Impaired Malate and Fumarate Accumulation Due to the Mutation of the Tonoplast Dicarboxylate Transporter Has Little Effects on Stomatal Behavior

Abstract

Malate is a central metabolite involved in a multiplicity of plant metabolic pathways, being associated with mitochondrial metabolism and playing significant roles in stomatal movements. Vacuolar malate transport has been characterized at the molecular level and is performed by at least one carrier protein and two channels in Arabidopsis () vacuoles. The absence of the Arabidopsis tonoplast Dicarboxylate Transporter (tDT) in the knockout mutant was associated previously with an impaired accumulation of malate and fumarate in leaves. Here, we investigated the consequences of this lower accumulation on stomatal behavior and photosynthetic capacity as well as its putative metabolic impacts. Neither the stomatal conductance nor the kinetic responses to dark, light, or high CO were highly affected in plants. In addition, we did not observe any impact on stomatal aperture following incubation with abscisic acid, malate, or citrate. Furthermore, an effect on photosynthetic capacity was not observed in the mutant lines. However, leaf mitochondrial metabolism was affected in the plants. Levels of the intermediates of the tricarboxylic acid cycle were altered, and increases in both light and dark respiration were observed. We conclude that manipulation of the tonoplastic organic acid transporter impacted mitochondrial metabolism, while the overall stomatal and photosynthetic capacity were unaffected.

The Role of Abscisic Acid Signaling in Maintaining the Metabolic Balance Required for Arabidopsis Growth under Nonstress Conditions

“…Subsequently, ABA or ethanol (solvent control) was added to the opening buffer to a final concentration of 5 mM ABA. After 2 h of incubation, images of the abaxial epidermis were taken as described in Medeiros et al (2017).…”

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 2003;Scheibe 2004), buffering of metabolism by photorespiration, and/or the alternative oxidase (Rasmusson et al 2009;Bauwe et al 2010), or retrograde signaling (Zarkovic et al 2005;Alhagdow et al 2007). That being said, as we detail later, a renaissance of work related to guard cell metabolism (Daloso et al 2017) has revealed that, counter to the perceived wisdom at the turn of the century (Outlaw 2003), malate does play a considerable role in guard cell function (Lee et al 2008;Araujo et al 2011).…”

“…Interestingly, the downregulation of AtQUAC1, an R-type anion channel responsible for the release of malate from guard cells, also resulted in a similar photosynthetic phenotype (Medeiros et al 2016), whereas the downregulation of the vacuolar malate transporter had little effect on either stomatal conductance or photosynthesis, with seemingly prioritizing malate for maintaining photosynthesis at the cost of photosynthesis (Medeiros et al 2017). Although we have previously expressed caution as to the applicability of enhancing photosynthesis by altering malate levels to field-grown crops, two recent studies suggest it may also be relevant for such plants.…”

Toward multifaceted roles of sucrose 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. [40][41][42] Whilst the accumulation of these metabolites at the apoplastic space of guard cells would be a mechanism to regulate anion efflux channels, [43][44][45] their accumulation within guard cell vacuoles act as counter-ion of K + during light-induced stomatal opening. Thus, Gln-mediated FUM1 and FUM2 activation could be a mechanism to increase the amount of fumarate to act as counter ion of K + (Figure 3).…”