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Plant-Unique cis/trans Isomerism of Long-Chain Base Unsaturation is Selectively Required for Aluminum Tolerance Resulting from Glucosylceramide-Dependent Plasma Membrane Fluidity

1
Graduate School of Science and Engineering, Saitama University, Saitama 338-8570, Japan
2
Graduate School of Life Sciences, Ritsumeikan University, Kusatsu, Shiga 525-8577, Japan
*
Author to whom correspondence should be addressed.
Plants 2020, 9(1), 19; https://doi.org/10.3390/plants9010019
Received: 11 November 2019 / Revised: 13 December 2019 / Accepted: 20 December 2019 / Published: 23 December 2019
(This article belongs to the Special Issue Plant Plasma Membrane)
Cis/trans 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 cis/trans ratios in plants. However, the biological significance of this isomeric diversity remains controversial. Here, we show that the plant-specific cis 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 cis-activity, or Arabidopsis (AtSLD-OX), showing preference for trans-activity, facilitated Δ8 unsaturation in different manners: a slight increase of cis-unsaturated glycosylinositolphosphoceramide (GIPC) in OsSLD-OX, and a drastic increase of trans-unsaturated GlcCer and GIPC in AtSLD-OX. Disruption of LCB Δ4 desaturase (des) significantly decreased the content of GlcCer. Fluorescence imaging analysis revealed that OsSLD-OX and AtSLD-OX showed increased plasma membrane fluidity, whereas des 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 des compared to OsSLD-OX and the control plants, which did not correlate with membrane fluidity. These results suggest that cis-unsaturated GlcCer, not GIPC, selectively serves to maintain the membrane fluidity specifically associated with aluminum tolerance. View Full-Text
Keywords: rice; glucosylceramide; cis/trans unsaturation; membrane fluidity; Al3+ tolerance rice; glucosylceramide; cis/trans unsaturation; membrane fluidity; Al3+ tolerance
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Sato, M.; Nagano, M.; Jin, S.; Miyagi, A.; Yamaguchi, M.; Kawai-Yamada, M.; Ishikawa, T. Plant-Unique cis/trans Isomerism of Long-Chain Base Unsaturation is Selectively Required for Aluminum Tolerance Resulting from Glucosylceramide-Dependent Plasma Membrane Fluidity. Plants 2020, 9, 19.

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