Do Galactolipid Synthases Play a Key Role in the Biogenesis of Chloroplast Membranes of Higher Plants?

Abstract

A unique feature of chloroplasts is their high content of the galactolipids monogalactosyldiacylglycerol (MGDG) and digalactosyldiacylglycerol (DGDG), which constitute up to 80% of their lipids. These galactolipids are synthesized in the chloroplast envelope membrane through the concerted action of galactosyltransferases, the so-called 'MGDG synthases (MGDs)' and 'DGDG synthases (DGDs),' which use uridine diphosphate (UDP)-galactose as donor. In Arabidopsis leaves, under standard conditions, the enzymes MGD1 and DGD1 provide the bulk of galactolipids, necessary for the massive expansion of thylakoid membranes. Under phosphate limited conditions, plants activate another pathway involving MGD2/MGD3 and DGD2 to provide additional DGDG that is exported to extraplastidial membranes where they partly replace phospholipids, a phosphate-saving mechanism in plants. A third enzyme system, which relies on the UDP-Gal-independent GGGT (also called SFR2 for SENSITIVE TO FREEZING 2), can be activated in response to a freezing stress. The biosynthesis of galactolipids by these multiple enzyme sets must be tightly regulated to meet the cellular demand in response to changing environmental conditions. The cooperation between MGD and DGD enzymes with a possible substrate channeling from diacylglycerol to MGDG and DGDG is supported by biochemical and biophysical studies and mutant analyses reviewed herein. The fine-tuning of MGDG to DGDG ratio, which allows the reversible transition from the hexagonal II to lamellar α phase of the lipid bilayer, could be a key factor in thylakoid biogenesis.

Keywords: Arabidopsis; DGDG; MGDG; biosynthesis; chloroplast; galactolipids.

FIGURE 1

Structures of the conserved quartet of lipids and their abundance (expressed in mol%) in chloroplast membranes. The small polar head of MGDG resembles a truncated cone, which induces a negative curvature favoring its organization into inverted micelles (HII phase). DGDG, SQDG, and PG form lamellar phases. THY, thylakoids; IEM, inner envelope membrane; OEM, outer envelope membrane. ^aFrom Block et al., 1983.

FIGURE 2

Biosynthesis of galactolipids in the chloroplast envelope membranes in Arabidopsis. The three enzyme systems are represented. The main pathway is mediated by MGD1 and DGD1 which provide the bulk of galactolipids for all chloroplast membranes in normal growth conditions. MGD2/3 and DGD2 are activated in response to Pi deprivation, and SFR2 is activated in response to a freezing stress. Flux of galactolipids between IEM and OEM are facilitated by PA-mediated contacts with N-DGD1 (as proposed by Kelly et al., 2016). The MGD1-MGDG association in the IEM forms a HII platform that allows the transit of galactolipids to newly synthesized thylakoids through a non-lamellar/non-vesicular process (as proposed by Bastien et al., 2016). This process might involve other cellular partners such as the IM30/VIPP1 protein (Hennig et al., 2015). Can MGD1, inserted in a locally non-lamellar microdomain, have access on one side or the other side of the IEM, or even both, has yet to be determined.