Accumulation of an apoplastic solute in the guard‐cell wall is sufficient to exert a significant effect on transpiration in <i>Vicia faba</i> leaflets

Ewert, M. S.; Outlaw, William H.; Zhang, S.; Aghoram, Karthik; Riddle, Kimberly A.

doi:10.1046/j.1365-3040.2000.00539.x

Cited by 42 publications

(56 citation statements)

References 42 publications

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“…Transgenic plants overexpressing hexokinase (HK, a sugar-phosphorylating enzyme involved in sugar sensing) specifically in guard cells exhibited accelerated stomatal closure induced by sugar. This observation supports the idea of photosynthesis feedback inhibition of stomatal conductance by Suc (Kelly et al, 2013) and agrees with the earlier suggestion by Outlaw and colleagues that Suc produced by mesophyll photosynthesis is loaded into the apoplast and carried to the vicinity of the guard cells, where an extracellular osmotic effect closes the stomata (Lu et al, 1995(Lu et al, , 1997Ewert et al, 2000;Outlaw and De Vlieghere-He, 2001;Kang et al, 2007). This might provide a mechanism for coordinating photosynthetic rates with transpiration.…”

Section: Role For Suc Other Than Osmoregulationsupporting

confidence: 92%

Rethinking Guard Cell Metabolism

2016

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ORCID IDs: 0000-0001-9686-1216 (D.S.); 0000-0002-4073-7221 (T.L.).Stomata control gaseous fluxes between the internal leaf air spaces and the external atmosphere and, therefore, play a pivotal role in regulating CO 2 uptake for photosynthesis as well as water loss through transpiration. Guard cells, which flank the stomata, undergo adjustments in volume, resulting in changes in pore aperture. Stomatal opening is mediated by the complex regulation of ion transport and solute biosynthesis. Ion transport is exceptionally well understood, whereas our knowledge of guard cell metabolism remains limited, despite several decades of research. In this review, we evaluate the current literature on metabolism in guard cells, particularly the roles of starch, sucrose, and malate. We explore the possible origins of sucrose, including guard cell photosynthesis, and discuss new evidence that points to multiple processes and plasticity in guard cell metabolism that enable these cells to function effectively to maintain optimal stomatal aperture. We also discuss the new tools, techniques, and approaches available for further exploring and potentially manipulating guard cell metabolism to improve plant water use and productivity.

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Section: Role For Suc Other Than Osmoregulationsupporting

confidence: 92%

Rethinking Guard Cell Metabolism

2016

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“…These results suggest the need for additional carbon sources for guard cell starch metabolism, which most likely are imported from the mesophyll or are produced in guard cells prior to chlorophyll removal in the present study. These data are in line with the hypothesis that apoplastic sucrose is a source for guard cell symplastic sucrose and acts as an osmoticum for stomatal opening or replacing guard cell carbon stores (Lu et al ., ; Ewert et al ., ; Outlaw and De Vlieghere‐He, ; Stadler et al ., ). Nevertheless, we have found that guard cell photosynthesis is critical for intact guard cell turgor production.…”

Section: Discussionmentioning

confidence: 99%

Guard cell photosynthesis is critical for stomatal turgor production, yet does not directly mediate CO₂‐ and ABA‐induced stomatal closing

et al. 2015

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SUMMARY Stomata mediate gas exchange between the inter-cellular spaces of leaves and the atmosphere. CO2 levels in leaves (Ci) are determined by respiration, photosynthesis, stomatal conductance and atmospheric [CO2]. [CO2] in leaves mediates stomatal movements. The role of guard-cell photosynthesis in stomatal conductance responses is a matter of debate, and genetic approaches are needed. We have generated transgenic Arabidopsis plants that are chlorophyll-deficient in guard cells only, expressing a constitutively active chlorophyllase in a guard-cell specific enhancer trap-line. Our data show that more than 90% of guard cells were chlorophyll-deficient. Interestingly, approximately ~ 45% of stomata had an unusual, previously not-described, morphology of thin-shaped chlorophyll-less stomata. Nevertheless, stomatal size, stomatal index, plant morphology, and whole-leaf photosynthetic parameters (PSII, qP, qN, FV′/FM′) were comparable to wild-type plants. Time-resolved intact leaf gas exchange analyses showed a reduction in stomatal conductance and carbon assimilation rates of the transgenic plants. Normalization of CO2 responses showed that stomata of transgenic plants respond to [CO2] shifts. Detailed stomatal aperture measurements of normal kidney-shaped stomata, which lack chlorophyll, showed stomatal closing responses to [CO2] elevation and abscisic acid (ABA), while thin-shaped stomata were continuously closed. Our present findings show that stomatal movement responses to [CO2] and ABA are functional in guard cells that lack chlorophyll. These data suggest that guard-cell CO2 and ABA signal transduction are not directly modulated by guard-cell photosynthesis/electron transport. Moreover, the finding that chlorophyll-less stomata cause a “deflated” thin-shaped phenotype, suggests that photosynthesis in guard cells is critical for energization and guard-cell turgor production.

