Abstract
BackgroundCeramide kinase (CERK) is a key regulator of cell survival in dicotyledonous plants and animals. Much less is known about the roles of CERK and ceramides in mediating cellular processes in monocot plants. Here, we report the characterization of a ceramide kinase, OsCERK, from rice (Oryza sativa spp. Japonica cv. Nipponbare) and investigate the effects of ceramides on rice cell viability.Principal Findings OsCERK can complement the Arabidopsis CERK mutant acd5. Recombinant OsCERK has ceramide kinase activity with Michaelis-Menten kinetics and optimal activity at 7.0 pH and 40°C. Mg2+ activates OsCERK in a concentration-dependent manner. Importantly, a CXXXCXXC motif, conserved in all ceramide kinases and important for the activity of the human enzyme, is critical for OsCERK enzyme activity and in planta function. In a rice protoplast system, inhibition of CERK leads to cell death and the ratio of added ceramide and ceramide-1-phosphate, CERK's substrate and product, respectively, influences cell survival. Ceramide-induced rice cell death has apoptotic features and is an active process that requires both de novo protein synthesis and phosphorylation, respectively. Finally, mitochondria membrane potential loss previously associated with ceramide-induced cell death in Arabidopsis was also found in rice, but it occurred with different timing.Conclusions OsCERK is a bona fide ceramide kinase with a functionally and evolutionarily conserved Cys-rich motif that plays an important role in modulating cell fate in plants. The vital function of the conserved motif in both human and rice CERKs suggests that the biochemical mechanism of CERKs is similar in animals and plants. Furthermore, ceramides induce cell death with similar features in monocot and dicot plants.
Highlights
Sphingolipids are key structural components of membranes and important signal molecules for cell growth, cell death, embryogenesis and development [1,2,3]
OsCERK is a bona fide ceramide kinase with a functionally and evolutionarily conserved Cys-rich motif that plays an important role in modulating cell fate in plants
We report the cloning of a ceramide kinase in rice and demonstrate that OsCERK is a bona fide ceramide kinase that can completely rescue acd5 mutant phenotypes, including spontaneous cell death, susceptibility to bacterial infection, reduced Ceramide kinase (CERK) activity and elevated PR1 expression
Summary
Sphingolipids are key structural components of membranes and important signal molecules for cell growth, cell death, embryogenesis and development [1,2,3]. Sphingolipid metabolism and functions have been intensively researched in animals and yeast Sphingolipids and their metabolic intermediates, including ceramide, sphingosine, sphingosine-1-phosphate, and ceramide1-phosphate (C1P), are significant bioactive molecules in a variety of biological processes [4]. Ceramide, which is the central core lipid in the metabolism of sphingolipids, mediates cell cycle events, differentiation, senescence, necrosis, proliferation and apoptosis [5]. Sphingosine, a metabolite of ceramide, exerts pleiotropic effects on protein kinases and other targets in animals, including regulating the actin cytoskeleton, endocytosis, cell cycle and apoptosis [3], whereas sphingosine-1-phosphate is intimately involved in cell motility, cell survival, cell proliferation and inflammation [1,3]. Ceramide kinase (CERK) is a key regulator of cell survival in dicotyledonous plants and animals. Nipponbare) and investigate the effects of ceramides on rice cell viability
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