Plant sphingolipids: decoding the enigma of the Sphinx

Abstract

Sphingolipids are a ubiquitous class of lipids present in a variety of organisms including eukaryotes and bacteria. In the last two decades, research has focused on characterizing the individual species of this complex family of lipids, which has led to a new field of research called 'sphingolipidomics'. There are at least 500 (and perhaps thousands of) different molecular species of sphingolipids in cells, and in Arabidopsis alone it has been reported that there are at least 168 different sphingolipids. Plant sphingolipids can be divided into four classes: glycosyl inositol phosphoceramides (GIPCs), glycosylceramides, ceramides, and free long-chain bases (LCBs). Numerous enzymes involved in plant sphingolipid metabolism have now been cloned and characterized, and, in general, there is broad conservation in the way in which sphingolipids are metabolized in animals, yeast and plants. Here, we review the diversity of sphingolipids reported in the literature, some of the recent advances in our understanding of sphingolipid metabolism in plants, and the physiological roles that sphingolipids and sphingolipid metabolites play in plant physiology.

Fig. 1

Structures of representative C18 long chain bases (LCBs) found in plants. Trivial names and systematic names are consistent with IUPAC (http://www.chem.qmul.ac.uk/iupac/lipid/) regulations and shorthand designations are given for each LCB. All dihydroxy (d) and trihydroxy (t) LCBs are naturally occurring in plants with D-erythro and D-ribo configurations, respectively. These LCBs are detected as part of ceramides, complex sphingolipids or as free LCBs.

Fig. 2

Schematic representation of complex sphingolipids from plants. The general structure of complex sphingolipids is based on a hydrophobic ceramide core and a hydrophilic head group. The ceramide core is made up of two moieties, a long chain base (LCB) and a fatty acid (FA) linked via an amide bond. The LCB moiety can vary and some of the common LCBs are shown in Fig. 1. The FA can vary in length, unsaturation and hydroxylation. The ceramide core shown here is dihydroceramide, which is a biosynthetic precursor of ceramide cores in the de novo pathway. GlcCER, glycosylceramide; IPC, inositolphospho ceramide. IPC can be further glycosylated with different sugar residues.

Fig. 3

Schematic representation of the sphingolipid biosynthesis pathway in plants. All metabolic steps indicated by a plain arrow have been demonstrated in vitro. Activities are indicated in black boxes. Genes which have been cloned are indicated in dark grey ovals. The substrates for desaturation and fatty acid (FA) hydroxylase remain to be determined. Although ceramidase (CDase) activity has been detected, the substrate specificity remains to be characterized. Note that reverse CDase activity (RCDA) and CDase are activities from the same enzyme. LCB, long chain base; IPC, inositolphospho ceramide.

Fig. 4

Schematic representation of the sphingolipid metabolic pathway for phosphorylation of ceramides and long chain bases (LCBs) in plants. Activities are indicated in black boxes. Genes which have been cloned are indicated in dark grey ovals. The substrate specificity has been characterized for LCB lyase and LCB kinase. Biochemical properties of LCB-P phosphatase remain to be determined.

Fig. 5

Schematic representation of the structure of the long chain base phosphates, 4-sphingenine-1-phosphate (S1P; d18:1^Δ4E-1-P), sphingahine-1-phosphate (dihydro-S1P; d18:0-1-P), and 4-hydroxysphinganine-1-phosphate (phyto-S1P; t18:0-1-P). The allylic alcohol group of d18:1^Δ4E-1-P comprising the hydroxyl group at C3 and Δ4 double bond (C4) is shown. The position of the carbon atoms are shown in numbers (only positions 3–5 are indicated). In 4-hydroxysphinganine-1-phosphate, a hydroxyl group is present at C4 as opposed to a Δ4 double bond which is characteristic of d18:1^Δ4E-1-P.