Intracellular pH sensing is altered by plasma membrane PIP aquaporin co-expression

Bellati, Jorge; Alleva, Karina; Soto, Gabriela; Vitali, Victoria Andrea; Jozefkowicz, Cintia; Amodeo, Gabriela

doi:10.1007/s11103-010-9658-8

Cited by 71 publications

(111 citation statements)

References 57 publications

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“…VPD-driven changes in guard cell volume connect with ion transport through the concurrent effects on ion concentration within the cytosol and vacuole, notably through changes in [Ca 2+ ] i and pH i , both of which are known to affect the osmotic conductance of the plasma membrane (Alleva et al, 2006;Verdoucq et al, 2008;Bellati et al, 2010;Maurel et al, 2015). In OnGuard2, such regulatory feedback is incorporated explicitly.…”

Section: Discussionmentioning

confidence: 99%

“…There is a general consensus that the activity of plasma membrane aquaporins, and osmotic permeability generally, is suppressed only as cytosolic pH approaches a value of 7.0 and below (Tournaire-Roux et al, 2003;Verdoucq et al, 2008;Bellati et al, 2010;Maurel et al, 2015). However, quantitative information relevant to aquaporin regulation by [Ca 2+ ] i is scant and quantitatively conflicted although, again, there is general agreement that elevated [Ca 2+ ] i inhibits aquaporin activity.…”

Section: Water Flux Across the Guard Cell Plasma Membranementioning

confidence: 99%

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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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Section: Discussionmentioning

confidence: 99%

Section: Water Flux Across the Guard Cell Plasma Membranementioning

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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“…Compared with mammals, plants express a high number of aquaporin isoforms, underlining their fundamental roles in growth, development, and abiotic stress tolerance Gomes et al, 2009;Heinen et al, 2009). Among the plant aquaporins, the plasma membrane intrinsic proteins (PIPs) are subdivided into two sequencerelated groups, PIP1s and PIP2s, the members of which exhibit different water channel activities when expressed in Xenopus laevis oocytes (Chaumont et al, 2000;Temmei et al, 2005;Vandeleur et al, 2009;Bellati et al, 2010;Otto et al, 2010). When expressed alone, maize (Zea mays) PIP1s are inactive, whereas Zm-PIP2s cause a marked increase in the osmotic water permeability coefficient, P f .…”

Section: Introductionmentioning

confidence: 99%

Selective Regulation of Maize Plasma Membrane Aquaporin Trafficking and Activity by the SNARE SYP121

et al. 2012

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Plasma membrane intrinsic proteins (PIPs) are aquaporins facilitating the diffusion of water through the cell membrane. We previously showed that the traffic of the maize (Zea mays) PIP2;5 to the plasma membrane is dependent on the endoplasmic reticulum diacidic export motif. Here, we report that the post-Golgi traffic and water channel activity of PIP2;5 are regulated by the SNARE (for soluble N-ethylmaleimide-sensitive factor protein attachment protein receptor) SYP121, a plasma membrane resident syntaxin involved in vesicle traffic, signaling, and regulation of K + channels. We demonstrate that the expression of the dominant-negative SYP121-Sp2 fragment in maize mesophyll protoplasts or epidermal cells leads to a decrease in the delivery of PIP2;5 to the plasma membrane. Protoplast and oocyte swelling assays showed that PIP2;5 water channel activity is negatively affected by SYP121-Sp2. A combination of in vitro (copurification assays) and in vivo (bimolecular fluorescence complementation, Förster resonance energy transfer, and yeast split-ubiquitin) approaches allowed us to demonstrate that SYP121 and PIP2;5 physically interact. Together with previous data demonstrating the role of SYP121 in regulating K + channel trafficking and activity, these results suggest that SYP121 SNARE contributes to the regulation of the cell osmotic homeostasis.

