A study of potassium gradients in the epidermis of intact leaves of Commelina communis L. in relation to stomatal opening

Penny, M. G.; Bowling, D. J. F.

doi:10.1007/bf00390818

Cited by 123 publications

(54 citation statements)

References 18 publications

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“…1). This effect could be partly responsible for the dessication noted during prolonged mannose feeding and could be related to the energy requirement for stomatal closure (16).…”

Section: Methodsmentioning

confidence: 99%

Effects of Mannose on Photosynthetic Gas Exchange in Spinach Leaf Discs

Harris¹,

Cheesbrough²,

Walker³

1983

Plant Physiol.

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When mannose is provided in the transpiration stream to spinach (Spinacia oleracea) leaf discs, a series of specific and nonspecific changes occur in CO2 and H20 vapor exchange as a function of feeding time. The initial increases in apparent photosynthesis and transpiration are nonspecific effects due to osmotic changes leading to passive stomatal opening. The mannose-specific effects are: (a) time-dependent changes in the CO2 concentration required for saturation; (b) complex kinetics of the inhibition of CO2 assimilation dependent on CO2 and 02 concentrations and the duration of feeding (high C02 and low 02 lead to rapid inhibitions of photosynthesis); (c) elimination of the capacity of 2% 02 to stimulate photosynthesis; and (d) oscillations in the CO2 exchange rate following transitions from 20% to 2% 02. The mannose-specific effects are reversible by orthophosphate. The mannose-dependent changes in gas exchange are attributed to altered IATPI/IADPI ratios.Previous work has established that when mannose is exogenously supplied to leaf discs it can lead to a progressive decline in the photosynthetic capacity of the tissue. This decline and the accompanying metabolic disturbances (10) have been attributed to the capacity of mannose to sequester Pi (4,11,12). In an effort to ascertain the early kinetics of the mannose-induced photosynthetic decline, and also the nature of the changes in the capacity of the leaf to respond to environmental parameters (02, C02), the photosynthetic gas exchange of spinach leaf discs was monitored during mannose feeding. MATERIALS AND METHODSMeasurements of CO2 and H20 vapor exchange were as reported previously (7). RESULTSWhen mannose was supplied to the transpiration stream of spinach leaf discs at mm concentrations (20-100 mM), several characteristic changes in the H20 vapor and CO2 exchange occurred. Leaf temperature dropped and transpiration and apparent photosynthesis increased within minutes of the start of feeding (Fig. 1) limits of the transpiration rate had not already been approached (data not shown). Following these initial nonspecific effects, a series of secondary changes occurred; these were only brought about by sugars which are known to sequester Pi (e.g. mannose and 2-deoxyglucose).When spinach leaf discs were enclosed within the Plexiglas chamber utilized in these experiments, they retained the characteristic C3 photosynthetic responses to changes in external partial pressures of 02 (2, 7). In saturating light at 25°C and with atmospheric concentrations of C02, the change from 20% 02 to 2% 02 increased apparent photosynthesis by 45% and lowered the mesophyll resistance (rm) from 3.8 to 2.2 s/cm (7). The kinetics of the transition to the higher rate under 2% 02 were without evident oscillations in the rate of CO2 exchange, and a new steady rate was generally reached in 2 to 5 min (Fig. 2).Following feeding with either deoxyglucose or mannose, there was progressive decline in the capacity of 2% 02 to stimulate photosynthesis, leading ultimately to a conditio...

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“…1). This effect could be partly responsible for the dessication noted during prolonged mannose feeding and could be related to the energy requirement for stomatal closure (16).…”

Section: Methodsmentioning

confidence: 99%

Effects of Mannose on Photosynthetic Gas Exchange in Spinach Leaf Discs

Harris¹,

Cheesbrough²,

Walker³

1983

Plant Physiol.

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“…Transfer of solutes (namely, K 1 ) to guard cells via subsidiary and epidermal cells has long been recognized (Fujino, 1967;Fischer, 1968;Humble and Hsiao, 1969;Sawhney and Zelitch, 1969;Humble and Raschke, 1971;Pallaghy, 1971;Penny and Bowling, 1974;Dayanandan and Kaufman, 1975;Macrobbie and Lettau, 1980;Outlaw, 1983), but here we make the case for mandatory and opposite changes in osmotic and turgor pressure of guard and subsidiary cells where epidermal or subsidiary cells have a large mechanical advantage over guard cells. This requirement would diminish in species with diminished mechanical advantage (e.g.…”

