Why are these lipids so commonly abundant in photosynthetic organisms?
|A model for evolution of higher plant galactolipid synthase.
Galactoglycerolipids, namely monogalactosyldiacylglycerol (MGDG) and digalactosyldiacylglycerol (DGDG), are commonly abundant in photosynthetic organisms, particularly in oxygen-evolving photosynthetic organisms such as cyanobacteria, algae and higher plants (1). Because these lipids are major components in their photosynthetic membranes, they have long been regarded to have important functions in their cells. Indeed, their necessity in photosynthesis, chloroplast development and embryogenesis has been shown in model plant Arabidopsis (2). Higher plant chloroplasts are thought to be acquired by endosymbiosis of an ancient cyanobacterium. In fact, membrane lipid compositions of cyanobacteria and chloroplasts greatly resemble each other. One could easily imagine that biosynthetic machineries of these membrane lipids in chloroplasts also have been derived from the endosymbiont cyanobacterium. But unexpectedly, the plant type of MGDG synthase gene has never been found in cyanobacterial genomes determined so far (3). Unlike plant cells, MGDG is synthesized by a two-step pathway in cyanobacteria. More specifically, monoglucosyldiacylglycerol (MGlcDG) is primarily synthesized by MGlcDG synthase, and then the glucolipid is further epimerized to MGDG by an unknown epimerase (4, 5). This MGlcDG synthase belongs to glycosyltransferase gene family GT2, whereas higher plant MGDG synthase is GT28.
We recently revealed that higher plant MGDG synthase has been derived from filamentous anoxygenic phototroph Chloroflexi independently of the early endosymbiotic event of chloroplasts (3, see figure). MGDG was suggested to have an important role in a large light-harvesting complex chlorosome in some anoxygenic photosynthetic bacteria. Chlorosomes are self-assembled supramolecular bacteriochlorophyll aggregates covered with a single-layer membrane (6). The requirement of the MGDG for another anoxygenic phototroph recently was proved in the green sulfur bacterium Chlorobaculum tepidum (7). MgdA was identified as a MGDG synthase gene in that bacterium. However, only the heterozygous mutants of the gene could be isolated. The mutant analysis revealed that MGDG has an important role in the chlorosome assembly. Interestingly, C. tepidum MgdA encodes a galactolipid synthase belonging to the GT1 family, which is largely distinct from those in Chloroflexi and higher plants. These findings indicate that galactolipids are commonly important in all photosynthetic organisms, but nevertheless their biosynthetic machineries have been established independently in each photosynthetic organism.
Galactolipids not only provide building blocks of photosynthetic membranes but also function as essential components in the photosynthetic reaction center complexes (8). Another interesting feature of galactolipids is their role in membrane lipid remodeling, in which galactolipids replace phospholipids under phosphate-starved circumstances (1). Upon phosphate shortage, higher plants globally degrade phospholipids in both plastidic and extraplastidic membranes, including plasma and mitochondrial membranes. Nonspecific phospholipase C (9) and soluble phosphatases (10) are known to be involved in the phospholipid degradation and to provide phosphates sufficient for plant survival. Instead, a galactolipid DGDG is supplied as a substitute of the membrane phospholipids (11).
Higher plants acquired this type of galactolipid synthesis on the surface of the outer envelope almost 320 million years ago (in the Carboniferous period), just after Spermatophyta (seed plants) emerged (3, figure). The outer-envelope MGDG synthase (Type B) mainly supplies MGDG as a precursor for the DGDG synthesis, particularly under phosphate-starved conditions (12). This function is different from inner envelope MGDG synthase (Type A), which is crucial for the synthesis of bulk membrane galactolipids in chloroplasts (2).
We hypothesize that the acquisition of another galactolipid synthetic pathway in the outer envelope may have been one of the critical developments for the current prosperity of seed plants, because nutrient shortages might have become more common after the landing of plants. As described above, photosynthetic membranes are mainly composed of glycolipids except for about 10 percent of phosphatidylglycerol. This may have saved excess usage of phosphorus-containing lipids in the ancient ocean before the landing of plants and brought about an explosive increase in photosynthetic organisms on Earth. Seed plants have acquired another advantage to become larger in size by using galactolipids even outside the chloroplasts, because phosphorus is one of the major minerals in cell components.
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Hiroyuki Ohta (email@example.com) is a professor at the Center for Biological Resources and Informatics at the Tokyo Institute of Technology.
Yuichi Yuzawa (firstname.lastname@example.org) is a former Ph.D. student at the Faculty of Bioscience and Biotechnology at the Tokyo Institute of Technology who moved to Fuji Oil Co. Ltd. as a researcher.
Mie Shimojima (email@example.com) is an assistant professor at the Center for Biological Resources and Informatics at the Tokyo Institute of Technology.