Regulation of cell division and expansion by sugar and auxin signaling

Abstract

Plant growth and development are modulated by concerted actions of a variety of signaling molecules. In recent years, evidence has emerged on the roles of sugar and auxin signals network in diverse aspects of plant growth and development. Here, based on recent progress of genetic analyses and gene expression profiling studies, we summarize the functional similarities, diversities, and their interactions of sugar and auxin signals in regulating two major processes of plant development: cell division and cell expansion. We focus on roles of sugar and auxin signaling in both vegetative and reproductive tissues including developing seed.

Keywords: auxin signaling; cell division; cell expansion; seed development; sugar signaling.

FIGURE 1

Glucose and auxin signal in cell cycle regulation (modified from Perrot-Rechenmann, 2010, Figure 2). 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). Some plant cells may skip the M phase under certain developmental processes, resulting “endoreduplication.” Cell cycle starts in G1. During this phase, Glc and auxin signals could induce the expression of CycD, while auxin is also able to increase CDKA transcription. The CycD/CDKA complex is activated by phosphorylation but can still be blocked by CDK inhibitor KRPs. Auxin was reported to reduce the expression of some KRPs. The active CycD/CDKA complex provokes phosphorylation of the transcriptional repressor RBR, and release the transcription regulator E2FA/B and DPA complex. By post-transcriptional regulation, auxin stabilizes the E2FA/B and DPA complex, which promote the expression of genes essential for the beginning of the S phase. The expression of CycA3 could be up-regulated by Glc signal, which is required to drive the cells from G1 to S phase. Auxin was shown to increase the degradation of the F-box SKP2 later in S phase, which indirectly stabilizes E2FC/DPB complex, and represses the S phase genes expression. As cell cycle processes into G2 phase, Glc signal was found to initiate the G2/M transition by repressing TSS transcription, and activating the expression of key cell cycle genes, such as CycB and CycD. Auxin signal is required for the initiation and completion of mitosis, probably though an unknown pathway independent or in parallel to Glc. Auxin is also likely to emit a negative signal to prevent cell from going into endoreduplication hence sustaining cell divisions. Glc and Auxin in italic indicate regulation at transcription level and those in non-italic suggest regulation at protein level.

FIGURE 2

Sugar and auxin signal in regulating sink cell expansion (modified from Perrot-Rechenmann, 2010, Figure 3). Unloaded Suc in sink tissues may enter into recipient cells either apoplasmically through cell wall matrix or symplasmically via plasmodesmatal. In the former case, sucrose could be taken up by sucrose transporter on plasma membrane, or be hydrolyzed by cw-Inv into Glc and Fru, and then be transported into cells by hexose transporter (HT). Apoplasmic Glc could be recognized by RGS1, which transmits extracellular sugar signal into the cell through G-proteins. In cytoplasm, Suc may be hydrolyzed by cyto-Inv or degraded by Sus. In the present of high Suc level, Sus intends to bind actin filaments and form a multi-protein complex bound to plasma membrane, which may facilitate cell expansion by providing UDPG for cellulose/callose biosynthesis. Cytoplasmic Suc could also be transported into nucleus, vacuole, plastid or mitochondrion. In vacuole, Suc could be hydrolyzed by vac-Inv, thus doubling the osmotic contribution of Suc, which has the potential to positively impact on cell turgor. Moreover, vac-Inv could also promote cell expansion via sugar signaling involving WAKs, which subsequently activates MPK3 in nucleus, and induces downstream gene expression for cell wall biosynthesis. Suc hydrolysis in vacuole could also regulates nuclear gene transcription, involving in auxin biosynthesis, distribution and signaling. An Arabidopsis cyto-Inv isoform was found in nucleus, where it interacts with and negatively regulated by a phosphatidylinositol monophosphate 5-kinase (AtPIP5K9). Hexoses generated by cyto-Inv could be sensed by a nuclear-localized HXK, producing a Glc signaling complex core combining VHA-B1 and RPT5B, which is sequentially integrated into a signal/metabolites loop modulating cell expansion. Auxin is perceived by the auxin receptor ABP1, which interacts with unknown membrane-associated proteins at the plasma membrane [such as glycosylphosphatidylinositol (GPI)-anchored protein C-terminal peptide-binding protein 1. (CBP1)]. This activates the proton pump ATPase, acidifying extracellular space for optimal function of expansins and XTH and activating K⁺ inward rectifying channels, essential for water uptake to sustain cell expansion. Auxin could also enhance these effects by promoting the transcription of these genes. Moreover, auxin is likely to act on actin microfilaments and microtubules via the modulation of ROP GTPases, thereby affecting vesicle delivery to plasma membrane and cell wall matrix.