The breakdown of stored triacylglycerols is required during light-induced stomatal opening

TY - JOUR

T1 - The breakdown of stored triacylglycerols is required during light-induced stomatal opening

AU - McLachlan, Deirdre H

AU - Lan, Jue

AU - Geilfus, Christoph-Martin

AU - Dodd, Anthony N

AU - Larson, TR

AU - Baker, Alison

AU - Horak, Hanna

AU - Kollist, Hannes

AU - He, Zhesi

AU - Graham, Ian Alexander

AU - Mickelbart, Michael V

AU - Hetherington, Alistair M.

N1 - © 2016 Authors. This content is made available by the publisher under a Creative Commons Attribution Licence. This means that a user may copy, distribute and display the resource providing that they give credit. Users must adhere to the terms of the licence.

PY - 2016/3/7

Y1 - 2016/3/7

N2 - Stomata regulate the uptake of CO 2 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 [3-6]. 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.

AB - Stomata regulate the uptake of CO 2 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 [3-6]. 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.

KW - Arabidopsis Proteins/metabolism

KW - Arabidopsis/genetics

KW - Light

KW - Plant Stomata/physiology

KW - Triglycerides/metabolism

UR - http://www.scopus.com/inward/record.url?scp=84960432012&partnerID=8YFLogxK

U2 - 10.1016/j.cub.2016.01.019

DO - 10.1016/j.cub.2016.01.019

M3 - Article

C2 - 26898465

SN - 0960-9822

VL - 26

SP - 707

EP - 712

JO - Current Biology

JF - Current Biology

IS - 5

ER -