Lipid droplet-peroxisome connections in plants

Authors: ESNAY, NICOLAS - University Of North Texas; Dyer, John; MULLEN, ROBERT - University Of Guelph; CHAPMAN, KENT - University Of North Texas

Submitted to: Contact
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/24/2020
Publication Date: 3/2/2020
Publication URL: https://handle.nal.usda.gov/10113/6949560
Citation: Esnay, N., Dyer, J.M., Mullen, R.T., Chapman, K.D. 2020. Lipid droplet-peroxisome connections in plants. Contact. 3:1-14. https://doi.org/10.1177/2515256420908765.
DOI: https://doi.org/10.1177/2515256420908765

Interpretive Summary: Lipid droplets are subcellular organelles that store neutral lipids, or "oil", in the cytoplasm of eukaryotic cells. Once viewed as static depots of carbon and energy, they are now recognized as bona fide organelles that play important roles in plant growth, development and stress responses. In oilseeds, seed germination initiates a process whereby the oil is rapidly broken down in peroxisomes and then converted into sugars, which are transported to other parts of the plant to help fuel post-germinative seedling growth. To help make this process more efficient, lipid droplets become physically associated with peroxisomes to help maximize lipid transfer between the organelles. This review article describes the mechanisms involved in formation of these intimate inter-organellar connections, and identifies new areas of research that need to be explored to help better understand the process. This information will be most useful to scientists interested in the molecular details of oilseed development and the efficiency of oil breakdown, which directly impacts seed germination and seedling-establishment of oilseed crops.

Technical Abstract: Lipid droplets (LDs) are the principal subcellular sites for the storage of triacylglycerols (TAGs), and in plants, TAG degradation requires metabolism in peroxisomes. This metabolic cooperation includes TAG hydrolysis by the sugar-dependent 1 (SDP1) lipase located on the LD surface and the transfer of fatty acids into the peroxisome matrix by the peroxisomal membrane ABC transporter, PXA1. During seed germination this process fuels heterotrophic growth and involves the retromer-dependent formation of peroxisomal membrane extensions called ‘peroxules’ that interact with LDs. Similar changes in membrane architecture are observed also during interactions of peroxisomes and LDs in yeast and mammalian cells, despite differences in the molecular components required for their connections. Proteins directly involved in LD- peroxisome membrane contact site formation in plants have not yet been identified, but the connection between these two organelles is dependent upon PXA1, which contains a cytoplasmic exposed FFAT (phenylalanine – acidic tract) motif capable of interacting with vesicle-associated membrane protein (VAMP)-associated proteins (VAPs). The identification of several VAPs in plant LD proteomes suggests that a VAP-PXA1 connection might be part of functional tethering complex that connects these two organelles and allows for efficient transfer of lipophilic substrates from LDs to the peroxisome matrix in plant cells, similar to how VAPs participate in lipid transfer reactions between other subcellular compartments in eukaryotic systems.