Abstract
Sphingolipids have essential structural and bioactive functions in membranes and in signaling. However, how plants regulate sphingolipid biosynthesis in the response to stress remains unclear. Here, we reveal that the plant hormone ethylene can modulate sphingolipid synthesis. The fungal toxin Fumonisin B1 (FB1) inhibits the activity of ceramide synthases, perturbing sphingolipid homeostasis, and thus inducing cell death. We used FB1 to test the role of ethylene signaling in sphingolipid synthesis in Arabidopsis thaliana. The etr1-1 and ein2 mutants, which have disrupted ethylene signaling, exhibited hypersensitivity to FB1; by contrast, the eto1-1 and ctr1-1 mutants, which have enhanced ethylene signaling, exhibited increased tolerance to FB1. Gene expression analysis showed that during FB1 treatment, transcripts of genes involved in de novo sphingolipid biosynthesis were down-regulated in ctr1-1 mutants but up-regulated in ein2 mutants. Strikingly, under normal conditions, ctr1-1 mutants contained less ceramides and hydroxyceramides, compared with wild type. After FB1 treatment, ctr1-1 and ein2 mutants showed a significant improvement in sphingolipid contents, except the ctr1-1 mutants showed little change in hydroxyceramide levels. Treatment of wild-type seedlings with the ethylene precursor 1-aminocyclopropane carboxylic acid down-regulated genes involved in the sphingolipid de novo biosynthesis pathway, thus reducing sphingolipid contents and partially rescuing FB1-induced cell death. Taking these results together, we propose that ethylene modulates sphingolipids by regulating the expression of genes related to the de novo biosynthesis of sphingolipids.
Highlights
Sphingolipids, the complex membrane lipids found ubiquitously in eukaryotes, have important functions in nutrient transport, inflammation, cell differentiation, mitogenesis, migration, apoptosis, senescence, and autophagy (Guenther et al, 2008; Hannun and Obeid, 2008; Hla and Dannenberg, 2012; Sentelle et al, 2012; Maceyka and Spiegel, 2014)
As ethylene plays a pivotal role in Fumonisin B1 (FB1)-induced cell death (Plett et al, 2009), we inferred that ethylene signaling may affect sphingolipid synthesis
We explored the role of ethylene signaling in sphingolipid synthesis by using the ceramide synthase inhibitor FB1
Summary
Sphingolipids, the complex membrane lipids found ubiquitously in eukaryotes, have important functions in nutrient transport, inflammation, cell differentiation, mitogenesis, migration, apoptosis, senescence, and autophagy (Guenther et al, 2008; Hannun and Obeid, 2008; Hla and Dannenberg, 2012; Sentelle et al, 2012; Maceyka and Spiegel, 2014). A sphingolipid has three parts: a long chain base moiety, a fatty acid moiety, and a head group (Sperling and Heinz, 2003; Pata et al, 2010). According to their molecular structures, plant sphingolipids can be divided into four classes: long-chain bases (LCBs), ceramides, glycosylceramides, and glycosyl inositol phosphoceramides (GIPCs; Pata et al, 2010). The de novo synthesis of sphingolipids starts from a condensation reaction of serine and palmitoyl-CoA by serine palmitoyltransferase (SPT). The resulting 3-keto-dihydrosphingosine is reduced to a LCB, which forms the backbone of sphingolipids.
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