Lipid droplets are versatile organelles involved in plant development and plant response to environmental changes

Abstract

Since decades plant lipid droplets (LDs) are described as storage organelles accumulated in seeds to provide energy for seedling growth after germination. Indeed, LDs are the site of accumulation for neutral lipids, predominantly triacylglycerols (TAGs), one of the most energy-dense molecules, and sterol esters. Such organelles are present in the whole plant kingdom, from microalgae to perennial trees, and can probably be found in all plant tissues. Several studies over the past decade have revealed that LDs are not merely simple energy storage compartments, but also dynamic structures involved in diverse cellular processes like membrane remodeling, regulation of energy homeostasis and stress responses. In this review, we aim to highlight the functions of LDs in plant development and response to environmental changes. In particular, we tackle the fate and roles of LDs during the plant post-stress recovery phase.

Keywords: autophagy; environmental stress; heat; lipid droplets; lipolysis; membrane remodeling; post-stress recovery; triacylglycerol.

Figure 1

Repartition and function of lipid droplets in different plant tissues. Depending on developmental stage and physiological state of the plant, lipid droplets (LDs) can be present either in seeds or vegetative tissues such as roots, leaves, dormant buds and pollen grains. Top left: cell of Arabidopsis seed stained with BODIPY, a LD-specific dye, and observed by confocal microcopy; center: Arabidopsis pollen grain filled with LDs (in black), observed by electron microscopy; top right: picture of dormant sweet cherry (Prunus avium) floral bud by electron microscopy; bottom left: cell of Arabidopsis leaf after five days of nitrogen starvation showing two LDs in contact with chloroplast, observed by electron microscopy; bottom right: LDs in Arabidopsis root tip labelled in green by overexpression of LDAP1-YFP, after two days of nitrogen starvation, observed by confocal microscopy. This figure was created at BioRender.com.

Figure 2

Schematic representation of LD life cycle and potential remobilization pathways. Biosynthesis of fatty acids (FAs) takes place in the chloroplast. Biosynthesis of plastidial galactolipids (MGDG, monogalactosyldiacylglycerol and DGDG, digalactosyldiacylglycerol) occuring within the chloroplast is termed the chloroplastic or ‘‘prokaryotic “ pathway, and the one in the endoplasmic reticulum (ER), that involves phospholipid synthesis (PA, phosphatidic acid; PC, phosphatidylcholine) and subsequent transfer to the chloroplast constitutes the endoplasmic or “ eukaryotic “ pathway. When exported to the cytosol, free FAs are first transported by FA EXPORT 1 protein (FAX1) accross the inner membrane and then converted to activated acyl-CoA by the LONG ACYL-COA SYNTHETASE 9 (LACS9). Acyl-coA are transported to the ER for TAG (triacylglycerol) and SE (sterol ester) assemblies. The major pathway for TAG synthesis is the Kennedy pathway. Diacylglycerol (DAG) is the direct precursor for TAG synthesis. DAG can be converted to TAG by DGAT (DIACYLGLYCEROL ACYLTRANSFERASE) or PDAT (PHOSPHOLIPID DIACYGLYCEROL ACYLTRANSFERASE), using acyl-CoA or PC as acyl donor, respectively. SEs are synthetized from free sterols by the enzymes PSAT (PHOSPHOLIPID STEROL ACYLTRANSFERASE) or ASAT (ACYL-COA STEROL ACYLTRANSFERASE). TAGs and SEs accumulate between the two leaflets of the ER, leading to the formation of a lens-like structure and the budding of a new lipid droplet (LD). Lipolysis and lipophagy are the two main pathways for LD remobilization. Lipolysis involves lipases like SDP1 (SUGAR DEPENDENT PROTEIN 1). PXA1 is a peroxisomal transporter required for uptake of FAs from LD to peroxisome for β-oxidation. Two distinct pathways of lipophagy may be at play: microlipophagy and macrolipophagy. Microphagy involves the invagination of tonoplast to trap LDs within the vacuole. Macrophagy involves the formation of double membrane vesicles called autophagosomes that will sequester LDs and bring them to vacuole for degradation. Both microlipophagy and macrolipophagy involve autophagy related preteins (ATG). TAGs within LDs could also be a source of FAs for lipid membrane remodeling thanks to enzymes that remain to be identified and through organelle contacts maintained by tethering proteins such as SLDP (SEED LD PROTEIN) and LIPA (LD-PLASMA MEMBRANE ADAPTATOR) at LD-plasma membrane connections. This figure was created at BioRender.com.