The High Road and the Low Road: Trafficking Choices in Plants
2007; Cell Press; Volume: 130; Issue: 6 Linguagem: Inglês
10.1016/j.cell.2007.09.003
ISSN1097-4172
Autores Tópico(s)Plant nutrient uptake and metabolism
ResumoPolar transport of the signaling molecule auxin is critical for plant development and depends on both the polar distribution of auxin efflux carriers, which pump auxin out of the cell and the alignment of these polarized cells. Two papers in this issue of Cell (Michniewicz et al., 2007Michniewicz M. Zago M.K. Abas L. Weijers D. Schweighofer A. Meskiene I. Heisler M.G. Ohno C. Zhang J. Huang F. et al.Cell. 2007; (this issue)PubMed Google Scholar, Jaillais et al., 2007Jaillais Y. Santambrogio M. Rozier F. Fobis-Loisy I. Miège C. Gaude T. Cell. 2007; (this issue)PubMed Google Scholar) address how polar transport of these carriers occurs and describe the endosomal pathways involved. Polar transport of the signaling molecule auxin is critical for plant development and depends on both the polar distribution of auxin efflux carriers, which pump auxin out of the cell and the alignment of these polarized cells. Two papers in this issue of Cell (Michniewicz et al., 2007Michniewicz M. Zago M.K. Abas L. Weijers D. Schweighofer A. Meskiene I. Heisler M.G. Ohno C. Zhang J. Huang F. et al.Cell. 2007; (this issue)PubMed Google Scholar, Jaillais et al., 2007Jaillais Y. Santambrogio M. Rozier F. Fobis-Loisy I. Miège C. Gaude T. Cell. 2007; (this issue)PubMed Google Scholar) address how polar transport of these carriers occurs and describe the endosomal pathways involved. Polar transport of the plant hormone auxin mediates axis formation in organ establishment, directional growth responses (tropisms), and numerous other processes. Plant cells display an unequal distribution of auxin efflux carriers at their surface such that the aligned polarity of the auxin-secreting cells imposes directionality on auxin transport. Important components of the auxin efflux machinery include integral plasma-membrane proteins named PINs whose localization correlates well with polar auxin transport. PIN proteins are dynamically relocated during development, and individual PINs display different, tissue-specific preferences for one particular side of a cell. For example, the PIN1 protein is localized at the basal end of inner cells, facilitating auxin flow toward the root pole. In contrast, PIN1 and PIN2 proteins accumulate at the apical end of epidermal cells, facilitating auxin flow toward the shoot pole. Such distinct localization patterns suggest the presence of protein-targeting pathways of considerable complexity. PIN proteins are indeed continuously trafficked through endosomal compartments, which is central to their correct localization and function (Geldner et al., 2003Geldner N. Anders N. Wolters H. Keicher J. Kornberger W. Muller P. Delbarre A. Ueda T. Nakano A. Jürgens G. Cell. 2003; 112: 219-230Abstract Full Text Full Text PDF PubMed Scopus (837) Google Scholar). However, the mechanism of apical versus basal targeting of PIN proteins is poorly understood as are the specific sorting signals of PINs and the endosomal compartments that are part of their trafficking routes. Two papers in this issue of Cell (Jaillais et al., 2007Jaillais Y. Santambrogio M. Rozier F. Fobis-Loisy I. Miège C. Gaude T. Cell. 2007; (this issue)PubMed Google Scholar, Michniewicz et al., 2007Michniewicz M. Zago M.K. Abas L. Weijers D. Schweighofer A. Meskiene I. Heisler M.G. Ohno C. Zhang J. Huang F. et al.Cell. 2007; (this issue)PubMed Google Scholar) now shed light on these aspects of PIN polar transport and help us to appreciate the distinct nature of plant endosomal trafficking. An initial hint at signals guiding PIN trafficking was provided by the discovery that overexpression or inactivation of the serine threonine protein kinase PINOID (PID) promoted apical or basal localization of PIN1, respectively, suggesting a major role of phosphorylation in targeting PIN proteins to opposite cell surfaces (Friml et al., 2004Friml J. Yang X. Michniewicz M. Weijers D. Quint A. Tietz O. Benjamins R. Ouwerkerk P.B. Ljung K. Sandberg G. et al.Science. 