Functional differences between galactolipids and glucolipids revealed in photosynthesis of higher plants

Abstract

Galactolipids represent the most abundant lipid class in thylakoid membranes, where oxygenic photosynthesis is performed. The identification of galactolipids at specific sites within photosynthetic complexes by x-ray crystallography implies specific roles for galactolipids during photosynthetic electron transport. The preference for galactose and not for the more abundant sugar glucose in thylakoid lipids and their specific roles in photosynthesis are not understood. Introduction of a bacterial glucosyltransferase from Chloroflexus aurantiacus into the galactolipid-deficient dgd1 mutant of Arabidopsis thaliana resulted in the accumulation of a glucose-containing lipid in the thylakoids. At the same time, the growth defect of the dgd1 mutant was complemented. However, the degree of trimerization of light-harvesting complex II and the photosynthetic quantum yield of transformed dgd1 plants were only partially restored. These results indicate that specific interactions of the galactolipid head group with photosynthetic protein complexes might explain the preference for galactose in thylakoid lipids of higher plants. Therefore, galactose in thylakoid lipids can be exchanged with glucose without severe effects on growth, but the presence of galactose is crucial to maintain maximal photosynthetic efficiency.chloroplast ͉ galactose ͉ glucose ͉ lipid ͉ glucosylgalactosyldiacylglycerol D irectly or indirectly, almost all life on earth depends on the photosynthetic conversion of water, CO 2 , and sunlight into chemical energy and oxygen. In cyanobacteria, green algae, and plants, the primary reactions of oxygenic photosynthesis are executed in thylakoid membranes. They harbor a set of multimeric protein complexes embedded into a lipid matrix of unique composition. The structure of the protein complexes and the lipid composition of thylakoid membranes are highly conserved in all organisms performing oxygenic photosynthesis. Thylakoid lipids comprise the two galactolipids monogalactosyldiacylglycerol (␤GalDG) and digalactosyldiacylglycerol (␣Gal␤GalDG), a sulfolipid, and phosphatidylglycerol as the only phospholipid (1-3). Based on their high proportion in thylakoid membranes and the abundance of plants and algae, galactolipids represent the most abundant lipid class in the biosphere (4, 5). Galactolipids are crucial to establish the proton-and ion-impermeable matrix of chloroplast membranes. An appropriate ratio of ␤GalDG to ␣Gal␤GalDG is required to maintain the intricate bilayer characteristics required for insertion, folding, movement, and conformational changes of membrane proteins (6). Crystalline chlorophyll-protein complexes contain galactolipid molecules firmly bound to specific sites, some of them in close proximity to the electron transfer chain. This association implies important roles of galactolipids in photosynthetic exciton and electron transfer within and between the different complexes (7-9). Mutants and transgenic plants of Arabidopsis thaliana are the basis for our current understanding of the role of th...

Galactolipid synthesis in chloroplast inner envelope is essential for proper thylakoid biogenesis, photosynthesis, and embryogenesis

“…Another chloroplast galactolipid, DGDG, has also been found in the crystallized PSII complex and in LHCII (5,15). Analyses of a dgd1 mutant in which DGDG content is significantly depleted indicated that DGDG plays a crucial role in PSII activity and the stabilization of trimeric LHCII (16)(17)(18). The dgd1 mutant also demonstrated the importance of DGDG for the stability and activity of the PSI complex (19,20).…”

Synthesis and transfer of galactolipids in the chloroplast envelope membranes of Arabidopsis thaliana

“…The cDNAs from Arabidopsis DGD1, DGD2, and Chloroflexus GlcT (5,8,15,19,20,45,46) were cloned into E. coli expression vectors for lipid measurements and lipid binding or liposome aggregation experiments (31,47) or into binary vectors (48) for Arabidopsis transformation (SI Appendix, SI Material and Methods). The Arabidopsis dgd1-1 mutant was transformed using the Agrobacterium floraldip method (49).…”

“…Next, the relevance of NDGD1 for glycolipid production in planta was studied by introducing NDGD1 constructs or chloroplast envelope-targeting sequences of MGD1 (NM1, targeting the inner envelope) or DGD2 (ND2, a short N-terminal sequence targeting the oEM), fused to CDGD1, DGD2, or a glucosyltransferase, GlcT, from Chloroflexus aurantiacus, into dgd1-1. GlcT adds a glucose to carbon 6 of the galactose moiety of MGDG, thereby producing GlcGalDG (19). The synthesis of DGDG or GlcGalDG was monitored by TLC separation and quantification by GC (Fig.…”

Configuration of the sugar head of glycolipids in thylakoid membranes

“…This led to various defects in the mutant, especially the dwarf phenotype, mainly because of overproduction of oxylipin and lignification of the phloem cap (Lin et al, 2016). These phenomena were partially complemented by introducing Chloroflexus aurantiacus glycosyltransferase (β-GlcT) (Hölzl et al, 2006(Hölzl et al, , 2009, which synthesizes…”