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“…It has been proposed that this process is a consequence of a physical interaction between PIP1 and PIP2, as reported in both homologous (31) and heterologous systems (14, 32). Although there are some PIP1 with the ability to reach the PM on their own (20,27,29), this PIP1-PIP2 interaction seems to be present for several pairs of PIP among different species with functional consequences (14,21,28,(33)(34)(35).…”

mentioning

confidence: 99%

“…PIP2 are very well described as a homotetramer with high water transport activity (18,19) and a gating mechanism unequivocally associated with specific and conserved amino acid motifs triggered by cytosolic acidification (20)(21)(22), phosphorylation (23,24), or divalent cation concentration (22). In contrast, PIP1 have shown complex heterogeneity in water and solute transport and posttranslational regulation.…”

mentioning

confidence: 99%

Heteromerization of PIP aquaporins affects their intrinsic permeability

Yaneff

Sigaut

Marquez

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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The plant aquaporin plasma membrane intrinsic proteins (PIP) subfamily represents one of the main gateways for water exchange at the plasma membrane (PM). A fraction of this subfamily, known as PIP1, does not reach the PM unless they are coexpressed with a PIP2 aquaporin. Although ubiquitous and abundantly expressed, the role and properties of PIP1 aquaporins have therefore remained masked. Here, we unravel how FaPIP1;1, a fruit-specific PIP1 aquaporin from Fragaria x ananassa, contributes to the modulation of membrane water permeability (P f ) and pH aquaporin regulation. Our approach was to combine an experimental and mathematical model design to test its activity without affecting its trafficking dynamics. We demonstrate that FaPIP1;1 has a high water channel activity when coexpressed as well as how PIP1-PIP2 affects gating sensitivity in terms of cytosolic acidification. PIP1-PIP2 random heterotetramerization not only allows FaPIP1;1 to arrive at the PM but also produces an enhancement of FaPIP2;1 activity. In this context, we propose that FaPIP1;1 is a key participant in the regulation of water movement across the membranes of cells expressing both aquaporins.T he plasma membrane (PM) is the first barrier that limits water exchange in plant cells. The rate of its water transport capacity is mainly associated with aquaporins. Among the seven aquaporin subfamilies described in the plant kingdom, only plasma membrane intrinsic proteins (PIP) and some members of the nodulin-26-like intrinsic proteins (NIP) and X intrinsic proteins (XIP) subfamilies have been shown to be preferentially localized at the PM (1, 2). Of these, PIP aquaporins appear to have a large role in controlling membrane water permeability, whereas NIP and XIP have been mainly described as solute transporters (2-4). Plant PIP aquaporins represent a conserved subfamily that has been historically divided into two subgroups due to their differences in primary structure, PIP1 and PIP2. Interestingly, PIP aquaporins compose ∼40% of the total aquaporin set, and the PIP1 and PIP2 ratio among different species is relatively constant (5-12). Fig. S1 shows the distribution of all aquaporin genes present in plants whose genome has been completely sequenced and analyzed. Antisense inhibition experiments on Arabidopsis thaliana PIP1 and PIP2 have suggested that the two subgroups of aquaporins contribute to root or leaf hydraulic conductivity in the same way (13). In several plant species, members of the PIP1 and PIP2 subgroups were shown to be coexpressed in the same cell type (14-17).Although PIP1 are as ubiquitous as PIP2, the functional properties of each type of channel are different. PIP2 are very well described as a homotetramer with high water transport activity (18, 19) and a gating mechanism unequivocally associated with specific and conserved amino acid motifs triggered by cytosolic acidification (20-22), phosphorylation (23, 24), or divalent cation concentration (22). In contrast, PIP1 have shown complex heterogeneity in water and solute transpor...

show abstract

Intracellular pH sensing is altered by plasma membrane PIP aquaporin co-expression

Cited by 71 publications

References 57 publications

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

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

Selective Regulation of Maize Plasma Membrane Aquaporin Trafficking and Activity by the SNARE SYP121

Heteromerization of PIP aquaporins affects their intrinsic permeability

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