2004; 306: 862-865Crossref PubMed Scopus (554) Google Scholar). PID kinase interacts with and appears to be activated by the membrane-associated 3-phosphoinositide-dependent protein kinase 1 (PDK1) (Zegzouti et al., 2006Zegzouti H. Anthony R.G. Jahchan N. Bögre L. Christensen S.K. Proc. Natl. Acad. Sci. USA. 2006; 103: 6404-6409Crossref PubMed Scopus (91) Google Scholar). Michniewicz et al., 2007Michniewicz M. Zago M.K. Abas L. Weijers D. Schweighofer A. Meskiene I. Heisler M.G. Ohno C. Zhang J. Huang F. et al.Cell. 2007; (this issue)PubMed Google Scholar now report antagonistic effects of PID kinase and trimeric serine threonine protein phosphatase 2A (PP2A) on PIN localization. PP2As have a fairly broad spectrum of activity, which is controlled by their regulatory subunits. In the model plant Arabidopsis, mutations in two regulatory A subunits display severe pleiotropic phenotypes (Zhou et al., 2004Zhou H.W. Nussbaumer C. Chao Y. DeLong A. Plant Cell. 2004; 16: 709-722Crossref PubMed Scopus (76) Google Scholar). Following the identification of an A subunit isoform that modifies the action of an auxin transport inhibitor, the authors now analyze knockouts of two or three regulatory A subunits as well as knock-down of these subunits through RNA interference (RNAi). These plants have defects in root development and PIN localization similar to the defects caused by PID overexpression or by multiple mutations in PIN genes. In addition, PID and PP2A subunit A partially colocalized with PIN1 and PIN2 at the plasma membrane, suggesting that PIN proteins might be direct substrates of these opposing enzymes. Indeed, PID could phosphorylate PIN proteins in vitro, and PID overexpression or pp2aa mutations increased PIN protein phosphorylation (on serine or threonine residues in the central hydrophilic loop) in vivo. Taken together, these results suggest that PIN proteins accumulate at the apical plasma membrane if PID activity is high, but at the basal plasma membrane if PID activity is low. It remains to be determined whether PP2A is specific to this process and whether it prevents activation of PID by autophosphorylation (Zegzouti et al., 2006Zegzouti H. Anthony R.G. Jahchan N. Bögre L. Christensen S.K. Proc. Natl. Acad. Sci. USA. 2006; 103: 6404-6409Crossref PubMed Scopus (91) Google Scholar) or counteracts PID by directly acting on PIN proteins. However, targeting of PIN appears to be more complex than this. When both PIN1 and PIN2 are expressed in the same cell of the root epidermis, they accumulate at opposite ends suggesting that the presence and localization of PID in itself does not determine PIN targeting (Wisniewska et al., 2006Wisniewska J. Xu J. Seifertova D. Brewer P.B. Ruzicka K. Blilou I. Rouquie D. Benkova E. Scheres B. Friml J. Science. 2006; 312: 883Crossref PubMed Scopus (616) Google Scholar). It is also unclear whether broad localization of PP2A confers any spatial regulation or simply fulfils a crucial, but possibly constitutive function of counteracting PID. Targeting of PIN1 protein to the basal plasma membrane requires PIN1 recycling from the plasma membrane to endosomes and is mediated by GNOM, an endosomal GDP/GTP exchange factor for ARF GTPases (Geldner et al., 2003Geldner N. Anders N. Wolters H. Keicher J. Kornberger W. Muller P. Delbarre A. Ueda T. Nakano A. Jürgens G. Cell. 2003; 112: 219-230Abstract Full Text Full Text PDF PubMed Scopus (837) Google Scholar). In contrast, PIN2 is transported through endosomes expressing SORTING NEXIN 1 (SNX1), which are sensitive to the phosphatidylinositol-3-OH kinase (PI-3K) inhibitor wortmannin and distinct from GNOM-positive endosomes (Jaillais et al., 2006Jaillais Y. Fobis-Loisy I. Miège C. Rollin C. Gaude T. Nature. 