Plant-Unique <i>cis</i>/<i>trans</i> Isomerism of Long-Chain Base Unsaturation is Selectively Required for Aluminum Tolerance Resulting from Glucosylceramide-Dependent Plasma Membrane Fluidity
<i>Cis</i>/<i>trans</i> isomerism of the Δ8 unsaturation of long-chain base (LCB) is found only in plant sphingolipids. This unique geometry is generated by sphingolipid LCB Δ8 desaturase SLD which produces both isomers at various ratios, resulting in divers...
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doaj-6af07c81afd147778103d236b96b53512020-11-25T02:06:56ZengMDPI AGPlants2223-77472019-12-01911910.3390/plants9010019plants9010019Plant-Unique <i>cis</i>/<i>trans</i> Isomerism of Long-Chain Base Unsaturation is Selectively Required for Aluminum Tolerance Resulting from Glucosylceramide-Dependent Plasma Membrane FluidityMasaya Sato0Minoru Nagano1Song Jin2Atsuko Miyagi3Masatoshi Yamaguchi4Maki Kawai-Yamada5Toshiki Ishikawa6Graduate School of Science and Engineering, Saitama University, Saitama 338-8570, JapanGraduate School of Life Sciences, Ritsumeikan University, Kusatsu, Shiga 525-8577, JapanGraduate School of Science and Engineering, Saitama University, Saitama 338-8570, JapanGraduate School of Science and Engineering, Saitama University, Saitama 338-8570, JapanGraduate School of Science and Engineering, Saitama University, Saitama 338-8570, JapanGraduate School of Science and Engineering, Saitama University, Saitama 338-8570, JapanGraduate School of Science and Engineering, Saitama University, Saitama 338-8570, Japan<i>Cis</i>/<i>trans</i> isomerism of the Δ8 unsaturation of long-chain base (LCB) is found only in plant sphingolipids. This unique geometry is generated by sphingolipid LCB Δ8 desaturase SLD which produces both isomers at various ratios, resulting in diverse <i>cis</i>/<i>trans</i> ratios in plants. However, the biological significance of this isomeric diversity remains controversial. Here, we show that the plant-specific <i>cis</i> unsaturation of LCB selectively contributes to glucosylceramide (GlcCer)-dependent tolerance to aluminum toxicity. We established three transgenic rice lines with altered LCB unsaturation profiles. Overexpression of SLD from rice (OsSLD-OX), which preferentially exhibits <i>cis</i>-activity, or Arabidopsis (AtSLD-OX), showing preference for <i>trans</i>-activity, facilitated Δ8 unsaturation in different manners: a slight increase of <i>cis</i>-unsaturated glycosylinositolphosphoceramide (GIPC) in OsSLD-OX, and a drastic increase of <i>trans</i>-unsaturated GlcCer and GIPC in AtSLD-OX. Disruption of LCB Δ4 desaturase (<i>des</i>) significantly decreased the content of GlcCer. Fluorescence imaging analysis revealed that OsSLD-OX and AtSLD-OX showed increased plasma membrane fluidity, whereas <i>des</i> had less fluidity, demonstrating that the isomers universally contributed to increasing membrane fluidity. However, the results of a hydroponic assay showed decreased aluminum tolerance in AtSLD-OX and <i>des</i> compared to OsSLD-OX and the control plants, which did not correlate with membrane fluidity. These results suggest that <i>cis</i>-unsaturated GlcCer, not GIPC, selectively serves to maintain the membrane fluidity specifically associated with aluminum tolerance.https://www.mdpi.com/2223-7747/9/1/19riceglucosylceramide<i>cis</i>/<i>trans</i> unsaturationmembrane fluidityal<sup>3+</sup> tolerance |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Masaya Sato Minoru Nagano Song Jin Atsuko Miyagi Masatoshi Yamaguchi Maki Kawai-Yamada Toshiki Ishikawa |
spellingShingle |
