Abstract
Phosphate (Pi) limitation causes drastic lipid remodeling in plant membranes. Glycolipids substitute for the phospholipids that are degraded, thereby supplying Pi needed for essential biological processes. Two major types of remodeling of membrane lipids occur in higher plants: whereas one involves an increase in the concentration of sulfoquinovosyldiacylglycerol in plastids to compensate for a decreased concentration of phosphatidylglycerol, the other involves digalactosyldiacylglycerol (DGDG) synthesis in plastids and the export of DGDG to extraplastidial membranes to compensate for reduced abundances of phospholipids. Lipid remodeling depends on an adequate supply of monogalactosyldiacylglycerol (MGDG), which is a substrate that supports the elevated rate of DGDG synthesis that is induced by low Pi availability. Regulation of MGDG synthesis has been analyzed most extensively using the model plant Arabidopsis thaliana, although orthologous genes that encode putative MGDG synthases exist in photosynthetic organisms from bacteria to higher plants. We recently hypothesized that two types of MGDG synthase diverged after the appearance of seed plants. This divergence might have both enabled plants to adapt to a wide range of Pi availability in soils and contributed to the diversity of seed plants. In the work presented here, we found that membrane lipid remodeling also takes place in sesame, which is one of the most common traditional crops grown in Asia. We identified two types of MGDG synthase from sesame (encoded by SeMGD1 and SeMGD2) and analyzed their enzymatic properties. Our results show that both genes correspond to the Arabidopsis type-A and -B isoforms of MGDG synthase. Notably, whereas Pi limitation up-regulates only the gene encoding the type-B isoform of Arabidopsis, low Pi availability up-regulates the expression of both SeMGD1 and SeMGD2. We discuss the significance of the different responses to low Pi availability in sesame and Arabidopsis.
Highlights
The regulation of galactolipid synthesis in Arabidopsis thaliana under phosphate (Pi)-limited conditions has been studied extensively
When sesame seedlings were grown under Pidepleted conditions, morphological changes in the lateral roots seemed to be more obvious than those observed in Arabidopsis (Figure 1A)
In Arabidopsis, we recently found that severe impairment of thylakoid membrane formation in mgd1-2 is only partially complemented by the synthesis of MGDG and DGDG that is induced by low availability of Pi (Kobayashi et al, 2013)
Summary
The regulation of galactolipid synthesis in Arabidopsis thaliana under phosphate (Pi)-limited conditions has been studied extensively. Under Pi-sufficient conditions, the galactolipids monogalactosyldiacylglycerol (MGDG) and digalactosyldiacylglycerol (DGDG) are found exclusively and abundantly in plastids, especially in thylakoid membranes. They are not observed in other extraplastidial membranes (Joyard et al, 1998). Under Pi-depleted conditions, synthesis of MGDG and DGDG is upregulated, and DGDG is exported from plastids to extraplastidial membranes to help maintain membrane structure after phospholipid degradation (Essigmann et al, 1998; Härtel et al., 2000; Andersson et al, 2003, 2005; Jouhet et al, 2004). DGDG can substitute for phosphatidylcholine (PC) in the membrane because DGDG and PC are both bilayer-forming lipids, whereas MGDG is not (Murphy, 1986). Regarding the substitution for non-bilayer or anionic phospholipids such as phosphatidylethanolamine and phosphatidylinositol under Pidepleted conditions, glucuronosyldiacylglycerol was suggested to play an essential role (Okazaki et al, 2013)
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