2006; 443: 106-109Crossref PubMed Scopus (263) Google Scholar). SNX1 is a component of the conserved retromer complex, which mediates retrograde transport from endosomal multivesicular bodies to the trans-Golgi network in yeast and mammals (Bonifacino and Rojas, 2006Bonifacino J.S. Rojas R. Nat. Rev. Mol. Cell Biol. 2006; 7: 568-579Crossref PubMed Scopus (462) Google Scholar; Figure 1, left). In their new work, Jaillais et al., 2007Jaillais Y. Santambrogio M. Rozier F. Fobis-Loisy I. Miège C. Gaude T. Cell. 2007; (this issue)PubMed Google Scholar address the trafficking role of VPS29, which is the retromer component in Arabidopsis that exists as a single copy and has been localized to multivesicular bodies in plants (Oliviusson et al., 2006Oliviusson P. Heinzerling O. Hillmer S. Hinz G. Tse Y.C. Jiang L. Robinson D.G. Plant Cell. 2006; 18: 1239-1252Crossref PubMed Scopus (133) Google Scholar). Plant vps29 mutants are affected in vacuolar trafficking of a storage protein, consistent with a conserved retromer function (Shimada et al., 2006Shimada T. Koumoto Y. Li L. Yamazaki M. Kondo M. Nishimura M. Hara-Nishimura I. Plant Cell Physiol. 2006; 47: 1187-1194Crossref PubMed Scopus (113) Google Scholar). Surprisingly, Jaillais et al. now observe intracellular accumulation of PIN1 and, to a lesser degree, PIN2 (but not that of several other plasma membrane-localized proteins) in vps29 mutants. This finding suggested that VPS29 is involved in PIN endosomal recycling. Indeed, VPS29 colocalized with SNX1 and mammalian Rab5-related endosomal RabF2. Furthermore, SNX1-positive, but not GNOM-positive, endosomes were morphologically altered in vps29 mutants. Additional data suggested that endocytosed PIN1 might first traffic through GNOM-positive endosomes and then be recycled through SNX1-positive endosomes to the plasma membrane. The authors propose a new role for the retromer in cargo-selective, endosomal recycling to the plasma membrane (Figure 1, middle). However, the results are also consistent with an alternative scenario that would be more in line with the known function of the retromer in endosome-trans-Golgi network trafficking. Inactivation of the retromer would cause inhibition of anterograde traffic from the trans-Golgi network, which in plants acts as an early endosome (Dettmer et al., 2006Dettmer J. Hong-Hermesdorf A. Stierhof Y.-D. Schumacher K. Plant Cell. 2006; 18: 715-730Crossref PubMed Scopus (617) Google Scholar) and thus could impair recycling of endocytosed cargo indirectly (Figure 1, right). The dependence of PIN recycling on retromer activity has an interesting parallel in animals. Long-range gradient formation of the signaling molecule Wnt in the nematode Caenorhabditis elegans and in mammals seems to require retromer function, but the mechanistic details are not as well understood in this case. These two new studies provide starting points for future mechanistic analysis of the amazingly flexible specification of apical-basal polarity in plants. One problem to address is how phosphorylation of PIN1 affects endosomal sorting and how phosphorylated PIN1 is diverted from the basal GNOM-dependent pathway to the apical recyling pathway. The phosphorylated PIN1 protein might provide a useful tool to identify compartments and mechanisms of the apical recycling pathway. In this context, it will be important to see how retromer function and the SNX1 endosomal compartment are involved in this trafficking decision. Finally, both of these new papers use the Arabidopsis root meristem for their studies and testify to the power of this system for the elucidation of axial polarity in plants, comparable to Madin-Darby Canine Kidney (MDCK) cultured epithelial cells that have been instrumental in studying epithelial polarity in mammals. Antagonistic Regulation of PIN Phosphorylation by PP2A and PINOID Directs Auxin FluxMichniewicz et al.CellSeptember 21, 2007In BriefIn plants, cell polarity and tissue patterning are connected by intercellular flow of the phytohormone auxin, whose directional signaling depends on polar subcellular localization of PIN auxin transport proteins. The mechanism of polar targeting of PINs or other cargos in plants is largely unidentified, with the PINOID kinase being the only known molecular component. Here, we identify PP2A phosphatase as an important regulator of PIN apical-basal targeting and auxin distribution. Genetic analysis, localization, and phosphorylation studies demonstrate that PP2A and PINOID both partially colocalize with PINs and act antagonistically on the phosphorylation state of their central hydrophilic loop, hence mediating PIN apical-basal polar targeting. Full-Text PDF Open Archive
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