Metabolism within the specialized guard cells of plants

Abstract

Contents Summary1018I.Introduction1018II.Guard cell photosynthesis1019III.Guard cell central metabolism1022IV.Guard cell starch metabolism differs from that of mesophyll cells and plays a key role in stomatal movement1025V.Connectors between mesophyll and guard cells1026VI.Challenges and perspectives in understanding and modelling guard cell metabolism1029Acknowledgements1030References1030 Summary Stomata are leaf epidermal structures consisting of two guard cells surrounding a pore. Changes in the aperture of this pore regulate plant water‐use efficiency, defined as gain of C by photosynthesis per leaf water transpired. Stomatal aperture is actively regulated by reversible changes in guard cell osmolyte content. Despite the fact that guard cells can photosynthesize on their own, the accumulation of mesophyll‐derived metabolites can seemingly act as signals which contribute to the regulation of stomatal movement. It has been shown that malate can act as a signalling molecule and a counter‐ion of potassium, a well‐established osmolyte that accumulates in the vacuole of guard cells during stomatal opening. By contrast, their efflux from guard cells is an important mechanism during stomatal closure. It has been hypothesized that the breakdown of starch, sucrose and lipids is an important mechanism during stomatal opening, which may be related to ATP production through glycolysis and mitochondrial metabolism, and/or accumulation of osmolytes such as sugars and malate. However, experimental evidence supporting this theory is lacking. Here we highlight the particularities of guard cell metabolism and discuss this in the context of the guard cells themselves and their interaction with the mesophyll cells.

On the role of the tricarboxylic acid cycle in plant productivity

“…Given the lack of consensus regarding the above two postulates, several other roles for mitochondria, during photosynthesis, have been proposed, including the balance of cellular redox status (Raghavendra and Padmasree ; Scheibe ), buffering of metabolism by photorespiration, and/or the alternative oxidase (Rasmusson et al ; Bauwe et al ), or retrograde signaling (Zarkovic et al ; Alhagdow et al ). That being said, as we detail later, a renaissance of work related to guard cell metabolism (Daloso et al ) has revealed that, counter to the perceived wisdom at the turn of the century (Outlaw ), malate does play a considerable role in guard cell function (Lee et al ; Araujo et al ).…”

Toward multifaceted roles of sucrose in the regulation of stomatal movement

“…28 We hypothesize that the C derived from sucrose breakdown would be directed toward Gln biosynthesis which would act as a signal to activate FUM activity and thus fumarate accumulation, a metabolite showed to accumulate in guard cells during dark-to-light transition. 20 In addition, it has been shown that guard cells have higher anaplerotic CO 2 fixation catalysed by the enzyme phosphoenolpyruvate carboxylase (PEPc) compared to mesophyll cells 12,24 and that this reaction activate the left branch of the TCA cycle. 22 Taken together, these results suggest that left and right branches of the TCA cycle are differentially activated depending on the source of the C, in which different non-cyclic modes of operation can be observed in this cycle.…”

“…derived from sucrose breakdown is directed toward Gln synthesis as a mechanism to stimulate FUM activity and fumarate accumulation (Figure 3), an important organic acid for stomatal movement regulation. 12 Fumarate and malate are the two main organic acids involved in the regulation of stomatal movement. 38,39 Similar to sucrose, they have also been pointed out as important metabolites for both stomatal opening and closure.…”

“…Most of the recent achievements is reviewed elsewhere. [11][12][13] Here, we provide an update in this field based on the results obtained from the most recent published works. We highlight recent metabolic and systems biology studies that have improved our understanding of guard cell sucrose metabolism and that have contributed to solve the controversy story regarding the role of sucrose in the regulation of stomatal movement.…”

From reproduction to production, stomata are the master regulators

“…Starch breakdown is induced by blue light in Arabidopsis guard cells via a pathway that is downstream of the phototropin‐dependent pathway for H + ‐ATPase activation, and light‐induced stomatal opening is delayed in mutants deficient in the α‐ (AMY3) and β‐amylases (BAM1) involved in starch degradation (Valerio et al , ; Horrer et al , ). The sugars released by starch breakdown may initially decrease guard cell osmotic potential, contributing to stomatal opening, and most are likely used for the synthesis of malate, which acts as a counter ion to K + , however the precise role of sugars in stomatal movement is still being elucidated (Granot and Kelly, ; Santelia and Lunn, ; see Daloso et al , ). Genes from the BAM1 and AMY3 clades are present in all land plants, including bryophytes (Thalmann et al , ; Ju et al , ), and the possibility that there is a conserved role in stomatal opening remains to be examined.…”