Cellular responses to auxin: division versus expansion

Abstract

The phytohormone auxin is a major regulator of plant growth and development. Many aspects of these processes depend on the multiple controls exerted by auxin on cell division and cell expansion. The detailed mechanisms by which auxin controls these essential cellular responses are still poorly understood, despite recent progress in the identification of auxin receptors and components of auxin signaling pathways. The purpose of this review is to provide an overview of the present knowledge of the molecular mechanisms involved in the auxin control of cell division and cell expansion. In both cases, the involvement of at least two signaling pathways and of multiple targets of auxin action reflects the complexity of the subtle regulation of auxin-mediated cellular responses. In addition, it offers the necessary flexibility for generating differential responses within a given cell depending on its developmental context.

Figure 1.

From cell proliferation to differentiation. Within plant meristems and cambial zones, new cells are formed by division. Between two successive rounds of division, the increase in size of these cells corresponds to cell growth. The main enlargement occurs after cells have left the meristem and often relies on a combination of two distinct processes: endoreplication and cell expansion. Cell expansion is an increase in cell size through vacuolization and enlargement of the vacuole leading to differentiation.

Figure 2.

Auxin and the G1/S transition. The cell cycle is divided into four phases: DNA replication (S), mitosis (M), and two Gap phases (G1 and G2, between M/S, and S/M, respectively). The cycle starts in G1. During this phase, expression of D-type cyclins and cyclin-dependent kinase (CDKA) is induced by various signals including auxin. The CDKA/CYCD complex is activated by phosphorylation but can still be blocked by CDK inhibitors (KRP). Auxin was reported to reduce the expression of some KRPs. The active CDK/CYCD complex provokes phosphorylation of the transcriptional repressor retinoblastoma-related protein (RBR) thus promoting expression of genes essential for the beginning of the S phase under the control of the E2FA/B and DPA complex. Auxin was shown to stabilize these transcriptional regulators. Later in S phase, E2Fc and DPB repress expression of S phase genes. Degradation of these proteins is under the control of the E3 ubiquitine ligase SCF^SKP2 and auxin was shown to increase the degradation of the F-box SKP2, thus indirectly stabilizing E2FC and DPB.

Figure 3.

Auxin-induced cell wall loosening and expansion. The scheme represents the cell wall/plasma membrane/cytoskeleton continuum and the consequences of auxin action. Auxin is perceived by the auxin receptor ABP1, which interacts with unknown membrane-associated proteins at the plasma membrane (such as the putative candidate GPI-anchored protein CBP1) (Shimomura 2006). This activates the proton pump ATPase, provoking the acidification (H⁺) of the extracellular space, the activation of cell wall proteins such as expansins and xyloglucan endotransglycosylase/hydrolases (XTH), which mediate cell wall loosening by acting on the cell wall polysaccharide network. Polysaccharides forming the cell wall are cellulose microfibrils, cross-linked hemicelluloses, and pectins. Activation of the H+ ATPase also induces hyperpolarization of the plasma membrane and activation of K+ inward rectifying channels, essential for the uptake of water sustaining cell expansion. Auxin also enhances these effects by inducing the expression of genes encoding plasma membrane ATPase, K+ channels, expansins, and cell wall remodelling enzymes and promotes exportation of new cell wall material. Auxin is likely to act on actin microfilaments and microtubules via the modulation of ROP GTPases.