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

• Main Authors: Masaya Sato, Minoru Nagano, Song Jin, Atsuko Miyagi, Masatoshi Yamaguchi, Maki Kawai-Yamada, Toshiki Ishikawa
• Format: Article
• Language: English
• Published: MDPI AG 2019-12-01
• Series: Plants
• Subjects: rice; glucosylceramide; <i>cis</i>/<i>trans</i> unsaturation; membrane fluidity; al³⁺ tolerance
• Online Access: https://www.mdpi.com/2223-7747/9/1/19

<i>Cis</i>/<i>trans</i> isomerism of the &#916;8 unsaturation of long-chain base (LCB) is found only in plant sphingolipids. This unique geometry is generated by sphingolipid LCB &#916;8 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 &#916;8 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 &#916;4 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.