependent timing with random displacement of division wall respect to the middle of the cell in the range $\pm$7.5%. Such random displacement desynchronizes divisions and produces cells at the end with diverse cell cycle phases (different colours) and sizes (though sizes remain within a factor of two of each other).

Fig. 2. Schematic growth and patterning of an indeterminate meristem, illustrated by a one-dimensional filament.

a–c Uniform tissue growth rate and threshold size for division. a Morphogen generated at the right end (apex) forms a gradient. Above threshold T1, cells adopt red identity, between T1 and T2, white identity, and below T2 blue identity. b Tissue growth rate (green line) and size at which cells divide (magenta), are both constant. c Fate of cells generated by a cell or cells at the right end of the filament shown continuously over time, with final cell pattern shown at the bottom. Red and white domains maintain the same size (domain size homeostasis) while the blue domain increases in size over time. Wall thickness increases with time and cells have uniform sizes. d–f Same as (a–c) but with threshold size for division modulated by morphogen concentration to give a rising curve. Cell size increases from right to left, with blue cells no longer dividing as they never reach the increased size threshold. g–i Same as (d–f), but with tissue growth rate modulated by morphogen concentration, with the highest rate at an intermediate concentration. The result of this combination of growth rate and cell division threshold curves is slow-growing small cells in the red domain, faster growing larger cells in the white domain, and slow-growing large cells in the blue domain.

Fig. 3. Generation of repeating units through inherent or growth-dependent timing.

Only the tissue in the red domain grows. a Inherent timing. The red domain cycles between light red and dark red with constant period. Cells adopt white identity when exiting the red domain in the light red state, but blue identity when exiting in the dark red state. Regularly spaced blue domains are generated. b As (a), but at a slower growth rate. Blue domains are spaced more closely, giving smaller repeating units (similar to the timer mechanism for cell division (Fig. 1c)). c Growth-dependent timing. Blue cells produce an inhibitory morphogen that prevents cells exiting the red domain from switching to the blue state. Red-exiting cells switch to white unless the nearest blue cell is sufficiently far away that inhibitory morphogen drops below a critical threshold. Regularly spaced blue domains are generated. d As (c) with slower growth rate. Fewer blue domains are generated but with the same spacing, giving fewer repeating units of the same size (similar to the sizer mechanism for cell division (Fig. 1d)). In (c) and (d), identity at a fixed distance from the end (orange arrow) oscillates between white and blue states through cells being displaced by growth, rather than temporal oscillations happening with the same cell, as in the light-dark red cycles in (a) and (b).

Fig. 4. Generation and timing of phyllotactic patterns.

a, b Development of a distichous pattern of primordia (blue) on a growing shoot apical meristem (grey) with a small central domain (red) exhibiting size homeostasis (red shading in (b)) throughout. Primordia emerge with a constant plastochron. Angle α indicates the angular position of primordia. c, d As (a, b), with radius of the central domain gradually increasing before reaching size homeostasis. A spiral (helical) phyllotactic pattern emerges, with 3 and 5 parastichies running in opposite directions (magenta and yellow, respectively). Plastochron decreases before size homeostasis is reached, and is subject to fluctuations. e, f As (a, b), with the meristem size and the central domain initially expanding in concert, and the central domain subsequently contracting. The resulting pattern has 13 and 21 contact parastichies. In the expansion phase, primordia emerge in bursts, shaded blue in (f), followed by periods in which newly initiated primordia migrate to positions that are asymmetric with respect to their neighbours. g Causal diagram capturing temporal precedence (arrows) between primordia initiation events (circles) necessary for the pattern (e) to emerge. Events not connected by directed paths (e.g., the initiation of primordia (3,4) or (6,8)), are not causally related and can take place in any order.

Fig. 5. Control of timing of transition to floral identity through changes in vegetativeness.

a The model. In a tfl1 mutant inflorescence, veg in the main apex declines rapidly and reaches the floral threshold T_f leading to production of a terminal flower. In wild type (TFL1), veg starts off higher and declines more slowly in the main apex, while veg drops in young lateral meristems (vertical lines). This drop is transient unless it reaches the floral threshold, in which case the meristem switches to floral identity. b–e Examples of inflorescences generated by the model with different parameter values: b, raceme; c, panicle; d, cyme; e, thyrse. f Incorporating environmental controls of flowering time. In early-flowering plants (lower black curve) veg in the main apex approaches floral threshold earlier than in late-flowering plants (upper black curve), leading to generation of a flowering raceme (red line). If late-flowering plants are moved to an environment that induces flowering, veg in the main apex drops (blue line).