Peroxisome extensions deliver the Arabidopsis SDP1 lipase to oil bodies

Abstract

Lipid droplets/oil bodies (OBs) are lipid-storage organelles that play a crucial role as an energy resource in a variety of eukaryotic cells. Lipid stores are mobilized in the case of food deprivation or high energy demands-for example, during certain developmental processes in animals and plants. OB degradation is achieved by lipases that hydrolyze triacylglycerols (TAGs) into free fatty acids and glycerol. In the model plant Arabidopsis thaliana, Sugar-Dependent 1 (SDP1) was identified as the major TAG lipase involved in lipid reserve mobilization during seedling establishment. Although the enzymatic activity of SDP1 is associated with the membrane of OBs, its targeting to the OB surface remains uncharacterized. Here we demonstrate that the core retromer, a complex involved in protein trafficking, participates in OB biogenesis, lipid store degradation, and SDP1 localization to OBs. We also report an as-yet-undescribed mechanism for lipase transport in eukaryotic cells, with SDP1 being first localized to the peroxisome membrane at early stages of seedling growth and then possibly moving to the OB surface through peroxisome tubulations. Finally, we show that the timely transfer of SDP1 to the OB membrane requires a functional core retromer. In addition to revealing previously unidentified functions of the retromer complex in plant cells, our work provides unanticipated evidence for the role of peroxisome dynamics in interorganelle communication and protein transport.oil bodies | retromer | SDP1 lipase | peroxisome | protein trafficking

Bioinformatics Reveal Five Lineages of Oleosins and the Mechanism of Lineage Evolution Related to Structure/Function from Green Algae to Seed Plants

“…No such docking signals in oleosins or perilipins on mammalian LDs are known. Naturally, lipase must bind to LDs for lipolysis, as shown in Arabidopsis seed (Thazar-Poulot et al, 2015). Phosphorylated perilipin interacts with lipase via a lipase moderator, a/b hydrolase domain-containing protein5, and binds to mitochondria via its C-terminal peptide; motifs in perilipin for these interactions are unknown (Wang et al, 2011).…”

Peroxisome Function, Biogenesis, and Dynamics in Plants

“…Peroxules can mediate interorganellar contacts, such as among peroxisomes and ER (Sinclair et al, 2009), oil bodies (Thazar-Poulot et al, 2015), mitochondria (Jaipargas et al, 2016), and chloroplasts (Gao et al, 2016). Moreover, peroxules can respond to environmental signals.…”

Molecular Mechanisms and Physiological Significance of Organelle Interactions and Cooperation

“…Finally, live cell imaging of peroxisomes in mammals and plants revealed that peroxisomes can form tubular membrane protrusions, which vividly extend and retract, and are thought to mediate interactions with other peroxisomes and organelles. Very recently, peroxisomal membrane extensions were reported to mediate contact with oil bodies (see Section Lipid Droplets) in the model plant Arabidopsis thaliana and to deliver a membrane-bound lipase, required for lipid mobilization during seedling establishment (Thazar-Poulot et al, 2015). Membrane protrusions may also be involved in the transfer of membrane lipids.…”

“…RAB18 presumably binds to droplets from the cytosol through its isoprenoid modification, similar to other Rab proteins. Finally, a triacylglycerol (TAG) lipase in Arabidopsis thaliana, SDP1, can transit to droplets from peroxisomes via a retromer complex (previously known to transport proteins from endosomes to the trans-Golgi network) during seed development (Thazar-Poulot et al, 2015). Bridges between the ER and droplets should allow transfer of phospholipid and neutral lipids between these two compartments.…”

“…Trafficking depended on the retromer complex; mutants of retromer subunits resulted in altered droplet morphology (Thazar-Poulot et al, 2015).…”