Aquaporins: Highly Regulated Channels Controlling Plant Water Relations

Chaumont, François; Tyerman, Stephen D.

doi:10.1104/pp.113.233791

Cited by 560 publications

(470 citation statements)

References 210 publications

(341 reference statements)

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“…This raises a question regarding the hierarchy of the hydraulic signal cascade controlling leaf water status (for review, see Chaumont and Tyerman, 2014).…”

Section: Bs-mesophyll Hydraulic Feed-forward Signalmentioning

confidence: 99%

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The Role of Plasma Membrane Aquaporins in Regulating the Bundle Sheath-Mesophyll Continuum and Leaf Hydraulics

et al. 2014

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Our understanding of the cellular role of aquaporins (AQPs) in the regulation of whole-plant hydraulics, in general, and extravascular, radial hydraulic conductance in leaves (K leaf ), in particular, is still fairly limited. We hypothesized that the AQPs of the vascular bundle sheath (BS) cells regulate K leaf . To examine this hypothesis, AQP genes were silenced using artificial microRNAs that were expressed constitutively or specifically targeted to the BS. MicroRNA sequences were designed to target all five AQP genes from the PLASMA MEMBRANE-INTRINSIC PROTEIN1 (PIP1) subfamily. Our results show that the constitutively silenced PIP1 (35S promoter) plants had decreased PIP1 transcript and protein levels and decreased mesophyll and BS osmotic water permeability (P f ), mesophyll conductance of CO 2 , photosynthesis, K leaf , transpiration, and shoot biomass. Plants in which the PIP1 subfamily was silenced only in the BS (SCARECROW:microRNA plants) exhibited decreased mesophyll and BS P f and decreased K leaf but no decreases in the rest of the parameters listed above, with the net result of increased shoot biomass. We excluded the possibility of SCARECROW promoter activity in the mesophyll. Hence, the fact that SCARECROW:microRNA mesophyll exhibited reduced P f , but not reduced mesophyll conductance of CO 2 , suggests that the BS-mesophyll hydraulic continuum acts as a feed-forward control signal. The role of AQPs in the hierarchy of the hydraulic signal pathway controlling leaf water status under normal and limited-water conditions is discussed.

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“…This raises a question regarding the hierarchy of the hydraulic signal cascade controlling leaf water status (for review, see Chaumont and Tyerman, 2014).…”

Section: Bs-mesophyll Hydraulic Feed-forward Signalmentioning

confidence: 99%

“…A N , Photosynthesis; C i , substomatal CO 2 concentration. Shatil-Cohen et al, 2011;Pantin et al, 2013; for review, see Chaumont and Tyerman, 2014). Under these conditions, decreases in AQP expression or activity in the BS should result in reduced water influx and decreased C leaf .…”

Section: Bs-mesophyll Hydraulic Feed-forward Signalmentioning

confidence: 99%

The Role of Plasma Membrane Aquaporins in Regulating the Bundle Sheath-Mesophyll Continuum and Leaf Hydraulics

et al. 2014

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“…These assumptions are that the water permeabilities of the plasma membrane and tonoplast are high, so water flux normally equilibrates rapidly with respect to ion transport, and that the apoplast of the cell wall space surrounding the guard cells provides a near-infinite reservoir for solutes uninfluenced by material entering or emanating from the guard cell. The first assumption is founded on reliable data (Hill and Findlay, 1981;Willmer and Fricker, 1996;Maurel, 1997;Chaumont and Tyerman, 2014;Maurel et al, 2015); it allows guard cell volume and turgor to be resolved from the Van't Hoff relation with stomatal aperture from empirical relations of steady state experimental measurements . The second assumption greatly simplifies a treatment of ion transport across the plasma membrane, leaving the external ion composition and the associated osmotic potential, C iso , to be defined by the user.…”