Section: Overcoming the Mechanical Advantagementioning

confidence: 99%

The Mechanical Diversity of Stomata and Its Significance in Gas-Exchange Control

2006

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Given that stomatal movement is ultimately a mechanical process and that stomata are morphologically and mechanically diverse, we explored the influence of stomatal mechanical diversity on leaf gas exchange and considered some of the constraints. Mechanical measurements were conducted on the guard cells of four different species exhibiting different stomatal morphologies, including three variants on the classical ''kidney'' form and one ''dumb-bell'' type; this information, together with gas-exchange measurements, was used to model and compare their respective operational characteristics. Based on evidence from scanning electron microscope images of cryo-sectioned leaves that were sampled under full sun and high humidity and from pressure probe measurements of the stomatal aperture versus guard cell turgor relationship at maximum and zero epidermal turgor, it was concluded that maximum stomatal apertures (and maximum leaf diffusive conductance) could not be obtained in at least one of the species (the grass Triticum aestivum) without a substantial reduction in subsidiary cell osmotic (and hence turgor) pressure during stomatal opening to overcome the large mechanical advantage of subsidiary cells. A mechanism for this is proposed, with a corollary being greatly accelerated stomatal opening and closure. Gas-exchange measurements on T. aestivum revealed the capability of very rapid stomatal movements, which may be explained by the unique morphology and mechanics of its dumb-bell-shaped stomata coupled with ''see-sawing'' of osmotic and turgor pressure between guard and subsidiary cells during stomatal opening or closure. Such properties might underlie the success of grasses.Although the morphological diversity of stomata is widely documented (Haberlandt, 1884;Meidner and Mansfield, 1968;Allaway and Milthorpe, 1976;Ziegler, 1987;Willmer and Fricker, 1996), little is known of how this translates into functional diversity and what the environmental context of this might be. Throughout the 400 million year (Ma) history of vascular plants on land, long-term decline in atmospheric CO 2 concentration and shifts in prevailing moisture patterns have placed selective pressures on stomata to increase epidermal conductance to CO 2 diffusion and also to increase transpiration efficiency (CO 2 fixed per unit water transpired). This posed two separate problems, upon which the combination of mutation and time might have worked to give rise to the current diversity of stomatal form and function. The first centered on the simple geometric practicalities of fitting enough functional stomatal units per unit leaf surface area to meet the desired CO 2 flux as atmospheric CO 2 concentration changed, or to service an increase in photosynthetic capacity. The second centered on the performance characteristics of any new stomatal structure or configuration in relation to transpiration efficiency. Here, by examining the mechanical and performance characteristics of stomata in four different species, we explore the nature of these two problem...

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“…The surrounding epidermal or subsidiary cells are thought to serve as a source for K + and other ions during stomatal opening and as a sink for the same ions when stomata close (Raschke and Fellows, 1971;MacRobbie and Lettau, 1980;Outlaw, 1983;Franks and Farquhar, 2007). MacRobbie and Lettau (1980) used K + -sensitive microelectrodes to demonstrate that the K + content in the epidermal cells of C. communis was reduced from between 180 and 300 mM to 80 mM when the nearby stomata opened, consistent with solute uptake by the guard cells from adjacent subsidiary cells (Penny and Bowling, 1974). However, when isolated in epidermal peels and superfused with solution containing millimolar KCl, any source-sink relations between guard cells and the surrounding epidermis are short-circuited by the nearly infinite volume of the buffer solution.…”

Section: Gas Exchange and Stomatal Patterningmentioning

confidence: 99%

Stomatal Spacing Safeguards Stomatal Dynamics by Facilitating Guard Cell Ion Transport Independent of the Epidermal Solute Reservoir

2016

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Stomata enable gaseous exchange between the interior of the leaf and the atmosphere through the stomatal pore. Control of the pore aperture depends on osmotic solute accumulation by, and its loss from the guard cells surrounding the pore. Stomata in most plants are separated by at least one epidermal cell, and this spacing is thought to enhance stomatal function, although there are several genera that exhibit stomata in clusters. We made use of Arabidopsis (Arabidopsis thaliana) stomatal patterning mutants to explore the impact of clustering on guard cell dynamics, gas exchange, and ion transport of guard cells. These studies showed that stomatal clustering in the Arabidopsis too many mouths (tmm1) mutant suppressed stomatal movements and affected CO 2 assimilation and transpiration differentially between dark and light conditions and were associated with alterations in K + channel gating. These changes were consistent with the impaired dynamics of tmm1 stomata and were accompanied by a reduced accumulation of K + ions in the guard cells. Our findings underline the significance of spacing for stomatal dynamics. While stomatal spacing may be important as a reservoir for K + and other ions to facilitate stomatal movements, the effects on channel gating, and by inference on K + accumulation, cannot be explained on the basis of a reduced number of epidermal cells facilitating ion supply to the guard cells.Stomata are pores found in the epidermis of most aerial parts of plants and are formed between a specialized pair of cells, the guard cells. Stomata facilitate the uptake of CO 2 at the expense of water vapor release via transpiration (Hetherington and Woodward, 2003). Hence, stomata play a crucial role in the physiology of plants. They permit gaseous exchange between the environment and the inside of the leaf for photosynthesis and, in turn, they influence the water use efficiency and growth of the plant. Mathematical models have suggested that historical changes in the freshwater resources can be attributed to stomatal transpiration, and it has been argued that the manipulation of stomata will be an important factor in ensuring water availability over the next 20 to 30 years (UNESCO World Water Development Report, 2015). Efforts to develop crops with higher water use efficiency through conventional breeding strategies have led to some successes, including the Drysdale wheat (Triticum aestivum) variety (Condon et al., 2002). It is likely that further advances will be possible as we gain insights into the physiology of stomata in situ.The regulation of gas exchange is achieved by controlling the stomatal pore. Stomata respond dynamically to environmental changes, including light quality and intensity, ambient CO 2 concentration, and humidity (Aphalo and Jarvis, 1991;Hetherington and Woodward, 2003;Shimazaki et al., 2007). Stomatal movements result from changes in guard cell volume and turgor and are driven by solute and water fluxes across the plasma membrane and tonoplast of guard cells. In particular, fluxes of ...

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A study of potassium gradients in the epidermis of intact leaves of Commelina communis L. in relation to stomatal opening

Cited by 123 publications

References 18 publications

Effects of Mannose on Photosynthetic Gas Exchange in Spinach Leaf Discs

Effects of Mannose on Photosynthetic Gas Exchange in Spinach Leaf Discs

The Mechanical Diversity of Stomata and Its Significance in Gas-Exchange Control

Stomatal Spacing Safeguards Stomatal Dynamics by Facilitating Guard Cell Ion Transport Independent of the Epidermal Solute Reservoir

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