Cycling in a crowd: Coordination of plant cell division, growth, and cell fate

Abstract

The reiterative organogenesis that drives plant growth relies on the constant production of new cells, which remain encased by interconnected cell walls. For these reasons, plant morphogenesis strictly depends on the rate and orientation of both cell division and cell growth. Important progress has been made in recent years in understanding how cell cycle progression and the orientation of cell divisions are coordinated with cell and organ growth and with the acquisition of specialized cell fates. We review basic concepts and players in plant cell cycle and division, and then focus on their links to growth-related cues, such as metabolic state, cell size, cell geometry, and cell mechanics, and on how cell cycle progression and cell division are linked to specific cell fates. The retinoblastoma pathway has emerged as a major player in the coordination of the cell cycle with both growth and cell identity, while microtubule dynamics are central in the coordination of oriented cell divisions. Future challenges include clarifying feedbacks between growth and cell cycle progression, revealing the molecular basis of cell division orientation in response to mechanical and chemical signals, and probing the links between cell fate changes and chromatin dynamics during the cell cycle.

Figure 1

Simplified regulatory pathways and cytoskeletal changes in the plant cell cycle. A, The wide arrow (bottom) represents progression through the cell cycle phases (G1, S, G2, M); above, cell cycle regulators mentioned in the main text are placed in simplified pathways that control the G1/S (magenta) and G2/M (green) transitions; blunted lines and arrows represent inhibitory and activating interactions; lines ending in a cross indicate degradation by the proteasome (orange shape); the box within G2/M shows components of the putative plant DREAM complex. B, Cytoskeletal changes required for chromosome segregation and cell division: microtubules (green) are re-organized from the CMT arrays seen in G1, S, and G2, to the PPB, mitotic spindle (SP), and phragmoplast (PHM); chromosomes (magenta) are replicated in S-phase (magenta shading) and segregated in mitosis (green shading); the PPB anticipates the orientation of the SP, PHM and, consequently, of the new cell wall separating the daughter cells.

Figure 2

Coordination between cell cycle and cell size. A, Control of G1 length by size at birth in meristem cells. The KRP4 protein (green) associates with chromosomes (magenta) during mitosis and is released in equal amounts in the daughter cells; cells born small spend more time growing in G1 until KRP4 is diluted sufficiently for progression to S-phase, and consequently cell size differences are corrected by the time cells reach S-phase. B, Relation between cell size and ploidy in the sepal epidermis. Cells that undergo endoreduplication (marked with asterisks on the left) continue to grow while skipping cell divisions; although the cells are larger, their relative growth rate and the concentration of DNA and biosynthetic machinery are comparable to what they would be if the cells had continued to divide (asterisks on the right); in this way, growing tissues maintain a comparable amount of genome copies, regardless of whether they are packaged in diploid or polyploid cells.

Figure 3

Selection of the cell division plane. A, In the absence of external cues, the division plane depends primarily on cell geometry; interactions between MT arrays (green) and the nucleus tend to select the smallest plane that divides the cell approximately in half. B, Mechanical stress, for example caused by growth of interconnected cells, leads to alignment of MTs with the stress orientation (blue arrows), influencing the position of the PPB and the subsequent division. C, Polarity proteins, such as BASL (magenta), activate mechanisms that re-position the nucleus, consequently changing the PPB position and the cell division plane.

Figure 4

Coordination between cell division and cell fate. A, Cell outlines in the Arabidopsis root meristem, indicating the position of specific cell types: the QC is marked in green; magenta marks the CEI, the CEID and the endodermis (E) and cortex (C) cells that result from asymmetric division of the CEID. B, C, Schematic relationships of cell fate genes (magenta) and the cell cycle machinery in the QC (B) and cortex-endodermis (C); JA: jasmonic acid. D, Cell outlines in the developing cotyledon epidermis, with stomatal lineage cells marked in green: the meristemoid (M) divides asymmetrically to renew itself and produce the surrounding stomatal lineage ground cells; the meristemoid eventually changes identity and becomes a guard mother cell, then divides symmetrically to produce two GC, which differentiate into the mature guard cells of a functional stoma. E and F, Schematic relationships of cell fate genes (magenta) and the cell cycle machinery in the stomatal lineage (E) and male gametophyte (F). In B, C, E, and F: thick arrows highlight the final step in cell fate specification, blunted lines and arrows represent inhibitory and activating interactions, respectively, and hormonal signals are marked in green.