Guard cell‐specific upregulation of sucrose synthase 3 reveals that the role of sucrose in stomatal function is primarily energetic

Abstract

SummaryIsoform 3 of sucrose synthase (SUS3) is highly expressed in guard cells; however, the precise function of SUS3 in this cell type remains to be elucidated.Here, we characterized transgenic Nicotiana tabacum plants overexpressing SUS3 under the control of the stomatal-specific KST1 promoter, and investigated the changes in guard cell metabolism during the dark to light transition.Guard cell-specific SUS3 overexpression led to increased SUS activity, stomatal aperture, stomatal conductance, transpiration rate, net photosynthetic rate and growth. Although only minor changes were observed in the metabolite profile in whole leaves, an increased fructose level and decreased organic acid levels and sucrose to fructose ratio were observed in guard cells of transgenic lines. Furthermore, guard cell sucrose content was lower during lightinduced stomatal opening. In a complementary approach, we incubated guard cell-enriched epidermal fragments in 13 C-NaHCO 3 and followed the redistribution of label during dark to light transitions; this revealed increased labeling in metabolites of, or associated with, the tricarboxylic acid cycle. The results suggest that sucrose breakdown is a mechanism to provide substrate for the provision of organic acids for respiration, and imply that manipulation of guard cell metabolism may represent an effective strategy for plant growth improvement.

Relationships of Leaf Net Photosynthesis, Stomatal Conductance, and Mesophyll Conductance to Primary Metabolism: A Multispecies Meta-Analysis Approach

“…Indeed, plants that have higher accumulation of malate and fumarate show higher g s (Nunes-Nesi et al, 2007;Araújo et al, 2011b;Medeiros et al, 2015). In contrast, transgenic tobacco plants that accumulate less succinate and 2-oxoglutarate in leaves and less succinate and citrate in their guard cells also have higher g s (Daloso et al, 2016). These findings further support our results and suggest that the different parts of the TCA cycle, which is supposed to operate in a noncyclic mode in illuminated leaves (Cheung et al, 2014), have differential contribution to stomatal movements.…”

A Tale of Two Sugars: Trehalose 6-Phosphate and Sucrose

“…If it does, then its influence on guard cell starch metabolism might differ from the regulation of starch breakdown in mesophyll cells, given the specific functions and contrasting diurnal profiles of starch in the two cell types. Suc can be one of the major osmolytes involved in stomatal opening (Lawson et al, 2014;Daloso et al, 2016aDaloso et al, , 2016b, so might Tre6P inhibit starch degradation in guard cells in the light if there is already sufficient Suc to drive stomatal opening? Conversely, might the distinct pathway of starch degradation in guard cells be insensitive to Tre6P, allowing starch to be degraded in the light even if Suc, and by implication Tre6P, levels are high?…”

Transitory Starch Metabolism in Guard Cells: Unique Features for a Unique Function

“…After falling to near zero in the first hour after dawn, starch levels then begin to rise again, with net accumulation continuing past dusk into the early hours of the night (Horrer et al, 2016). Guard cell chloroplasts contain Rubisco and seem capable of net CO 2 assimilation (Lawson et al, 2002(Lawson et al, , 2003, so some of the carbon for starch synthesis in the light may come from guard cell photosynthesis but is likely to be supplemented by import of sugars from the apoplast or from sugars stored in the guard cells during the previous light phase (Daloso et al, 2016;Santelia and Lawson, 2016).…”

“…By extrapolation, we might speculate that T6P also inhibits the rapid starch degradation that occurs in guard cells upon illumination, perhaps preventing unnecessary starch turnover if the guard cells have sufficient Suc to drive stomatal opening ( Fig. 2; Lawson et al, 2014;Daloso et al, 2016). However, given the different functions, diurnal patterns of turnover and degradative pathways in guard cells compared to mesophyll cells (Valerio et al, 2011;Prasch et al, 2015;Horrer et al, 2016), differences in the sensitivity of starch degradation to T6P are also possible.…”