Masaya Sato Minoru Nagano Song Jin Atsuko Miyagi Masatoshi Yamaguchi Maki Kawai-Yamada Toshiki Ishikawa Plant-Unique <i>cis</i>/<i>trans</i> Isomerism of Long-Chain Base Unsaturation is Selectively Required for Aluminum Tolerance Resulting from Glucosylceramide-Dependent Plasma Membrane Fluidity Plants rice glucosylceramide <i>cis</i>/<i>trans</i> unsaturation membrane fluidity al<sup>3+</sup> tolerance |
author_facet |
Masaya Sato Minoru Nagano Song Jin Atsuko Miyagi Masatoshi Yamaguchi Maki Kawai-Yamada Toshiki Ishikawa |
author_sort |
Masaya Sato |
title |
Plant-Unique <i>cis</i>/<i>trans</i> Isomerism of Long-Chain Base Unsaturation is Selectively Required for Aluminum Tolerance Resulting from Glucosylceramide-Dependent Plasma Membrane Fluidity |
title_short |
Plant-Unique <i>cis</i>/<i>trans</i> Isomerism of Long-Chain Base Unsaturation is Selectively Required for Aluminum Tolerance Resulting from Glucosylceramide-Dependent Plasma Membrane Fluidity |
title_full |
Plant-Unique <i>cis</i>/<i>trans</i> Isomerism of Long-Chain Base Unsaturation is Selectively Required for Aluminum Tolerance Resulting from Glucosylceramide-Dependent Plasma Membrane Fluidity |
title_fullStr |
Plant-Unique <i>cis</i>/<i>trans</i> Isomerism of Long-Chain Base Unsaturation is Selectively Required for Aluminum Tolerance Resulting from Glucosylceramide-Dependent Plasma Membrane Fluidity |
title_full_unstemmed |
Plant-Unique <i>cis</i>/<i>trans</i> Isomerism of Long-Chain Base Unsaturation is Selectively Required for Aluminum Tolerance Resulting from Glucosylceramide-Dependent Plasma Membrane Fluidity |
title_sort |
plant-unique <i>cis</i>/<i>trans</i> isomerism of long-chain base unsaturation is selectively required for aluminum tolerance resulting from glucosylceramide-dependent plasma membrane fluidity |
publisher |
MDPI AG |
series |
Plants |
issn |
2223-7747 |
publishDate |
2019-12-01 |
description |
<i>Cis</i>/<i>trans</i> isomerism of the Δ8 unsaturation of long-chain base (LCB) is found only in plant sphingolipids. This unique geometry is generated by sphingolipid LCB Δ8 desaturase SLD which produces both isomers at various ratios, resulting in diverse <i>cis</i>/<i>trans</i> ratios in plants. However, the biological significance of this isomeric diversity remains controversial. Here, we show that the plant-specific <i>cis</i> unsaturation of LCB selectively contributes to glucosylceramide (GlcCer)-dependent tolerance to aluminum toxicity. We established three transgenic rice lines with altered LCB unsaturation profiles. Overexpression of SLD from rice (OsSLD-OX), which preferentially exhibits <i>cis</i>-activity, or Arabidopsis (AtSLD-OX), showing preference for <i>trans</i>-activity, facilitated Δ8 unsaturation in different manners: a slight increase of <i>cis</i>-unsaturated glycosylinositolphosphoceramide (GIPC) in OsSLD-OX, and a drastic increase of <i>trans</i>-unsaturated GlcCer and GIPC in AtSLD-OX. Disruption of LCB Δ4 desaturase (<i>des</i>) significantly decreased the content of GlcCer. Fluorescence imaging analysis revealed that OsSLD-OX and AtSLD-OX showed increased plasma membrane fluidity, whereas <i>des</i> had less fluidity, demonstrating that the isomers universally contributed to increasing membrane fluidity. However, the results of a hydroponic assay showed decreased aluminum tolerance in AtSLD-OX and <i>des</i> compared to OsSLD-OX and the control plants, which did not correlate with membrane fluidity. These results suggest that <i>cis</i>-unsaturated GlcCer, not GIPC, selectively serves to maintain the membrane fluidity specifically associated with aluminum tolerance. |
topic |
rice glucosylceramide <i>cis</i>/<i>trans</i> unsaturation membrane fluidity al<sup>3+</sup> tolerance |
url |
https://www.mdpi.com/2223-7747/9/1/19 |
work_keys_str_mv |
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