Lateral CO2 Diffusion inside Dicotyledonous Leaves Can Be Substantial: Quantification in Different Light Intensities

Morison, J. I. L.; Lawson, Tracy; Cornic, Gabriel

doi:10.1104/pp.107.107318

Cited by 31 publications

(32 citation statements)

References 32 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…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. We have integrated these ideas within OnGuard2 by ascribing the effects of increasing VPD to a local depression in water potential adjacent to the guard cells and by modeling evaporative demand as a simple linear function of water feed to the leaf and substomatal cavity.…”

Section: Discussionmentioning

confidence: 72%

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

et al. 2017

Self Cite

View full text Add to dashboard Cite

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...

show abstract

Section: Discussionmentioning

confidence: 72%

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

et al. 2017

Self Cite

View full text Add to dashboard Cite

show abstract

“…Recently, Morison et al . (2007) reported on gas exchange measurement on leaves covered by circular grease patches.…”

Section: Discussionmentioning

confidence: 99%

“…Morison et al . (2005) concluded from measurements performed on homobaric Commelina communis leaves that lateral diffusion of CO 2 is not sufficient to support photosynthesis; however, they modified their previous interpretation, reporting in a very recent contribution that lateral CO 2 diffusion can be substantial inside dicotyledonous leaves (Morison et al ., 2007).…”

Section: Introductionmentioning

confidence: 99%

“…The impact of lateral diffusion on photosynthesis was estimated for different light conditions, CO 2 concentrations, widths of the grease stripes, stomatal conductances ( g s ) and D C ′ lat values. Using the improved method, the results obtained clearly demonstrate that the surplus CO 2 assimilation rates in the greased leaf areas ( A gr ) were not similar for the investigated plant species (as suggested by Morison et al ., 2007), but differed clearly depending on the lateral conductivities of the respective leaves.…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Photosynthesis can be enhanced by lateral CO₂ diffusion inside leaves over distances of several millimeters

et al. 2008

View full text Add to dashboard Cite

Summary• This study examines the extent to which lateral gas diffusion can influence intercellular CO 2 concentrations (c i ) and thus photosynthesis in leaf areas with closed stomata.• Leaves were partly greased to close stomata artificially, and effects of laterally diffusing CO 2 into the greased areas were studied by gas-exchange measurement and chlorophyll fluorescence imaging. Effective quantum yields (ΔF/F m ′) across the greased areas were analysed with an image-processing tool and transposed into c i profiles, and lateral CO 2 diffusion coefficients (D C ′ lat ), directly proportional to lateral conductivities ( ), were estimated using a one-dimensional (1D) diffusion model.• Effective CO 2 diffusion distances in Vicia faba (homobaric), Commelina vulgaris (homobaric) and Phaseolus vulgaris (heterobaric) leaves clearly differed, and were dependent on D C ′ lat , light intensity, [CO 2 ], and [O 2 ]: largest distances were approx. 7.0 mm for homobaric leaves (with high D C ′ lat ) and approx. 1.9 mm for heterobaric leaves (low D C ′ lat ).• Modeled lateral CO 2 fluxes indicate large support of photosynthesis over submillimeter distances for leaves with low D C ′ lat , whereas in leaves with large D C ′ lat , photosynthesis can be stimulated over distances of several millimeters. For the plant species investigated, the surplus CO 2 assimilation rates of the greased leaf areas (A gr ) differed clearly, depending on lateral conductivities of the respective leaves.

show abstract

“…The latter possess bundle sheath extensions (BSEs) that connect the epidermis and vascular bundles (Wylie, 1952). BSEs can help distribute light through thicker leaves, enhancing photosynthesis (Nikolopoulos et al, 2002), and they may limit lateral CO 2 diffusion within the leaf (Terashima, 1992;Morison et al, 2007). BSEs are more common in xeric, high-light species and upper canopy trees (Kenzo et al, 2007) and in deciduous woody species than in herbs (Wylie, 1952;McClendon, 1992).…”

mentioning

confidence: 99%

The Role of Bundle Sheath Extensions and Life Form in Stomatal Responses to Leaf Water Status

2011

View full text Add to dashboard Cite

Bundle sheath extensions (BSEs) are key features of leaf structure with currently little-understood functions. To test the hypothesis that BSEs reduce the hydraulic resistance from the bundle sheath to the epidermis (r be ) and thereby accelerate hydropassive stomatal movements, we compared stomatal responses with reduced humidity and leaf excision among 20 species with heterobaric or homobaric leaves and herbaceous or woody life forms. We hypothesized that low r be due to the presence of BSEs would increase the rate of stomatal opening (V) during transient wrong-way responses, but more so during wrong-way responses to excision (V e ) than humidity (V h ), thus increasing the ratio of V e to V h . We predicted the same trends for herbaceous relative to woody species given greater hydraulic resistance in woody species. We found that V e , V h , and their ratio were 2.3 to 4.4 times greater in heterobaric than homobaric leaves and 2.0 to 3.1 times greater in herbaceous than woody species. To assess possible causes for these differences, we simulated these experiments in a dynamic compartment/resistance model, which predicted larger V e and V e /V h in leaves with smaller r be . These results support the hypothesis that BSEs reduce r be . Comparison of our data and simulations suggested that r be is approximately 4 to 16 times larger in homobaric than heterobaric leaves. Our study provides new evidence that variations in the distribution of hydraulic resistance within the leaf and plant are central to understanding dynamic stomatal responses to water status and their ecological correlates and that BSEs play several key roles in the functional ecology of heterobaric leaves.

show abstract

Lateral CO2 Diffusion inside Dicotyledonous Leaves Can Be Substantial: Quantification in Different Light Intensities

Cited by 31 publications

References 32 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

Photosynthesis can be enhanced by lateral CO₂ diffusion inside leaves over distances of several millimeters

The Role of Bundle Sheath Extensions and Life Form in Stomatal Responses to Leaf Water Status

Contact Info

Product

Resources

About

Lateral CO2 Diffusion inside Dicotyledonous Leaves Can Be Substantial: Quantification in Different Light Intensities

Cited by 31 publications

References 32 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

Photosynthesis can be enhanced by lateral CO2 diffusion inside leaves over distances of several millimeters

The Role of Bundle Sheath Extensions and Life Form in Stomatal Responses to Leaf Water Status

Contact Info

Product

Resources

About

Photosynthesis can be enhanced by lateral CO₂ diffusion inside leaves over distances of several millimeters