Higher sterol content regulated by CYP51 with concomitant lower phospholipid content in membranes is a common strategy for aluminium tolerance in several plant species

Several studies have shown that differences in lipid composition and in the lipid biosynthetic pathway affect the aluminium (Al) tolerance of plants, but little is known about the molecular mechanisms underlying these differences. Phospholipids create a negative charge at the surface of the plasma m...

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Veröffentlicht in:Journal of experimental botany 2015-02, Vol.66 (3), p.907-918
Hauptverfasser: Wagatsuma, Tadao, Khan, Md. Shahadat Hossain, Watanabe, Toshihiro, Maejima, Eriko, Sekimoto, Hitoshi, Yokota, Takao, Nakano, Takeshi, Toyomasu, Tomonobu, Tawaraya, Keitaro, Koyama, Hiroyuki, Uemura, Matsuo, Ishikawa, Satoru, Ikka, Takashi, Ishikawa, Akifumi, Kawamura, Takeshi, Murakami, Satoshi, Ueki, Nozomi, Umetsu, Asami, Kannari, Takayuki
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container_issue 3
container_start_page 907
container_title Journal of experimental botany
container_volume 66
creator Wagatsuma, Tadao
Khan, Md. Shahadat Hossain
Watanabe, Toshihiro
Maejima, Eriko
Sekimoto, Hitoshi
Yokota, Takao
Nakano, Takeshi
Toyomasu, Tomonobu
Tawaraya, Keitaro
Koyama, Hiroyuki
Uemura, Matsuo
Ishikawa, Satoru
Ikka, Takashi
Ishikawa, Akifumi
Kawamura, Takeshi
Murakami, Satoshi
Ueki, Nozomi
Umetsu, Asami
Kannari, Takayuki
description Several studies have shown that differences in lipid composition and in the lipid biosynthetic pathway affect the aluminium (Al) tolerance of plants, but little is known about the molecular mechanisms underlying these differences. Phospholipids create a negative charge at the surface of the plasma membrane and enhance Al sensitivity as a result of the accumulation of positively charged Al3+ ions. The phospholipids will be balanced by other electrically neutral lipids, such as sterols. In the present research, Al tolerance was compared among pea (Pisum sativum) genotypes. Compared with Al-tolerant genotypes, the Al-sensitive genotype accumulated more Al in the root tip, had a less intact plasma membrane, and showed a lower expression level of PsCYP51, which encodes obtusifoliol-14α-demethylase (OBT 14DM), a key sterol biosynthetic enzyme. The ratio of phospholipids to sterols was higher in the sensitive genotype than in the tolerant genotypes, suggesting that the sterol biosynthetic pathway plays an important role in Al tolerance. Consistent with this idea, a transgenic Arabidopsis thaliana line with knocked-down AtCYP51 expression showed an Al-sensitive phenotype. Uniconazole-P, an inhibitor of OBT 14DM, suppressed the Al tolerance of Al-tolerant genotypes of maize (Zea mays), sorghum (Sorghum bicolor), rice (Oryza sativa), wheat (Triticum aestivum), and triticale (×Triticosecale Wittmark cv. Currency). These results suggest that increased sterol content, regulated by CYP51, with concomitant lower phospholipid content in the root tip, results in lower negativity of the plasma membrane. This appears to be a common strategy for Al tolerance among several plant species.