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“…Suc metabolism has been proposed to play a role in the longer term coordination (over the diurnal period) of A and g s (for review, see . Initially proposed by Outlaw and coworkers (Outlaw and Manchester, 1979;Lu et al, 1995Lu et al, , 1997Ewert et al, 2000;Outlaw and De Vlieghere-He, 2001;Kang et al, 2007), Suc generated by mesophyll photosynthesis is uploaded to the phloem and transported away from sources to sinks driven by transpiration (Outlaw and De Vlieghere-He, 2001). Excess Suc (when photosynthesis is high) is carried toward the stomata by the apoplast, stimulating stomatal closure either through some signaling mechanism or by acting as an osmoticum (Lu et al, 1997;Outlaw, 2003;Kang et al, 2007;Kelly et al, 2013).…”

Section: Mechanisms Of Coordination Between Stomatal Behavior and Mesmentioning

confidence: 99%

Diurnal Variation in Gas Exchange: The Balance between Carbon Fixation and Water Loss

2017

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Stomatal control of transpiration is critical for maintaining important processes, such as plant water status, leaf temperature, as well as permitting sufficient CO 2 diffusion into the leaf to maintain photosynthetic rates (A). Stomatal conductance often closely correlates with A and is thought to control the balance between water loss and carbon gain. It has been suggested that a mesophyll-driven signal coordinates A and stomatal conductance responses to maintain this relationship; however, the signal has yet to be fully elucidated. Despite this correlation under stable environmental conditions, the responses of both parameters vary spatially and temporally and are dependent on species, environment, and plant water status. Most current models neglect these aspects of gas exchange, although it is clear that they play a vital role in the balance of carbon fixation and water loss. Future efforts should consider the dynamic nature of whole-plant gas exchange and how it represents much more than the sum of its individual leaf-level components, and they should take into consideration the long-term effect on gas exchange over time.As the waxy surface of most leaves makes them virtually impermeable to CO 2 and water, nearly all CO 2 absorbed by the plant and water lost pass through the stomatal pores (Cowan and Troughton, 1971;Caird et al., 2007;Jones, 2013). Although these pores represent only a small fraction of the leaf surface, stomatal behavior has major consequences for photosynthetic CO 2 fixation and water loss from leaf to canopy levels, influencing carbon and hydrological cycles at global scales (Hetherington and Woodward, 2003;Keenan et al., 2013). Guard cells that surround the stomatal pore open and close in response to environmental stimuli, controlling the flux of gas between the leaf interior and the bulk atmosphere. Stomatal conductance (g s ) appears to be closely linked with mesophyll demands for CO 2 , and a strong correlation between photosynthetic rate (A) and g s is often observed (Wong et al., 1979;Farquhar and Sharkey, 1982;Mansfield et al., 1990;Buckley and Mott, 2013), and although conserved, it is not always constant (Lawson and Morison, 2004;Bonan et al., 2014). However, the A and properties of each leaf may not be identical and depend on acclimation to the surrounding microclimatic conditions; therefore, each leaf could be considered unique (Niinemets, 2016).In order to maintain an appropriate water status, plants must balance water loss between leaves with different properties depending on the availability of soil water, which raises the question about the regulation of g s at the whole-plant level. Early experiments by Meinzer and Grantz (1990) showed that the balance between water loss and water transport capacity enables the maintenance of a constant leaf water status over a wide range of plant sizes and growing conditions. Therefore, plants regulate the transpiration of each leaf independently in response to variations in microclimate by constantly adjusting stomatal aperture. The sto...

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Accumulation of an apoplastic solute in the guard‐cell wall is sufficient to exert a significant effect on transpiration in Vicia faba leaflets

Cited by 42 publications

References 42 publications

Rethinking Guard Cell Metabolism

Rethinking Guard Cell Metabolism

Guard cell photosynthesis is critical for stomatal turgor production, yet does not directly mediate CO₂‐ and ABA‐induced stomatal closing

Diurnal Variation in Gas Exchange: The Balance between Carbon Fixation and Water Loss

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Accumulation of an apoplastic solute in the guard‐cell wall is sufficient to exert a significant effect on transpiration in Vicia faba leaflets

Cited by 42 publications

References 42 publications

Rethinking Guard Cell Metabolism

Rethinking Guard Cell Metabolism

Guard cell photosynthesis is critical for stomatal turgor production, yet does not directly mediate CO2‐ and ABA‐induced stomatal closing

Diurnal Variation in Gas Exchange: The Balance between Carbon Fixation and Water Loss

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Guard cell photosynthesis is critical for stomatal turgor production, yet does not directly mediate CO₂‐ and ABA‐induced stomatal closing