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

Murakawa M, Shimojima M, Shimomura Y, Kobayashi K, Awai K, Ohta H - Front Plant Sci (2014)

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Graduate School of Biological Sciences, Tokyo Institute of Technology Yokohama, Japan.

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.

No MeSH data available.


Related in: MedlinePlus

Cell cycle–related gene (A) and trehalose-6-phosphate (T6P)-metabolism-related gene (B) expression in WT and OE7 seedlings. Plants grown on MS agar with +suc or −suc for 7 d were then were transferred to ½MS agar with or without sucrose, respectively, for another 7 d. Relative mRNA abundance of cell cycle–related genes (CYCD2;1, CYCD3, CDKB2, CDKA1) and of T6P-metabolism-related genes (TPS5, TPS1, TPPB, ALIN11) in shoots were analyzed by quantitative RT-PCR. Relative expression was normalized to the corresponding mRNA abundance in WT. Values represent the mean ± SD from three independent measurements.
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Figure 7: Cell cycle–related gene (A) and trehalose-6-phosphate (T6P)-metabolism-related gene (B) expression in WT and OE7 seedlings. Plants grown on MS agar with +suc or −suc for 7 d were then were transferred to ½MS agar with or without sucrose, respectively, for another 7 d. Relative mRNA abundance of cell cycle–related genes (CYCD2;1, CYCD3, CDKB2, CDKA1) and of T6P-metabolism-related genes (TPS5, TPS1, TPPB, ALIN11) in shoots were analyzed by quantitative RT-PCR. Relative expression was normalized to the corresponding mRNA abundance in WT. Values represent the mean ± SD from three independent measurements.

Mentions: We observed enhanced growth of OE7 plants only when sucrose was supplied in the growth medium (Figure 4A). Sucrose is a major mobile form of photoassimilates, but there were no significant differences in photosynthetic activity between WT and OE7 (Table 1). Thus, we also analyzed expression levels of genes involved in cell cycle and trehalose-6-phposphate metabolism (Figure 7). Trehalose-6-phosphate metabolism and its content in plants are known to be related to growth enhancement under sucrose-supplemented conditions (Zhang et al., 2009; Debast et al., 2011; Delatte et al., 2011; Martínez-Barajas et al., 2011). However, expression levels of genes were comparable between WT and OE7 (Figures 7A,B). Thus, to clarify whether the growth difference was due to the uptake efficiency of the exogenously supplied sucrose, we first measured the sucrose concentration in shoots and roots of WT and OE7 in the absence or presence of sucrose (Figure 8). In both shoots and roots, the sucrose concentration in plants grown without exogenous sucrose was comparable between WT and OE7 (Figure 8). When sucrose was supplied, its concentration—especially in shoots—of WT and OE7 was higher than that in plants grown without sucrose (Figure 8A). In shoots of OE7 and WT grown with sucrose, sucrose concentration was 1.7- and 2.2-fold higher, respectively, compared with OE7 and WT grown without sucrose (Figure 8A). As a result, the sucrose concentration in shoots of OE7 was ~26% lower than that of WT only under sucrose supplementation. Sucrose supplementation did not significantly affect the sucrose content in roots (Figure 8B).


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

Murakawa M, Shimojima M, Shimomura Y, Kobayashi K, Awai K, Ohta H - Front Plant Sci (2014)

Cell cycle–related gene (A) and trehalose-6-phosphate (T6P)-metabolism-related gene (B) expression in WT and OE7 seedlings. Plants grown on MS agar with +suc or −suc for 7 d were then were transferred to ½MS agar with or without sucrose, respectively, for another 7 d. Relative mRNA abundance of cell cycle–related genes (CYCD2;1, CYCD3, CDKB2, CDKA1) and of T6P-metabolism-related genes (TPS5, TPS1, TPPB, ALIN11) in shoots were analyzed by quantitative RT-PCR. Relative expression was normalized to the corresponding mRNA abundance in WT. Values represent the mean ± SD from three independent measurements.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4066442&req=5

Figure 7: Cell cycle–related gene (A) and trehalose-6-phosphate (T6P)-metabolism-related gene (B) expression in WT and OE7 seedlings. Plants grown on MS agar with +suc or −suc for 7 d were then were transferred to ½MS agar with or without sucrose, respectively, for another 7 d. Relative mRNA abundance of cell cycle–related genes (CYCD2;1, CYCD3, CDKB2, CDKA1) and of T6P-metabolism-related genes (TPS5, TPS1, TPPB, ALIN11) in shoots were analyzed by quantitative RT-PCR. Relative expression was normalized to the corresponding mRNA abundance in WT. Values represent the mean ± SD from three independent measurements.
Mentions: We observed enhanced growth of OE7 plants only when sucrose was supplied in the growth medium (Figure 4A). Sucrose is a major mobile form of photoassimilates, but there were no significant differences in photosynthetic activity between WT and OE7 (Table 1). Thus, we also analyzed expression levels of genes involved in cell cycle and trehalose-6-phposphate metabolism (Figure 7). Trehalose-6-phosphate metabolism and its content in plants are known to be related to growth enhancement under sucrose-supplemented conditions (Zhang et al., 2009; Debast et al., 2011; Delatte et al., 2011; Martínez-Barajas et al., 2011). However, expression levels of genes were comparable between WT and OE7 (Figures 7A,B). Thus, to clarify whether the growth difference was due to the uptake efficiency of the exogenously supplied sucrose, we first measured the sucrose concentration in shoots and roots of WT and OE7 in the absence or presence of sucrose (Figure 8). In both shoots and roots, the sucrose concentration in plants grown without exogenous sucrose was comparable between WT and OE7 (Figure 8). When sucrose was supplied, its concentration—especially in shoots—of WT and OE7 was higher than that in plants grown without sucrose (Figure 8A). In shoots of OE7 and WT grown with sucrose, sucrose concentration was 1.7- and 2.2-fold higher, respectively, compared with OE7 and WT grown without sucrose (Figure 8A). As a result, the sucrose concentration in shoots of OE7 was ~26% lower than that of WT only under sucrose supplementation. Sucrose supplementation did not significantly affect the sucrose content in roots (Figure 8B).

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Graduate School of Biological Sciences, Tokyo Institute of Technology Yokohama, Japan.

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.

No MeSH data available.


Related in: MedlinePlus