Stomatal responses to humidity and temperature in darkness

Mott, Keith A.; Peak, David

doi:10.1111/j.1365-3040.2010.02129.x

Cited by 68 publications

(84 citation statements)

References 28 publications

(47 reference statements)

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“…and water transport. Recent studies support the idea that water in the guard cell wall is normally maintained by, and equilibrates with, the vapor phase within the intercellular air space of the leaf (Shope et al, 2008;Mott and Peak, 2010;Pieruschka et al, 2010;Rockwell et al, 2014). Since gaseous exchange within the leaf is extremely rapid (Sack and Holbrook, 2006;Morison et al, 2007;Peak and Mott, 2011), this equilibrium implies that the water potential of the guard cell wall is coupled directly to the surrounding air space within the substomatal cavity and it suggests a formal basis for connecting the macroscopic conductance of the leaf with the microscopic processes of the guard cell.…”

Section: Discussionmentioning

confidence: 80%

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: 80%

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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“…2A, top right panel). Under high-humidity conditions, stomates will remain open in the dark (Barbour and Buckley, 2007;Mott and Peak, 2010), and again, guard cells showed high GUS staining ( Fig. 2A, bottom right panel).…”

Section: Apy1 and Apy2 Promoter Activities And Protein Levels Correlamentioning

confidence: 95%

Extracellular Nucleotides and Apyrases Regulate Stomatal Aperture in Arabidopsis

et al. 2011

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This study investigates the role of extracellular nucleotides and apyrase enzymes in regulating stomatal aperture. Prior data indicate that the expression of two apyrases in Arabidopsis (Arabidopsis thaliana), APY1 and APY2, is strongly correlated with cell growth and secretory activity. Both are expressed strongly in guard cell protoplasts, as determined by reverse transcription-polymerase chain reaction and immunoblot analyses. Promoter activity assays for APY1 and APY2 show that expression of both apyrases correlates with conditions that favor stomatal opening. Correspondingly, immunoblot data indicate that APY expression in guard cell protoplasts rises quickly when these cells are moved from darkness into light. Both short-term inhibition of ectoapyrase activity by polyclonal antibodies and long-term suppression of APY1 and APY2 transcript levels significantly disrupt normal stomatal behavior in light. Stomatal aperture shows a biphasic response to applied adenosine 5#-[g-thio]triphosphate (ATPgS) or adenosine 5#-[b-thio] diphosphate, with lower concentrations inducing stomatal opening and higher concentrations inducing closure. Equivalent concentrations of adenosine 5#-O-thiomonophosphate have no effect on aperture. Two mammalian purinoceptor inhibitors block ATPgS-and adenosine 5#-[b-thio] diphosphate-induced opening and closing and also partially block the ability of abscisic acid to induce stomatal closure and of light to induce stomatal opening. Treatment of epidermal peels with ATPgS induces increased levels of nitric oxide and reactive oxygen species, and genetically suppressing the synthesis of these agents blocks the effects of nucleotides on stomatal aperture. A luciferase assay indicates that treatments that induce either the closing or opening of stomates also induce the release of ATP from guard cells. These data favor the novel conclusion that ectoapyrases and extracellular nucleotides play key roles in regulating stomatal functions.

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“…1C) raises questions about the origin of this nocturnal water loss. Although recent studies have shown that stomata remain partially open in the dark (30,31), including in grapevine (32), a slightly permeable cuticle might also be responsible for these observations. To decipher the respective contributions of stomata and cuticle to the genetic variability of E n , a subset of 28 genotypes with contrasting E n were selected from the S×G population.…”

Section: Genetic Variability In Nighttime Transpiration Mostly Originmentioning

confidence: 98%

Reduced nighttime transpiration is a relevant breeding target for high water-use efficiency in grapevine

Coupel‐Ledru

Lebon

Christophe

et al. 2016

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

123

101

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Increasing water scarcity challenges crop sustainability in many regions. As a consequence, the enhancement of transpiration efficiency (TE)-that is, the biomass produced per unit of water transpired-has become crucial in breeding programs. This could be achieved by reducing plant transpiration through a better closure of the stomatal pores at the leaf surface. However, this strategy generally also lowers growth, as stomatal opening is necessary for the capture of atmospheric CO 2 that feeds daytime photosynthesis. Here, we considered the reduction in transpiration rate at night (E n ) as a possible strategy to limit water use without altering growth. For this purpose, we carried out a genetic analysis for E n and TE in grapevine, a major crop in drought-prone areas. Using recently developed phenotyping facilities, potted plants of a cross between Syrah and Grenache cultivars were screened for 2 y under well-watered and moderate soil water deficit scenarios. High genetic variability was found for E n under both scenarios and was primarily associated with residual diffusion through the stomata. Five quantitative trait loci (QTLs) were detected that underlay genetic variability in E n . Interestingly, four of them colocalized with QTLs for TE. Moreover, genotypes with favorable alleles on these common QTLs exhibited reduced E n without altered growth. These results demonstrate the interest of breeding grapevine for lower water loss at night and pave the way to breeding other crops with this underexploited trait for higher TE.night transpiration | transpiration efficiency | growth | stomata | QTL

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Stomatal responses to humidity and temperature in darkness

Cited by 68 publications

References 28 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

Extracellular Nucleotides and Apyrases Regulate Stomatal Aperture in Arabidopsis

Reduced nighttime transpiration is a relevant breeding target for high water-use efficiency in grapevine

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