Phosphate deprivation induces transfer of DGDG galactolipid from chloroplast to mitochondria

Abstract

In many soils plants have to grow in a shortage of phosphate, leading to development of phosphate-saving mechanisms. At the cellular level, these mechanisms include conversion of phospholipids into glycolipids, mainly digalactosyldiacylglycerol (DGDG). The lipid changes are not restricted to plastid membranes where DGDG is synthesized and resides under normal conditions. In plant cells deprived of phosphate, mitochondria contain a high concentration of DGDG, whereas mitochondria have no glycolipids in control cells. Mitochondria do not synthesize this pool of DGDG, which structure is shown to be characteristic of a DGD type enzyme present in plastid envelope. The transfer of DGDG between plastid and mitochondria is investigated and detected between mitochondria-closely associated envelope vesicles and mitochondria. This transfer does not apparently involve the endomembrane system and would rather be dependent upon contacts between plastids and mitochondria. Contacts sites are favored at early stages of phosphate deprivation when DGDG cell content is just starting to respond to phosphate deprivation.

Glycerolipid transfer for the building of membranes in plant cells

“…Under phosphate deprivation, DGDG formation is stimulated corresponding to activation or stimulation of a part of the galactolipid synthesis pathway indicated in red [42; 6; 9]. Under these conditions, DGDG is transferred through membrane contact between chloroplast and mitochondria [9]. …”

“…By contrast with vesicular trafficking, transfer by contact does not involve a transfer of a portion of a bilayer as such but a selective transfer of some components of the membrane. In plants, some indications of a lipid transfer by membrane contact between plastid envelope and mitochondria were recently reported [9].…”

“…Upon phosphate deprivation, DGDG, a specific plastid lipid in standard conditions, was found in the plasma membrane [7,8], a membranous compartment disconnected from plastid membranes, but dynamically connected to the overall endomembrane system. Moreover, several lines of evidence have 6 shown that large amounts of DGDG are also present in mitochondria upon phosphate deprivation [9].…”

The Phosphate Fast-Responsive Genes PECP1 and PPsPase1 Affect Phosphocholine and Phosphoethanolamine Content

“…Many enzymes involved in this process are well known, and independent pathways are concomitantly triggered to ensure a fast and sizable lipid remobilization (Nakamura, 2013;Pant et al, 2015). For instance, SQD1 and SQD2 are involved in sulfolipid biosynthesis, whereas MGD2 and MGD3 are strongly induced to increase galactolipid content (Yu et al, 2002;Jouhet et al, 2004;Nakamura et al, 2005;Kobayashi et al, 2009). To achieve these substitutions, phospholipids are degraded by different types of lipases, resulting in the release of lipid subcomponents that can reenter the metabolism or be converted into other lipid forms (Nakamura, 2013).…”

Role of phosphatidic acid in plant galactolipid synthesis

“…At an early stage of Pi deprivation a transient increase of PLDz2-enriched domains has been observed in tonoplast [63]. These domains are close to mitochondria and chloroplasts whose contacts are themselves increased at this stage and concomitant with galactolipid transfer from chloroplasts to mitochondria [19,64]. On the model of what has been observed in mammal cells, one can propose that PLDz2-produced PA can facilitate hemifusion of membranes and eventually remodelling of lipids between tonoplast, chloroplasts and mitochondria.…”