Multiple roles for membrane-associated protein trafficking and signaling in gravitropism

Abstract

Gravitropism is a process that allows plant organs to guide their growth relative to the gravity vector. It requires them to sense changes in their orientation and generate a biochemical signal that they transmit to the tissues that drive organ curvature. Trafficking between the plasma membrane and endosomal compartments is important for all of these phases of the gravitropic response. The sedimentation of starch-filled organelles called amyloplasts plays a key role in sensing reorientation, and vacuolar integrity is required for amyloplast sedimentation in shoots. Other proteins associated with the vesicle trafficking pathway contribute to early gravity signal transduction independently of amyloplast sedimentation in both roots and hypocotyls. Phosphatidylinositol signaling, which starts at the plasma membrane and later affects the localization of auxin efflux facilitators, is a likely second messenger in the signal transduction phase of gravitropism. Finally, membrane-localized auxin influx and efflux facilitators contribute to a differential auxin gradient across the gravistimulated organs, which directs root curvature.

Keywords: Arabidopsis; PIN; auxin transport; endomembrane; gravitropism; phosphatidylinositol; trafficking; vacuole.

FIGURE 1

Cellular control of auxin carriers. (A) Phosphorylation by PINOID kinase and dephosphorylation by PP2A regulate PIN protein localization. (B) PIN proteins are removed from the plasma membrane through clathrin-mediated endocytosis into endocytic compartments. (C) PIN proteins may also be ubiquitylated and targeted to the vacuole via PVCs for degradation. (D) Alternatively, following endocytosis PIN proteins may be exocytosed in a selective, polar manner that requires the activity of an unidentified ARF GTPase. The activity of the GTPase is controlled by a GEF called GNOM, which removes the used GDP and allows fresh GTP to reload. (E) Treating plants with BFA inhibits GNOM, which likely inactivates the ARF GTPase. As a result, PIN proteins accumulate in intracellular aggregates termed BFA bodies. (F) Auxin can be actively transported across the plasma membrane. PIN proteins are gradient-powered auxin efflux carriers. Members of the ABC transporter family are ATP-driven and act as either auxin influx or efflux facilitators. AUX1 and its relative LAX are auxin influx carriers that use an existing ion gradient to allow auxin into cells.

FIGURE 2

Gravitropism overview. The steps of gravitropism are shown down the center core of the diagram. During plant reorientation, a plant is rotated relative to the gravity vector. This results in the sedimentation of dense amyloplasts within the statocytes. In roots the statocytes are the columella cells, whereas in stems they are the endodermal cells. Each endodermal cell contains a large vacuole, and the amyloplasts must traverse it by tunneling through transvacuolar strands in order to reach the new lower side of the cell. This requires proper vacuole structure, which the SGR proteins mediate. Amyloplast sedimentation is then thought to activate signal transduction through second messengers, possibly calcium ions or protons. Another second messenger is InsP₃, which is produced by cleavage of the phospholipid, PIP₂. In a process that is not completely understood, the second messengers activate the relocalization of auxin transporters, such as PIN3 and PIN7 in the columella cells. The new polarized distribution of these auxin efflux carriers changes the flow of auxin throughout the plant. This differential auxin transport affects cell elongation rates, thereby resulting in organ curvature as the plant grows.