Guarding the gates: TOR mediates guard cell starch degradation to control stomatal opening

On a typical day, just after dawn, guard cell blue-light receptors activate and initiate signals for leaf stomata to open. A complex intercellular signaling cascade follows that rapidly culminates in increased guard cell turgor pressure that drives stomatal opening needed to facilitate photosynthetic gas exchange. At the metabolic level, several changes occur in guard cells to cause the build-up of ions and metabolites that drive water uptake and swelling by osmosis. One such event is the rapid breakdown of starch into glucose in the guard cell chloroplasts (Flütsch et al., 2020). Besides being essential for stomatal opening, guard cell starch degradation is interesting because it occurs at a different time (dawn) and requires different enzyme isoforms than the typical nocturnal starch degradation that occurs in other leaf cells. In their recent Plant Cell article, Chao Han and colleagues (Han et al., 2022) sought to elucidate the mechanism by which guard cells control their starch degradation. Using Arabidopsis leaf epidermal peals, which allow enrichment of intact guard cells, the authors observed that inhibition of a regulatory kinase called target of rapamycin (TOR), by either chemical or genetic means, completely blocked the light-induced breakdown of starch in guard cells (Figure A). TOR-dependent inhibition of starch breakdown consequently blocked light-induced stomatal aperture formation (Figure B). The function of TOR as a master regulator of many aspects of energy, growth and stress metabolism across all eukaryotes is well established. However, a role for TOR in controlling stomatal opening had not previously been described. TOR-dependent starch degradation and stomatal opening in Arabidopsis guard cells. Time course visualization by confocal microscopy of starch granule size (A) and stomatal aperture (B) in epidermal peals following treatment with the specific TOR inhibitor AZD8055. EoN, end of night and EoD, end of day. Adapted from Han et al. (2022), Figure 1. It was known that a specific isoform of β-amylase, β-amylase 1 (BAM1), is needed for starch degradation in guard cells (Horrer et al., 2016). Han et al. (2022) used transcript and protein quantification to determine that BAM1 protein level in guard cells was strongly upregulated by 1 h of light treatment after dawn, or by exogenous sugars, but either process was blocked if TOR was inactivated. Furthermore, the ability of TOR to inhibit BAM1 accumulation was prevented by the inclusion of either autophagy or proteasome inhibitors. These inhibitors also partly reversed the effects of TOR inhibition on starch degradation and stomatal opening. This evidence suggested that TOR exerts control over guard cell function by regulating the accumulation of BAM1. Previous phosphoproteomics analysis revealed that BAM1 contains a TOR-dependent phosphorylation site on its N-terminus at Ser31 (Van Leene et al., 2019). Here, the authors determined that this phosphorylation of BAM1 is of clear regulatory importance in guard cells. Plants expressing site-directed BAM1 mutants lacking the N-terminal phosphosite reproduced the effects of TOR inhibition within guard cells with respect to reduced BAM1 stability, starch degradation, and stomatal opening. Conversely, plants expressing BAM1 with a phospho-mimetic Ser-Asp mutation at residue 31 were immune to the effects of TOR inhibition on BAM1 stability, guard cell starch degradation, and stomatal opening. These results indicate a molecular mechanism whereby activation of TOR leads to downstream stabilizing phosphorylation of BAM1 at Ser31, leading to the accumulation of BAM1 activity and the rapid degradation of guard cell starch. More work is needed to place this TOR-dependent regulatory mechanism in the context of other signaling components such as brassinosteroids, which also influence stomatal opening via starch degradation (Li et al., 2020). The physiological implications of TOR control of stomatal opening also require investigation: what environmental conditions might signal to restrict TOR activity and thus the opening of stomata even in the presence of light?

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