Section: Rationale For the Modeling Approachmentioning

confidence: 99%

Unexpected Connections between Humidity and Ion Transport Discovered Using a Model to Bridge Guard Cell-to-Leaf Scales

et al. 2017

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Stomatal movements depend on the transport and metabolism of osmotic solutes that drive reversible changes in guard cell volume and turgor. These processes are defined by a deep knowledge of the identities of the key transporters and of their biophysical and regulatory properties, and have been modeled successfully with quantitative kinetic detail at the cellular level. Transpiration of the leaf and canopy, by contrast, is described by quasilinear, empirical relations for the inputs of atmospheric humidity, CO 2 , and light, but without connection to guard cell mechanics. Until now, no framework has been available to bridge this gap and provide an understanding of their connections. Here, we introduce OnGuard2, a quantitative systems platform that utilizes the molecular mechanics of ion transport, metabolism, and signaling of the guard cell to define the water relations and transpiration of the leaf. We show that OnGuard2 faithfully reproduces the kinetics of stomatal conductance in Arabidopsis thaliana and its dependence on vapor pressure difference (VPD) and on water feed to the leaf. OnGuard2 also predicted with VPD unexpected alterations in K + channel activities and changes in stomatal conductance of the slac1 Cl 2 channel and ost2 H + -ATPase mutants, which we verified experimentally. OnGuard2 thus bridges the micro-macro divide, offering a powerful tool with which to explore the links between guard cell homeostasis, stomatal dynamics, and foliar transpiration. INTRODUCTIONStomata provide the main pathway for CO 2 entry for photosynthesis and for transpirational water loss across the leaf epidermis. Pairs of guard cells surround each stoma, regulating the aperture to balance the often conflicting demands for CO 2 and for water conservation. Guard cells open and close the pore, driven by osmotic solute uptake and loss, notably of K + and Cl 2 , and by the synthesis and metabolism of organic solutes, especially sucrose (Suc) and malate (Mal) (Willmer and Fricker, 1996;Kim et al., 2010;Roelfsema and Hedrich, 2010;Lawson and Blatt, 2014;Jezek and Blatt, 2017). A number of well-defined signals, including light, CO 2 , and the water stress hormone abscisic acid (ABA), modulate transport and solute accumulation to alter cell volume, turgor, and stomatal aperture. Much research at the cellular level has focused on these inputs and their connection to stomatal movements, especially stomatal closing. Studies have highlighted both Ca 2+ -independent and Ca 2+ -dependent signaling, including elevated free cytosolic Ca 2+ concentration ([Ca 2+ ] i ), cytosolic pH (pH i ), protein kinases, and phosphatases, that inactivate inward-rectifying K + channels and activate Cl 2 channels and outward-rectifying K + channels to bias the membrane for solute loss (Blatt et al., 1990;Lemtiri-Chlieh and MacRobbie, 1994; Blatt, 1998, 1999;Marten et al., 2007;Assmann and Jegla, 2016;Jezek and Blatt, 2017).At the tissue and whole-plant levels, by contrast, attention has been drawn to inputs closely tied to photosynthesis, including tra...

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“…[1][2][3] Aquaporins of the plasma membrane intrinsic protein (PIP) subfamily have classically been described as localized in the plasma membrane (PM). 4,5 However, when expressed alone in maize (Zea mays) cells, PIP proteins belonging to the ZmPIP1 and ZmPIP2 groups display distinct subcellular localization patterns.…”

mentioning

confidence: 99%

The LxxxA motif in the third transmembrane helix of the maize aquaporin ZmPIP2;5 acts as an ER export signal

Chevalier

Chaumont

2015

Plant Signaling & Behavior

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Aquaporins: Highly Regulated Channels Controlling Plant Water Relations

Cited by 560 publications

References 210 publications

The Role of Plasma Membrane Aquaporins in Regulating the Bundle Sheath-Mesophyll Continuum and Leaf Hydraulics

The Role of Plasma Membrane Aquaporins in Regulating the Bundle Sheath-Mesophyll Continuum and Leaf Hydraulics

Unexpected Connections between Humidity and Ion Transport Discovered Using a Model to Bridge Guard Cell-to-Leaf Scales

The LxxxA motif in the third transmembrane helix of the maize aquaporin ZmPIP2;5 acts as an ER export signal

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