Regulation of Division and Differentiation of Plant Stem Cells

Abstract

A major challenge in developmental biology is unraveling the precise regulation of plant stem cell maintenance and the transition to a fully differentiated cell. In this review, we highlight major themes coordinating the acquisition of cell identity and subsequent differentiation in plants. Plant cells are immobile and establish position-dependent cell lineages that rely heavily on external cues. Central players are the hormones auxin and cytokinin, which balance cell division and differentiation during organogenesis. Transcription factors and miRNAs, many of which are mobile in plants, establish gene regulatory networks that communicate cell position and fate. Small peptide signaling also provides positional cues as new cell types emerge from stem cell division and progress through differentiation. These pathways recruit similar players for patterning different organs, emphasizing the modular nature of gene regulatory networks. Finally, we speculate on the outstanding questions in the field and discuss how they may be addressed by emerging technologies.

Keywords: asymmetric divisions; cell identity; meristem; mobile signals; plant stem cells; transcriptional regulation.

Figure 1

An Arabidopsis seedling depicting the developmental organization of (moving counterclockwise from top left) the shoot apical meristem (SAM), root apical meristem (RAM), root developmental zones, and hormone domains of the RAM and SAM. (Top left) The SAM is positioned by the central organizing center (OC), which maintains the stem cells in the overlying central zone (CZ). Cells differentiate into either leaf or shoot cells as they are displaced into the peripheral zone (PZ) or the rib meristem (RM). (Bottom left) The quiescent center (QC) maintains the surrounding stem cells (gray) that give rise to all the tissues in the root. (Bottom center) Actively dividing cells are found in the meristematic zone. The transition to differentiation starts in the elongation zone when cells exit the mitotic cycle and enter a period of endoreduplication. Cells acquire their specialized features, such as root hairs, in the differentiation zone. (Right) The hormones auxin and cytokinin establish juxtaposed signaling domains that regulate division and differentiation in the SAM and RAM.

Figure 2

Hormonal treatment can convert lateral root primordia into shoot primordia and switch the characteristic auxin-cytokinin gradient of a root within a short developmental window. Presented is a schematic of how lateral root primordia responded to hormonal treatments by Rosspopoff et al. (2017) at different developmental stages. Early lateral root primordia are aborted. In contrast, intermediate-stage lateral root primordia transition to accumulate cytokinin in the stem cell niche and grow to resemble a shoot apical meristem. Past a certain stage, lateral root primordia maintain their characteristic auxin-cytokinin domains and emerge as lateral roots.

Figure 3

Transcription factor movement through plasmodesmata. (a) WUSCHEL (WUS) is expressed in the organizing center, and WUS protein (W) moves into central zone stem cells. In those cells, W activates the expression of CLAVATA3 (CLV3), a small signaling peptide that prevents WUS expression outside the organizing center. New evidence suggests that WUS dimers repress CLV3 expression in the organizing center. (b) SHORTROOT (SHR) is expressed in the stele, where it localizes to both the nucleus and cytoplasm. SHR protein (S) moves into the endodermis, where it activates the expression of SCARECROW (SCR). Physical interaction with SCR sequesters S to the nucleus, preventing further movement.

Figure 4

Leaf epidermal cells in various stages of stomatal development. A meristemoid mother cell undergoes the first asymmetric division to produce a meristemoid (M), which continues to divide asymmetrically until it converts into a guard mother cell (GMC). The GMC divides symmetrically to form the two guard cells of the stomatal pore. Each stoma is separated by puzzle piece–shaped pavement cells.