The Galactolipid Digalactosyldiacylglycerol Accumulates in the Peribacteroid Membrane of Nitrogen-fixing Nodules of Soybean and Lotus

Abstract

The peribacteroid membrane (PBM) surrounding nitrogen fixing rhizobia in the nodules of legumes is crucial for the exchange of ammonium and nutrients between the bacteria and the host cell. Digalactosyldiacylglycerol (DGDG), a galactolipid abundant in chloroplasts, was detected in the PBM of soybean (Glycine max) and Lotus japonicus. Analyses of membrane marker proteins and of fatty acid composition confirmed that DGDG represents an authentic PBM lipid of plant origin and is not derived from the bacteria or from plastid contamination. In Arabidopsis, DGDG is known to accumulate in extraplastidic membranes during phosphate deprivation. However, the presence of DGDG in soybean PBM was not restricted to phosphate limiting conditions. Complementary DNA sequences corresponding to the two DGDG synthases, DGD1 and DGD2 from Arabidopsis, were isolated from soybean and Lotus. The two genes were expressed during later stages of nodule development in infected cells and in cortical tissue. Because nodule development depends on the presence of high amounts of phosphate in the growth medium, the accumulation of the non-phosphorus galactolipid DGDG in the PBM might be important to save phosphate for other essential processes, i.e. nucleic acid synthesis in bacteroids and host cells.

Three Enzyme Systems for Galactoglycerolipid Biosynthesis Are Coordinately Regulated in Plants

“…The presence of small amounts of galactoglycerolipids in the plasma membrane or the tonoplast (vacuolar membrane) has been described previously (39 -41), and recent reexamination of this issue has now firmly established that phosphate deprivation induces the accumulation of DGDG in plasma membranes (42)(43)(44), possibly to substitute for bilayer-forming phospholipids (4,45). Moreover, DGDG has been found in the peribacteroid membrane of legume root nodules (46), and it is also a major glycolipid of non-photosynthetic floral organs in petunia (47). Analysis of MGD2/3 and DGD2 mRNA abundance showed that the expression of these genes is strongly induced by phosphate deprivation and is generally higher in non-photosynthetic tissues with high levels of DGDG in extraplastidic membranes (15,26,33,46).…”

“…Moreover, DGDG has been found in the peribacteroid membrane of legume root nodules (46), and it is also a major glycolipid of non-photosynthetic floral organs in petunia (47). Analysis of MGD2/3 and DGD2 mRNA abundance showed that the expression of these genes is strongly induced by phosphate deprivation and is generally higher in non-photosynthetic tissues with high levels of DGDG in extraplastidic membranes (15,26,33,46). Unlike the phosphate-deprived dgd1 mutant (29), the dgd2 mutant is unable to produce a phosphate stress-induced DGDG molecular species, suggesting that DGD2 is responsible for the biosynthesis of this phosphate stress-specific DGDG pool (28).…”

The Sulfate Transporter SST1 Is Crucial for Symbiotic Nitrogen Fixation in Lotus japonicus Root Nodules

“…For instance, the concentration of protein in legume nodules is more than 30 times higher than in the roots, whereas phosphate and fatty acid concentrations are between three and four times higher in nodules than in roots (Gaude et al, 2004). Much of the phosphate of nodule cells is presumably invested in rRNA to support the high rates of protein synthesis and metabolic activity in this organ.…”

“…Much of the phosphate of nodule cells is presumably invested in rRNA to support the high rates of protein synthesis and metabolic activity in this organ. Interestingly, more than half of the protein and approximately one-third of the phosphate of nodules are present in the bacteroids (Gaude et al, 2004). Essentially all of the inorganic and organic building blocks for nodule development are imported from other organs.…”

Live-Cell Imaging Reveals Periarbuscular Membrane Domains and Organelle Location in Medicago truncatula Roots during Arbuscular Mycorrhizal Symbiosis

“…has not been reported, in the symbiosis between M. truncatula and Rhizobium bacteria, peribacteroid membranes surrounding symbiotic bacteria can be purified and their lipid and protein compositions have been analyzed. Such studies have shown that the peribacteroid membrane has a higher concentration of galactolipids than the plasma membrane (Gaude et al, 2004) and also a number of proteins involved in transport and secretion, including a syntaxin, MtSyp132, and a putative GPI-anchored protein, MtEnod16 (Catalano et al, 2004(Catalano et al, , 2007.…”