Expression of Arabidopsis Hexokinase in Citrus Guard Cells Controls Stomatal Aperture and Reduces Transpiration

Lugassi, Nitsan; Kelly, Gilor; Fidel, Lena; Yaniv, Yossi; Attia, Ziv; Levi, A.; Alchanatis, V.; Moshelion, Menachem; Raveh, Eran; Carmi, Nir; Granot, David

doi:10.3389/fpls.2015.01114

Cited by 70 publications

(93 citation statements)

References 55 publications

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“…The first evidence for this alternative mechanism is that the addition of 100 mM sucrose induces stomatal closure via HXK activity and guard cell nitric oxide accumulation, a component of the ABA signalling pathway. Transgenic A. thaliana, Solanum lycopersicum and Citrus sinensis plants overexpressing HXK1 under control of the inward rectifying K + channel (KST1) promoter, which drives guard cell-specific expression, show higher stomatal closure via a pathway induced by sugar and mediated by ABA (Kelly et al, 2013;Lugassi et al, 2015). These data suggest that sucrose and HXK activity could represent a possible mechanism that induces stomatal closure during periods of high photosynthetic rates (Kelly et al, 2013).…”

Section: Role Of Mesophyll-derived Sucrose In Stomatal Closurementioning

confidence: 99%

“…The idea that sucrose acts as a mesophyll‐to‐guard cell connector is strongly supported by experiments in which labelled 14 CO 2 provided to mesophyll cells was detected at the apoplastic space of guard cells as sucrose (Lu et al ., ). Furthermore, it has been shown that sucrose accumulation in the guard cell apoplast of phloem loader species (Lu et al ., ), or its dissimilation within guard cells (Kelly et al ., ; Lugassi et al ., ), induces stomatal closure in periods of high photosynthetic rate. These results suggest that guard cells import sucrose from the apoplastic space and that the majority, if not all, comes from surrounding mesophyll cells (Fig.…”

Section: The Role Of Sucrose As a Mesophyll‐to‐guard Cell Connectormentioning

confidence: 99%

“…Recent results suggest that HXK is a key regulator of stomatal movements in response to sucrose. It has been shown that overexpression of HXK specifically in guard cells leads to higher and lower stomatal conductance (g s ) under low and high light intensities, respectively (Lugassi et al, 2015). This suggests that HXK can mediate the control of g s based on the concentration of sucrose and hexoses in guard cells.…”

Section: Sucrose Breakdown As An Important Mechanism During Light-indmentioning

confidence: 99%

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Roles of sucrose in guard cell regulation

2016

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SummaryThe control of stomatal aperture involves reversible changes in the concentration of osmolytes in guard cells. Sucrose has long been proposed to have an osmolytic role in guard cells. However, direct evidence for such a role is lacking. Furthermore, recent evidence suggests that sucrose may perform additional roles in guard cells. Here, we provide an update covering the multiple roles of sucrose in guard cell regulation, highlighting the knowledge accumulated regarding spatiotemporal differences in the synthesis, accumulation, and degradation of sucrose as well as reviewing the role of sucrose as a metabolic connector between mesophyll and guard cells. Analysis of transcriptomic data from previous studies reveals that several genes encoding sucrose and hexose transporters and genes involved in gluconeogenesis, sucrose and trehalose metabolism are highly expressed in guard cells compared with mesophyll cells. Interestingly, this analysis also showed that guard cells have considerably higher expression of C 4 -marker genes than mesophyll cells. We discuss the possible roles of these genes in guard cell function and the role of sucrose in stomatal opening and closure. Finally, we provide a perspective for future experiments which are required to fill gaps in our understanding of both guard cell metabolism and stomatal regulation.

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Section: Role Of Mesophyll-derived Sucrose In Stomatal Closurementioning

confidence: 99%

Section: The Role Of Sucrose As a Mesophyll‐to‐guard Cell Connectormentioning

confidence: 99%

Section: Sucrose Breakdown As An Important Mechanism During Light-indmentioning

confidence: 99%

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Roles of sucrose in guard cell regulation

2016

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“…photosynthesis (for review, see Lugassi et al, 2015;Daloso et al, 2016;Santelia and Lawson, 2016;Santelia and Lunn, 2017). By the end of the day, the slow response of g s can result in the maintenance of high g s , which leads to substantial water losses that are not accompanied by any carbon uptake (Blom-Zandstra et al, 1995).…”

Section: Diurnal Impact On Stomatal Behavior and Implications For Futmentioning

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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“…The roles of HXKs could be summarized in participation to the juvenile-to-adult transition, to the uptake of minerals, mainly phosphates, to the short-term (reversible) sugar-sensing regulation and to the long-term growth-inhibiting effect in case of constitutive expression of AtHXK1 under the 35S promoter in Arabidopsis and tomato plants . However, recent studies with citrus, tomato and Arabidopsis have shown that HXK is involved in guard cells control and provokes stomatal closure independent of its osmotic effect Lugassi et al, 2015). It is not yet known if in strawberry the MAKRs (membrane associated kinase regulators) could be directly involved in the same metabolic pathway.…”

Section: Introductionmentioning

confidence: 99%