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Characterisation of Lipid Changes in Ethylene-Promoted Senescence and Its Retardation by Suppression of Phospholipase Dδ in Arabidopsis Leaves.

Jia Y, Li W - Front Plant Sci (2015)

Bottom Line: Lipid profiling revealed that ethylene caused a decrease in all lipids levels, except phosphatidic acid (PA), caused increases in the ratios of digalactosyl diglyceride/monogalactosyl diglyceride (MGDG) and phosphatidylcholine (PC)/phosphatidylethanolamine (PE), and caused degradation of plastidic lipids before that of extraplastidic lipids in wild-type plants.The accelerated degradation of plastidic lipids during ethylene-promoted senescence in wild-type plants was attenuated in PLDδ-KO plants.The integrity of the cell membrane in PLDδ-KO plants facilitated maintenance of the membrane function and of the proteins associated with the membrane.

View Article: PubMed Central - PubMed

Affiliation: Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences Kunming, China.

ABSTRACT
Ethylene and abscisic acid (ABA) both accelerate senescence of detached Arabidopsis leaves. We previously showed that suppression of Phospholipase Dδ (PLDδ) retarded ABA-promoted senescence. Here, we report that ethylene-promoted senescence is retarded in detached leaves lacking PLDδ. We further used lipidomics to comparatively profile the molecular species of membrane lipids between wild-type and PLDδ-knockout (PLDδ-KO) Arabidopsis during ethylene-promoted senescence. Lipid profiling revealed that ethylene caused a decrease in all lipids levels, except phosphatidic acid (PA), caused increases in the ratios of digalactosyl diglyceride/monogalactosyl diglyceride (MGDG) and phosphatidylcholine (PC)/phosphatidylethanolamine (PE), and caused degradation of plastidic lipids before that of extraplastidic lipids in wild-type plants. The accelerated degradation of plastidic lipids during ethylene-promoted senescence in wild-type plants was attenuated in PLDδ-KO plants. No obvious differences in substrate and product of PLDδ-catalyzed phospholipid hydrolysis were detected between wild-type and PLDδ-KO plants, which indicated that the retardation of ethylene-promoted senescence by suppressing PLDδ might not be related to the role of PLDδ in catalyzing phospholipid degradation. In contrast, higher plastidic lipid content, especially of MGDG, in PLDδ-KO plants was crucial for maintaining photosynthetic activity. The lower relative content of PA and higher PC/PE ratio in PLDδ-KO plants might contribute to maintaining cell membrane integrity. The integrity of the cell membrane in PLDδ-KO plants facilitated maintenance of the membrane function and of the proteins associated with the membrane. Taking these findings together, higher plastidic lipid content and the integrity of the cell membrane in PLDδ-KO plants might contribute to the retardation of ethylene-promoted senescence by the suppression of PLDδ.

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Changes in the molecular species of PA in WS and PLDδ-KO plants during ethylene-promoted senescence. “∗” indicates that the value is significantly different from that of the WS under the same conditions (p < 0.05). Values are means ± SD (n = 4 or 5).
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Figure 3: Changes in the molecular species of PA in WS and PLDδ-KO plants during ethylene-promoted senescence. “∗” indicates that the value is significantly different from that of the WS under the same conditions (p < 0.05). Values are means ± SD (n = 4 or 5).

Mentions: To investigate how PLDδ functions in ethylene-promoted senescence, we analyzed the changes in the absolute level and relative content of PA under ethylene treatment in the two genotypes plants leaves. During ethylene-promoted senescence, no significant changes were detected in absolute levels of PA in either WS or PLDδ-KO plants. Upon analysis of the relative content of membrane lipids, we found that the relative content of PA increased 3.5-fold (from 0.02 to 0.07%) in WS plants, but remained unchanged in PLDδ-KO plants, which resulted in the relative content of PA in WS being much higher than that in PLDδ-KO plants after ethylene treatment for 5 days, especially for the molecular species PA 34:3, 36:3, and 36:6 (Tables 1 and 3; Figure 3). PA is a non-bilayer lipid and a potent promoter of the formation of the hexagonal phase and destabilization of the plasma membrane. For further assessment of the cell membrane stabilization of Arabidopsis during ethylene-promoted senescence, we calculated the PC/PE ratio in this process. This ratio in WS plants increased from 1.61 (NS) to 2.11 (leaves treated with ethylene for 3 days), and then decreased to the initial level of 1.73 (leaves treated with ethylene for 5 days). The PC/PE ratio in PLDδ-KO leaves increased constantly in the course of ethylene-promoted senescence, from 1.66 (NS) to 2.39 (leaves treated with ethylene for 5 days). In addition, the ratio of PC/PE in PLDδ-KO detached leaves was much higher than that in WS leaves after ethylene treatment for 5 days, namely, 2.39 and 1.73, respectively (Table 4). Our results indicate that the increase in the relative content of PA promoted destabilization of the plasma membrane; this may have led to the loss of membrane integrity and functions of membrane-associated proteins, thereby promoting senescence. Therefore, a reduction in the relative content of PA in PLDδ-KO leaves may have accounted for the higher ratio of PC/PE, which may have helped to maintain plasma membrane integrity and normal membrane protein function that eventually resulted in the retardation of ethylene-promoted senescence.


