Unsaturation of Very-Long-Chain Ceramides Protects Plant from Hypoxia-Induced Damages by Modulating Ethylene Signaling in Arabidopsis

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.

Plant acyl-CoA-binding proteins: An emerging family involved in plant development and stress responses

“…There was an increase in the degree of unsaturation of VLC ceramides that protects plants against hypoxia-induced damages by regulating ethylene signaling in Arabidopsis [177]. In addition, hypoxia usually occurs with other environmental stresses such as darkness in flooding/submergence under the natural environment, consistent with observations that AtACBP3 contributes to the dark-induced leaf senescence by modulating membrane phospholipids and the stability of an autophagy-related protein ATG8 [43].…”

Group VII Ethylene Response Factors in Arabidopsis: Regulation and Physiological Roles

“…During hypoxia, AtRAP2.12 is quickly displaced from the plasma membrane toward the nucleus . Given that the regulation of fatty acid profiles has been associated with hypoxic stress (Klinkenberg et al, 2014;Xie et al, 2015a;Xie et al, 2015b), the evidence available can be the basis of a speculative model of hypoxia sensing, in which the dynamic acylation state of the ERF-VII TFs collects indirect low oxygen signals to regulate their intracellular trafficking and activity.…”

Polyunsaturated linolenoyl‐CoA modulates ERF‐VII‐mediated hypoxia signaling in Arabidopsis

“…Given that the recombinant ACBP3 bound to VLCACoAs better than LCACoAs in vitro , these findings implied that extracellular ACBP3 is involved in the negative regulation of hypoxia responses by modulating VLC fatty acid metabolism in Arabidopsis (Xie et al 2015b). Through a comprehensive mass spectrometry‐based investigation, our subsequent study discovered that upon hypoxia, Arabidopsis rosettes accumulate significant amounts of ceramides (Xie et al 2015a). By genetic and phenotypic analyses, we demonstrated that the dynamic unsaturation of VLC ceramides likely functions as a novel protective mechanism for hypoxia tolerance in Arabidopsis (Xie et al 2015a).…”