Abstract
Sphingolipids act as regulators of programmed cell death (PCD) and the plant defence response. The homeostasis between long-chain base (LCB) and ceramide (Cer) seems to play an important role in executions of PCD. Therefore, deciphering the role of neutral ceramidases (NCER) is crucial to identify the sphingolipid compounds that trigger and execute PCD. We performed comprehensive sphingolipid and phytohormone analyses of Arabidopsis ncer mutants, combined with gene expression profiling and microscopic analyses. While ncer1 exhibited early leaf senescence (developmentally controlled PCD - dPCD) and an increase in hydroxyceramides, ncer2 showed spontaneous cell death (pathogen-triggered PCD-like - pPCD) accompanied by an increase in LCB t18:0 at 35d, respectively. Loss of NCER1 function resulted in accumulation of jasmonoyl-isoleucine (JA-Ile) in the leaves, whereas disruption of NCER2 was accompanied by higher levels of salicylic acid (SA) and increased sensitivity to Fumonisin B1 (FB1 ). All mutants were also found to activate plant defence pathways. These data strongly suggest that NCER1 hydrolyses ceramides whereas NCER2 functions as a ceramide synthase. Our results reveal an important role of NCER in the regulation of both dPCD and pPCD via a tight connection between the phytohormone and sphingolipid levels in these two processes.
Highlights
Sphingolipids are a diverse group of lipids ubiquitously distributed in eukaryotic cells and in a few bacteria (Hannun & Obeid, 2008; Pata et al, 2010)
Phylogenetic analysis of putative plant neutral ceramidases showed that Arabidopsis NCER1 together with NCER3 form a distinct branch than AtNCER2 (Fig. S1)
Arabidopsis NCER2 is highly related to other putative NCER2s from species belonging to the Brassicaceae family, such as Capsella rubella or Brassica napus
Summary
Sphingolipids are a diverse group of lipids ubiquitously distributed in eukaryotic cells and in a few bacteria (Hannun & Obeid, 2008; Pata et al, 2010). In animals, their structural role, sphingolipid metabolites regulate many cellular processes including autophagy or apoptosis (Young et al, 2013). It has been demonstrated that sphingolipids play an important role in the regulation of programmed cell death (PCD) occurring during plant development (developmentally controlled PCD – dPCD) (Li et al, 2016) or associated with plant defence responses (pathogen-triggered PCD-like – pPCD) (Ternes et al, 2011; K€onig et al, 2012; Bi et al, 2014). The ratio between the content of LCB and their phosphorylated form (LCBP) was found to be correlated with the degree of FB1-induced PCD
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