Plant-Unique cis/trans Isomerism of Long-Chain Base Unsaturation is Selectively Required for Aluminum Tolerance Resulting from Glucosylceramide-Dependent Plasma Membrane Fluidity
Plant-Unique cis/trans Isomerism of Long-Chain Base Unsaturation is Selectively Required for Aluminum Tolerance Resulting from Glucosylceramide-Dependent Plasma Membrane Fluidity
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DOI：
10.3390/plants9010019
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发表时间：
2019-12
期刊：
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通讯作者：
Masaya Sato;M. Nagano;Songmo Jin;A. Miyagi;M. Yamaguchi;M. Kawai‐Yamada;T. Ishikawa
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文献类型：
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作者：
Masaya Sato;M. Nagano;Songmo Jin;A. Miyagi;M. Yamaguchi;M. Kawai‐Yamada;T. Ishikawa
长链碱基不饱和Δ8的顺式/反式异构体仅存在于植物鞘脂中。这种独特的几何构型是由鞘磷脂LCBΔ8去饱和酶SLD产生的，它以不同的比例产生这两种异构体，导致植物中不同的顺式/反式比率。然而，这种异构体多样性的生物学意义仍然存在争议。在这里，我们证明了植物特有的LCB顺式不饱和选择性地促进了依赖于葡萄糖神经酰胺(GlcCer)的铝毒耐受性。我们建立了三个改变了LCB不饱和图谱的转基因水稻品系。从水稻(OsSLD-ox)和拟南芥(AtSLD-OX)过表达的SLD以不同的方式促进了Δ8的不饱和：OsSLD-OX中顺不饱和的糖肌醇磷酰胺(GIPC)略有增加，而反式不饱和GlcCer和GIPC的含量急剧增加。阻断LCBΔ4去饱和酶(DES)可显著降低GlcCer的含量。荧光成像分析表明，OsSLD-OX和AtSLD-OX表现出质膜流动性的增加，而DES的流动性较小，这表明异构体普遍有助于增加膜的流动性。然而，水培试验结果表明，与OsSLD-OX和对照相比，AtSLD-OX和DES的耐铝性降低，这与膜流动性无关。这些结果表明，顺式不饱和GlcCer，而不是GIPC，选择性地维持与耐铝性有关的膜流动性。
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.