The Black-Box of Plant Apoplast Lipidomes

The apoplast has gained recent attention owing to advances in—omics approaches, esp. the proteomics studies in apoplasts, xylem saps, and intercellular washing fluids (IWF) from diverse plant species. Apoplastic interactions are integral to plant signaling, growth, defense, physiology, and reproduction. In addition, the plant apoplast serves as a hub of pathogen effectors and a great deal of pathogenic proteins and small molecules are cataloged in literature. In spite of its importance in plant biology, the knowledge about apoplastic lipids and their carriers have been limited to few seminal studies and sporadic efforts. Here, the attempt is to comprehend the gained knowledge and remaining gaps in plant apoplastic lipidomes and address means as to how efforts can unveil the black box of plant apoplastic lipidome. The apoplast is defined as the extracellular matrix, the plant cell wall and the intercellular spaces where the apoplastic fluid circulates (Agrawal et al., 2010). In addition, the intercellular fluids and xylem sap samples, for instance represent the apoplastic system that transports distinct molecules along the plant system (Kehr and Rep, 2007; Seifert and Blaukopf, 2010). In vascular plants, the apoplastic xylem saps demonstrate considerable differences in composition from the apoplast used in phloem loading. The complement of all proteins and metabolites that are exported out of the symplast comprises the plant's secretome (or apoplastic proteome and metabolome, respectively). Important roles assigned to apoplastic proteome is that of conferring basal immunity (Feussner and Polle, 2015) among other important functions. Plant apoplast proteomics studies conducted in tobacco (Dani et al., 2005; Goulet et al., 2010), cowpea (Fecht-Christoffers et al., 2003), Arabidopsis (Boudart et al., 2005; Kwon et al., 2005; Ge et al., 2011; Floerl et al., 2012), canola (Floerl et al., 2008), rice (Zhang et al., 2009), soybean (Djordjevic et al., 2007), poplar (Pechanova et al., 2010), and Medicago (Soares et al., 2009) have furthered our knowledge by helping researchers catalog proteins involved in pathogen interactions, heavy metal accumulation, oxidative stress, pollen germination, cell wall biosynthesis and regeneration, salinity stress tolerance among other pivotal plant physiological, and defense responses. Moreover, the plant secretome proteomes have been reviewed elsewhere (Jwa, 2008; Agrawal et al., 2010; Alexandersson et al., 2013; Krause et al., 2013). In contrast, transcriptomic (Blomster et al., 2011) and metabolomics (Floerl et al., 2012) studies of apoplasts are rare and remains to be explored. Surprisingly, absolutely no information is available yet on the lipidome of the plant apoplast. Plant lipidome is huge and the major classes of lipids discovered till date include, but are not limited to, triacylglycerols (TAGs)—the most abundant class of storage lipids, wax esters, sterols, sterol esters, acylated sterol glycosides, phytoglycolipids, ceramides, glucosylceramides. For instance only phospholipids consists of major classes of phospholipids such as phosphatidylcholines (PC), phosphatidylglycerols (PG), phosphatidylethanolamines (PE), phosphatidylserines (PS), and phosphatidylinositols (PI) are structural phospholipids that have distinct and specific distributions in the cellular membranes, contributing to their identity (van Meer et al., 2008). On the other hand, phosphatidic acid (PA), phosphatidylinositolmonophosphate (PIP), phosphatidylinositolbisphosphate (PIP2) and lysophospholipids such as lysophosphatidylcholine (LPC), lysophosphatidylethanolamine (LPE), and lysophosphatidic acid (LPA) are produced from structural phospholipids by specific enzymatic pathways and are minor constituents of the cell membranes (Meijer and Munnik, 2003). Although information on the plant lipidome exists in the form of oil-crops and seed oils, little is known about their apoplastic abundances or distribution. Hence, in this review, we look into the apoplast lipids and their associated biosynthetic machineries, where a lot have been deciphered in terms of bound proteins, polymers, and proteins. Apoplast includes the cell-walls which are known to boast a diverse metabolites, the extracellular spaces where the “secretomes” are released (including the organ surfaces) and cuticles which is consisted of lipid and hydrocarbon polymers impregnated with wax among others. Cell walls include macromolecular polymeric structures such as lignins, pectins, cellulose among others. Suberin is an apoplastic biopolymer that contributes to the control of diffusion of water and solutes across internal root tissues and in periderms (Ranathunge et al., 2011). However, I exclude the cell-wall bound apoplastic constituents to focus on the dynamic aspects of lipidome.