Regulation of the Polarity of Protein Trafficking by Phosphorylation

Abstract

The asymmetry of environmental stimuli and the execution of developmental programs at the organism level require a corresponding polarity at the cellular level, in both unicellular and multicellular organisms. In plants, cell polarity is important in major developmental processes such as cell division, cell enlargement, cell morphogenesis, embryogenesis, axis formation, organ development, and defense. One of the most important factors controlling cell polarity is the asymmetric distribution of polarity determinants. In particular, phosphorylation is implicated in the polar distribution of the determinant protein factors, a mechanism conserved in both prokaryotes and eukaryotes. In plants, formation of local gradients of auxin, the morphogenic hormone, is critical for plant developmental processes exhibiting polarity. The auxin efflux carriers PIN-FORMEDs (PINs) localize asymmetrically in the plasma membrane and cause the formation of local auxin gradients throughout the plant. The asymmetry of PIN distribution in the plasma membrane is determined by phosphorylationmediated polar trafficking of PIN proteins. This review discusses recent studies on the role of phosphorylation in polar PIN trafficking.

Inactivation of Plasma Membrane–Localized CDPK-RELATED KINASE5 Decelerates PIN2 Exocytosis and Root Gravitropic Response inArabidopsis

“…Based on the remarkable conservation of kinase domains in the CRK family, it is tempting to speculate that in analogy to the AGC kinases PID, WAG1, WAG2, and D6PK (reviewed in Ganguly et al, 2012), CRKs might contribute to cell type-specific phosphorylation of specific residues in hydrophilic loops of certain PINs and thereby regulate their polar membrane recycling. Thus, homologous members of the CRK family might perform overlapping cell type-specific functions, which could explain the relatively mild developmental effects of the crk5-1 mutation.…”

“…Remarkably, endocytosis of PIN2 from the apical membrane is inhibited by brefeldin in gln1 mutant roots, suggesting that the apical endocytosis pathway is either dependent on or coregulated with the BFA-sensitive GNOM-dependent basal recycling pathway (Teh and Moore, 2007). Recently, Zhang et al (2010) identified two PID-independent phosphorylation sites in the hydrophilic loop of PIN1, which indicates that in addition to already known classes of AGCs (Ganguly et al, 2012), other protein kinases might also be involved in cell type-specific localization of some of the PINs.…”

“…Cellular transport of auxin is controlled by the AUX/LAX influx and PIN-FORMED (PIN) efflux carriers, and the PGP/ABCB (for P-glycoprotein/ATP binding cassette protein subfamily B) transporters, several of which function in conjunction with PINs (reviewed in Kramer, 2004;Bandyopadhyay et al, 2007;Titapiwatanakun and Murphy, 2009). Whereas regulation of polar localization, activity, and stability of auxin carriers and transporters is being deciphered in detail (Friml, 2010;Ganguly et al, 2012), it is less clear how primary sensing of gravity is linked to specific switches in polar auxin transport.…”

Functional Analysis of the Hydrophilic Loop in Intracellular Trafficking of Arabidopsis PIN-FORMED Proteins

“…Three major families of auxin transporters have been identified: AUXIN-RESISTANT1 (AUX1)/AUX1-LIKEs for auxin influx and PIN-FORMED proteins (PINs) and several ATP binding cassette B/P-glycoprotein members for auxin efflux. PINs are particularly important for directional auxin transport and local auxin gradient formation because they localize asymmetrically in the plasma membrane (PM) and dynamically change their intracellular distribution in response to developmental and environmental signals (Grunewald and Friml, 2010;Ganguly et al, 2012b).…”

Genetic Identification of a Second Site Modifier of ctr1-1 that Controls Ethylene-Responsive and Gravitropic Root Growth in Arabidopsis thaliana

“…However, it is noteworthy that the pleiotropic effects of are1-1 are reminiscent of pin2 loss-of-function mutant Luschnig et al, 1998;Muller et al, 1998;Stepanova et al, 2007;Swarup et al, 2007;Utsuno et al, 1998), suggestive of close functional relationship between ARE1 and PIN2. It will be of great interest to test whether ARE1 is involved in posttranscriptional regulation of PIN2 that includes cell-type specific polar localization, stability, endocytosis and activity (Ganguly et al, 2012;Kleine-Vehn and Friml, 2008). An alternative possible mode of action of are1-1 is that it might change the cell-typespecific expression of auxin transporters other than PIN2.…”