Evolution, biosynthesis and protective roles of oligogalactolipids: Key molecules for terrestrial photosynthesis?

Galactolipids (GLs) are the main lipids in chloroplast membranes and by default are also the most abundant polar lipids on earth. GLs with one or two galactose residues, monogalactosyldiacylglycerol (MGDG) and digalactosyldiacylglycerol (DGDG), are ubiquitous and essential for photosynthesis. GLs with a headgroup formed by three to five galactoses, the so-called oligogalactolipids (OGLs), are only detected in some taxa, organs and environmental conditions. OGLs can be synthesized by two metabolic pathways: successive galactosylation by DGDG synthase (DGD) or transgalactosylation from MGDG by the GL:GL galactosyltransferase (GGGT/SFR2). While the first route appeared early in the evolution (cyanobacteria), the second evolved associated to the process of terrestrialization in the streptophytes. Both routes also differ on the anomeric type of glycosidic linkages formed: alpha-type in DGD and beta-type in GGGT/SFR2. Despite functional differences between both configurations, the anomeric analysis of OGLs allows tracking their biosynthetic origin. While alpha-OGLs are constitutive and present in some algae and non-vegetative organs of vascular plants, beta-OGLs are typically stress inducible in photosynthetic tissues. Land colonization by plants involved new challenges, such as the risk of dehydration, which required developing biochemical and physiological strategies to stabilize chloroplast membranes and safeguard their functioning. Based on the integrated assessment of data available we propose that the appearance of OGLs was one of those adaptations that simultaneously could have provided advantages against other environmental constraints such as freezing.