Aquaporins: highly regulated channels controlling plant water relations

Abstract

Plant growth and development are dependent on tight regulation of water movement. Water diffusion across cell membranes is facilitated by aquaporins that provide plants with the means to rapidly and reversibly modify water permeability. This is done by changing aquaporin density and activity in the membrane, including posttranslational modifications and protein interaction that act on their trafficking and gating. At the whole organ level aquaporins modify water conductance and gradients at key "gatekeeper" cell layers that impact on whole plant water flow and plant water potential. In this way they may act in concert with stomatal regulation to determine the degree of isohydry/anisohydry. Molecular, physiological, and biophysical approaches have demonstrated that variations in root and leaf hydraulic conductivity can be accounted for by aquaporins but this must be integrated with anatomical considerations. This Update integrates these data and emphasizes the central role played by aquaporins in regulating plant water relations.

Figure 1.

Regulation of PIPs within the cell. PIP genes are transcribed, their mRNA translated in the rough ER, and the proteins targeted to the plasma membrane (PM). PIPs belonging to the PIP2 group (in yellow) form homo- or heterooligomers by associating with PIP1 isoforms (in green). Some PIP2s contain a diacidic motif (red circle) in their N terminus that is thought to be recognized by the Sec24 subunit of the COPII coat complex of the vesicles budding at the ER membrane and transiting to the Golgi apparatus. PIP oligomers transit through the Golgi apparatus and trans-Golgi network (TGN) and are then loaded into secretory vesicles and routed to the plasma membrane. Insertion of PIPs into the plasma membrane is mediated by the syntaxin SYP121. Internalization of plasma membrane-localized PIPs occurs as a result of constitutive recycling. Once internalized in vesicles, PIPs are delivered to the trans-Golgi network before being routed back to the plasma membrane or directed into lytic vacuoles for degradation. Salt stress causes dephosphorylation and internalization of PIPs, and drought stress induces ubiquitylation of PIPs, which are then degraded in the proteasome. The water channel activity or gating of PIPs is regulated by different mechanisms (heteromerization, phosphorylation, interaction with SYP121, protonation, pressure gradient, and Ca²⁺ concentration). Question marks indicate possible regulation mechanisms not yet supported by experimental evidence. In the bullet is shown the topological structure of an aquaporin monomer (Murata et al., 2000), which consists of six membrane-spanning α-helices (1–6) connected by five loops (A–E) and N and C termini facing the cytosol. The loops B and E form two short hydrophobic α-helices (in red) dipping halfway into the membranes, which, together with the membrane-spanning helices, create a pore with high specificity. Phosphorylated Ser residues are in green circles (the putative phosphorylated Ser in loop D is not indicated), the protonated His of loop D is in a blue circle, and the Cys residue of loop A involved in disulfide bound formation between monomers is in a purple circle. The transcription, translation, trafficking, and gating of PIPs are regulated by environmental and developmental factors involving signaling molecules, phytohormones, and the circadian clock. See text for more details and references.

Figure 2.

Long-distance signaling within plants involving aquaporins to coordinate water demand by the shoot with supply by the roots. On the left side is shown a summary of root-to-shoot signaling that occurs when roots are subjected to water stress. The classic ABA signaling pathway (including a coordinating effect of xylem sap pH; Wilkinson and Davies, 2002) is shown as a direct link to the stomata or through a hydraulic (pressure) signal that releases ABA in the shoot through an as yet unknown transduction process (Christmann et al., 2007). Also shown is an independent ABA signaling mode wherein bundle sheath cells and/or xylem parenchyma cells respond by reducing the activity of aquaporins (Shatil-Cohen et al., 2011; Pantin et al., 2013). This is proposed to convey a hydraulic signal to the stomata. The degree of isohydry/anisohydry (Output, top left) has been hypothesized to potentially reside in the gain of the ABA transduction process (Pantin et al., 2013). On the right side of the diagram is shoot-to-root signaling that appears to regulate L_pr in response to transpiration. The Output graph summarizes observations from various plants (Vandeleur et al., 2014). Increased transpiration increases root aquaporin expression and activity and L_pr (Levin et al., 2009; Sakurai-Ishikawa et al., 2011; Laur and Hacke, 2013), and the signal may be an increase in xylem tension that is rapidly transmitted to roots (McElrone et al., 2007); alternatively, phloem ABA may increase and stimulate root aquaporin activity (Kudoyarova et al., 2011). The method of signal transduction is unknown. Lowered transpiration leads to down-regulation of aquaporin activity and reduced L_pr possibly via release of xylem tension. Shoot wounding may interfere with this feedback system because similar aquaporin transcripts change in response to shoot decapitation, as in response to reduced transpiration (Sakurai-Ishikawa et al., 2011; Vandeleur et al., 2014). Isohydric and anisohydric plants appear to sit on the same linear response of L_pr versus transpiration (Vandeleur et al., 2009), suggesting that the degree of isohydry/anisohydry is more related to the response of the shoot to ABA, though this has not been explicitly tested.