The Breakdown of Stored Triacylglycerols Is Required during Light-Induced Stomatal Opening

Abstract

SummaryStomata regulate the uptake of CO2 and the loss of water vapor [1] and contribute to the control of water-use efficiency [2] in plants. Although the guard-cell-signaling pathway coupling blue light perception to ion channel activity is relatively well understood [3], we know less about the sources of ATP required to drive K+ uptake [3, 4, 5, 6]. Here, we show that triacylglycerols (TAGs), present in Arabidopsis guard cells as lipid droplets (LDs), are involved in light-induced stomatal opening. Illumination induces reductions in LD abundance, and this involves the PHOT1 and PHOT2 blue light receptors [3]. Light also induces decreases in specific TAG molecular species. We hypothesized that TAG-derived fatty acids are metabolized by peroxisomal β-oxidation to produce ATP required for stomatal opening. In silico analysis revealed that guard cells express all the genes required for β-oxidation, and we showed that light-induced stomatal opening is delayed in three TAG catabolism mutants (sdp1, pxa1, and cgi-58) and in stomata treated with a TAG breakdown inhibitor. We reasoned that, if ATP supply was delaying light-induced stomatal opening, then the activity of the plasma membrane H+-ATPase should be reduced at this time. Monitoring changes in apoplastic pH in the mutants showed that this was the case. Together, our results reveal a new role for TAGs in vegetative tissue and show that PHOT1 and PHOT2 are involved in reductions in LD abundance. Reductions in LD abundance in guard cells of the lycophyte Selaginella suggest that TAG breakdown may represent an evolutionarily conserved mechanism in light-induced stomatal opening.

Critical roles for α/β hydrolase domain 5 (ABHD5)/comparative gene identification-58 (CGI-58) at the lipid droplet interface and beyond

“…This report is in agreement with similar findings in human colorectal cancer cells [56]. Also, CGI-58-facilitated TAG hydrolysis in plants has recently been shown to be necessary for the physiological process of light-induced stomatal opening [101]. Therefore, in a manner similar to vertebrate CGI-58 isoforms, plant CGI-58 regulates TAG hydrolysis to provide critical fuel for ATP synthesis, but also participates in the generation of hormone-like second messengers that further shape cellular energy metabolism and physiological processes such as stomatal opening (Fig.…”

Blue Light Regulation of Stomatal Opening and the Plasma Membrane H+-ATPase

“…Correspondingly, guard cells lacking chloroplasts in the crumpled leaf mutant displayed attenuation of both guard cell ATP levels and stomatal opening in response to light (Wang et al, 2014). Stored triacylglycerols in guard cells are broken down in response to light and the catabolic process is also thought to supply ATP for PM H + -ATPase activity in stomatal opening (McLachlan et al, 2016).…”

Plant peroxisomes: recent discoveries in functional complexity, organelle homeostasis, and morphological dynamics

“…The SUGAR-DEPENDENT1 lipase (SDP1) [14] and PXA1 transporter [9,15] are required not only for lipid mobilization during germination but also contribute to stomatal opening [16]. Blue-light-induced stomatal opening is accompanied by reduced oil body volume in Arabidopsis guard cells, and sdp1 , pxa1 , and cgi58 mutants all display slowed light-induced stomatal opening, presumably because impaired fatty acid catabolism reduces ATP production in these mutants and limits apoplast acidification [16]. These findings provide a rationale for the occurrence of stomatal oil bodies throughout the plant kingdom [16].…”