Characterisation of Lipid Changes in Ethylene-Promoted Senescence and Its Retardation by Suppression of Phospholipase Dδ in Arabidopsis Leaves.

Jia Y, Li W - Front Plant Sci (2015)

Changes in the molecular species of PA in WS and PLDδ-KO plants during ethylene-promoted senescence. “∗” indicates that the value is significantly different from that of the WS under the same conditions (p < 0.05). Values are means ± SD (n = 4 or 5).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4663248&req=5

Figure 3: Changes in the molecular species of PA in WS and PLDδ-KO plants during ethylene-promoted senescence. “∗” indicates that the value is significantly different from that of the WS under the same conditions (p < 0.05). Values are means ± SD (n = 4 or 5).
Mentions: To investigate how PLDδ functions in ethylene-promoted senescence, we analyzed the changes in the absolute level and relative content of PA under ethylene treatment in the two genotypes plants leaves. During ethylene-promoted senescence, no significant changes were detected in absolute levels of PA in either WS or PLDδ-KO plants. Upon analysis of the relative content of membrane lipids, we found that the relative content of PA increased 3.5-fold (from 0.02 to 0.07%) in WS plants, but remained unchanged in PLDδ-KO plants, which resulted in the relative content of PA in WS being much higher than that in PLDδ-KO plants after ethylene treatment for 5 days, especially for the molecular species PA 34:3, 36:3, and 36:6 (Tables 1 and 3; Figure 3). PA is a non-bilayer lipid and a potent promoter of the formation of the hexagonal phase and destabilization of the plasma membrane. For further assessment of the cell membrane stabilization of Arabidopsis during ethylene-promoted senescence, we calculated the PC/PE ratio in this process. This ratio in WS plants increased from 1.61 (NS) to 2.11 (leaves treated with ethylene for 3 days), and then decreased to the initial level of 1.73 (leaves treated with ethylene for 5 days). The PC/PE ratio in PLDδ-KO leaves increased constantly in the course of ethylene-promoted senescence, from 1.66 (NS) to 2.39 (leaves treated with ethylene for 5 days). In addition, the ratio of PC/PE in PLDδ-KO detached leaves was much higher than that in WS leaves after ethylene treatment for 5 days, namely, 2.39 and 1.73, respectively (Table 4). Our results indicate that the increase in the relative content of PA promoted destabilization of the plasma membrane; this may have led to the loss of membrane integrity and functions of membrane-associated proteins, thereby promoting senescence. Therefore, a reduction in the relative content of PA in PLDδ-KO leaves may have accounted for the higher ratio of PC/PE, which may have helped to maintain plasma membrane integrity and normal membrane protein function that eventually resulted in the retardation of ethylene-promoted senescence.

Bottom Line: Lipid profiling revealed that ethylene caused a decrease in all lipids levels, except phosphatidic acid (PA), caused increases in the ratios of digalactosyl diglyceride/monogalactosyl diglyceride (MGDG) and phosphatidylcholine (PC)/phosphatidylethanolamine (PE), and caused degradation of plastidic lipids before that of extraplastidic lipids in wild-type plants.The accelerated degradation of plastidic lipids during ethylene-promoted senescence in wild-type plants was attenuated in PLDδ-KO plants.The integrity of the cell membrane in PLDδ-KO plants facilitated maintenance of the membrane function and of the proteins associated with the membrane.

View Article: PubMed Central - PubMed

Affiliation: Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences Kunming, China.

ABSTRACT
Ethylene and abscisic acid (ABA) both accelerate senescence of detached Arabidopsis leaves. We previously showed that suppression of Phospholipase Dδ (PLDδ) retarded ABA-promoted senescence. Here, we report that ethylene-promoted senescence is retarded in detached leaves lacking PLDδ. We further used lipidomics to comparatively profile the molecular species of membrane lipids between wild-type and PLDδ-knockout (PLDδ-KO) Arabidopsis during ethylene-promoted senescence. Lipid profiling revealed that ethylene caused a decrease in all lipids levels, except phosphatidic acid (PA), caused increases in the ratios of digalactosyl diglyceride/monogalactosyl diglyceride (MGDG) and phosphatidylcholine (PC)/phosphatidylethanolamine (PE), and caused degradation of plastidic lipids before that of extraplastidic lipids in wild-type plants. The accelerated degradation of plastidic lipids during ethylene-promoted senescence in wild-type plants was attenuated in PLDδ-KO plants. No obvious differences in substrate and product of PLDδ-catalyzed phospholipid hydrolysis were detected between wild-type and PLDδ-KO plants, which indicated that the retardation of ethylene-promoted senescence by suppressing PLDδ might not be related to the role of PLDδ in catalyzing phospholipid degradation. In contrast, higher plastidic lipid content, especially of MGDG, in PLDδ-KO plants was crucial for maintaining photosynthetic activity. The lower relative content of PA and higher PC/PE ratio in PLDδ-KO plants might contribute to maintaining cell membrane integrity. The integrity of the cell membrane in PLDδ-KO plants facilitated maintenance of the membrane function and of the proteins associated with the membrane. Taking these findings together, higher plastidic lipid content and the integrity of the cell membrane in PLDδ-KO plants might contribute to the retardation of ethylene-promoted senescence by the suppression of PLDδ.

No MeSH data available.


Related in: MedlinePlus