Monogalactosyldiacylglycerol synthesis in the outer envelope membrane of chloroplasts is required for enhanced growth under sucrose supplementation

Abstract

Plant galactolipid synthesis on the outer envelope membranes of chloroplasts is an important biosynthetic pathway for sustained growth under conditions of phosphate (Pi) depletion. During Pi starvation, the amount of digalactosyldiacylglycerol (DGDG) is increased to substitute for the phospholipids that are degraded for supplying Pi. An increase in DGDG concentration depends on an adequate supply of monogalactosyldiacylglycerol (MGDG), which is a substrate for DGDG synthesis and is synthesized by a type-B MGDG synthase, MGD3. Recently, sucrose was suggested to be a global regulator of plant responses to Pi starvation. Thus, we analyzed expression levels of several genes involved in lipid remodeling during Pi starvation in Arabidopsis thaliana and found that the abundance of MGD3 mRNA increased when sucrose was exogenously supplied to the growth medium. Sucrose supplementation retarded the growth of the Arabidopsis MGD3 knockout mutant mgd3 but enhanced the growth of transgenic Arabidopsis plants overexpressing MGD3 compared with wild type, indicating the involvement of MGD3 in plant growth under sucrose-replete conditions. Although most features such as chlorophyll content, photosynthetic activity, and Pi content were comparable between wild-type and the transgenic plants overexpressing MGD3, sucrose content in shoot tissues decreased and incorporation of exogenously supplied carbon to DGDG was enhanced in the MGD3-overexpressing plants compared with wild type. Our results suggest that MGD3 plays an important role in supplying DGDG as a component of extraplastidial membranes to support enhanced plant growth under conditions of carbon excess.

Tangled evolutionary processes with commonality and diversity in plastidial glycolipid synthesis in photosynthetic organisms

“…DGDG is a bilayer-forming lipid, as is PC, and is therefore able to functionally replace bulk PC. Recently, A. thaliana MGD3 was also found to be upregulated when carbon is in excess, i.e., to support enhanced growth [74]. It was also reported that expression of Type-B MGD genes are induced upon treatment of plants with hydrogen peroxide [75].…”

Photosynthetic response to increased irradiance correlates to variation in transcriptional response of lipid‐remodeling and heat‐shock genes

“…() nor Murakawa et al. () have found a link between increased irradiance, photosynthetic acclimation, and phosphate deficiency. This study implicates that increased expression of phosphate‐deficiency‐initiated lipid‐remodeling genes (for the synthesis of galactolipids) in the response to an irradiance increase is a way to provide the extra Pi needed for the up‐regulation of photosynthetic and downstream carbohydrate (sucrose) metabolism (Figures and ).…”

“…In addition, phosphate deficiency responsive genes are shown to be sugar inducible (Müller, Morant, Jarmer, Nilsson, & Hamborg Nielsen, ). This transcriptional correlation is thought to be important for either (a) maintenance of the ratio of available Pi and carbon by reducing the cellular sucrose content via galactolipid synthesis; or (b) for the supply of galactolipids as components of the plasma membrane to support enhance growth under sucrose supplementation (Murakawa et al., ). Neither Müller et al.…”

Emerging knowledge of the organelle outer membranes – research snapshots and an updated list of the chloroplast outer envelope proteins

“…Under phosphate starvation, phospholipids in the cell membranes, mainly those in extraplastidic compartments, are used as the source of free phosphates and substituted by galactolipids made in the chloroplast outer envelope. Murakawa et al ( 2014 ) have used Arabidopsis mutants and feeding assays to show that the outer-envelope-dependent galactolipid synthesis is stimulated by sucrose supplementation and this stimulation in turn enhances utilization of the added sucrose for plant growth. This work nicely illustrates the physiological significance of the metabolic activity localized in the chloroplast outer envelope for plant growth and development.…”