Abstract
Lipid remodeling is crucial for hypoxic tolerance in animals, whilst little is known about the hypoxia-induced lipid dynamics in plants. Here we performed a mass spectrometry-based analysis to survey the lipid profiles of Arabidopsis rosettes under various hypoxic conditions. We observed that hypoxia caused a significant increase in total amounts of phosphatidylserine, phosphatidic acid and oxidized lipids, but a decrease in phosphatidylcholine (PC) and phosphatidylethanolamine (PE). Particularly, significant gains in the polyunsaturated species of PC, PE and phosphatidylinositol, and losses in their saturated and mono-unsaturated species were evident during hypoxia. Moreover, hypoxia led to a remarkable elevation of ceramides and hydroxyceramides. Disruption of ceramide synthases LOH1, LOH2 and LOH3 enhanced plant sensitivity to dark submergence, but displayed more resistance to submergence under light than wild type. Consistently, levels of unsaturated very-long-chain (VLC) ceramide species (22:1, 24:1 and 26:1) predominantly declined in the loh1, loh2 and loh3 mutants under dark submergence. In contrast, significant reduction of VLC ceramides in the loh1-1 loh3-1 knockdown double mutant and lacking of VLC unsaturated ceramides in the ads2 mutants impaired plant tolerance to both dark and light submergences. Evidence that C24:1-ceramide interacted with recombinant CTR1 protein and inhibited its kinase activity in vitro, enhanced ER-to-nucleus translocation of EIN2-GFP and stabilization of EIN3-GFP in vivo, suggests a role of ceramides in modulating CTR1-mediated ethylene signaling. The dark submergence-sensitive phenotypes of loh mutants were rescued by a ctr1-1 mutation. Thus, our findings demonstrate that unsaturation of VLC ceramides is a protective strategy for hypoxic tolerance in Arabidopsis.
Highlights
Lipids are essential constituents of plant cells that provide both the structural basis for cell membranes and an energy source for cellular metabolism [1,2]
The Group VII ethylene-responsive factors (ERFs) have been demonstrated to be master regulators for oxygen sensing through an N-end rule protein degradation mechanism
Recent investigations have suggested that lipid molecules such VLC ceramides may play crucial roles in hypoxia signaling in both animal and plant cells
Summary
Lipids are essential constituents of plant cells that provide both the structural basis for cell membranes and an energy source for cellular metabolism [1,2]. A wide range of molecules including very-longchain fatty acids (VLCFAs) and their derivatives such as sphingolipids and cuticular lipids, play indispensable roles in regulation of plant stress responses [5,6]. VLCFAs are direct precursors for biosynthesis of cuticular lipids and sphingolipids; the latter act as major components of the plasma membrane and play key roles in intracellular activities as well as diverse signaling pathways [8,9]. The sphingolipids are composed of a polar head group, a sphingoid long-chain base (LCB) and an amidelinked fatty-acyl chain. Among these components, the fatty acid chains vary in length from 16 to 26 carbon atoms, which can be either saturated or unsaturated with a cis-ω9 double bond [10]. Ceramides serve as both intermediates for turnover of sphingolipids and backbones for synthesis of more complex sphingolipids in planta
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