doi_str_mv 10.1093/jxb/eru455
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Shahadat Hossain ; Watanabe, Toshihiro ; Maejima, Eriko ; Sekimoto, Hitoshi ; Yokota, Takao ; Nakano, Takeshi ; Toyomasu, Tomonobu ; Tawaraya, Keitaro ; Koyama, Hiroyuki ; Uemura, Matsuo ; Ishikawa, Satoru ; Ikka, Takashi ; Ishikawa, Akifumi ; Kawamura, Takeshi ; Murakami, Satoshi ; Ueki, Nozomi ; Umetsu, Asami ; Kannari, Takayuki</creator><creatorcontrib>Wagatsuma, Tadao ; Khan, Md. Shahadat Hossain ; Watanabe, Toshihiro ; Maejima, Eriko ; Sekimoto, Hitoshi ; Yokota, Takao ; Nakano, Takeshi ; Toyomasu, Tomonobu ; Tawaraya, Keitaro ; Koyama, Hiroyuki ; Uemura, Matsuo ; Ishikawa, Satoru ; Ikka, Takashi ; Ishikawa, Akifumi ; Kawamura, Takeshi ; Murakami, Satoshi ; Ueki, Nozomi ; Umetsu, Asami ; Kannari, Takayuki</creatorcontrib><description>Several studies have shown that differences in lipid composition and in the lipid biosynthetic pathway affect the aluminium (Al) tolerance of plants, but little is known about the molecular mechanisms underlying these differences. Phospholipids create a negative charge at the surface of the plasma membrane and enhance Al sensitivity as a result of the accumulation of positively charged Al3+ ions. The phospholipids will be balanced by other electrically neutral lipids, such as sterols. In the present research, Al tolerance was compared among pea (Pisum sativum) genotypes. Compared with Al-tolerant genotypes, the Al-sensitive genotype accumulated more Al in the root tip, had a less intact plasma membrane, and showed a lower expression level of PsCYP51, which encodes obtusifoliol-14α-demethylase (OBT 14DM), a key sterol biosynthetic enzyme. The ratio of phospholipids to sterols was higher in the sensitive genotype than in the tolerant genotypes, suggesting that the sterol biosynthetic pathway plays an important role in Al tolerance. Consistent with this idea, a transgenic Arabidopsis thaliana line with knocked-down AtCYP51 expression showed an Al-sensitive phenotype. Uniconazole-P, an inhibitor of OBT 14DM, suppressed the Al tolerance of Al-tolerant genotypes of maize (Zea mays), sorghum (Sorghum bicolor), rice (Oryza sativa), wheat (Triticum aestivum), and triticale (×Triticosecale Wittmark cv. Currency). These results suggest that increased sterol content, regulated by CYP51, with concomitant lower phospholipid content in the root tip, results in lower negativity of the plasma membrane. 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Phospholipids create a negative charge at the surface of the plasma membrane and enhance Al sensitivity as a result of the accumulation of positively charged Al3+ ions. The phospholipids will be balanced by other electrically neutral lipids, such as sterols. In the present research, Al tolerance was compared among pea (Pisum sativum) genotypes. Compared with Al-tolerant genotypes, the Al-sensitive genotype accumulated more Al in the root tip, had a less intact plasma membrane, and showed a lower expression level of PsCYP51, which encodes obtusifoliol-14α-demethylase (OBT 14DM), a key sterol biosynthetic enzyme. The ratio of phospholipids to sterols was higher in the sensitive genotype than in the tolerant genotypes, suggesting that the sterol biosynthetic pathway plays an important role in Al tolerance. Consistent with this idea, a transgenic Arabidopsis thaliana line with knocked-down AtCYP51 expression showed an Al-sensitive phenotype. Uniconazole-P, an inhibitor of OBT 14DM, suppressed the Al tolerance of Al-tolerant genotypes of maize (Zea mays), sorghum (Sorghum bicolor), rice (Oryza sativa), wheat (Triticum aestivum), and triticale (×Triticosecale Wittmark cv. Currency). These results suggest that increased sterol content, regulated by CYP51, with concomitant lower phospholipid content in the root tip, results in lower negativity of the plasma membrane. This appears to be a common strategy for Al tolerance among several plant species.</abstract><cop>England</cop><pub>Oxford University Press</pub><pmid>25416794</pmid><doi>10.1093/jxb/eru455</doi><tpages>12</tpages><oa>free_for_read</oa></addata></record>
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subjects Aluminum - metabolism
Cell Membrane - metabolism
Cloning, Molecular
Gene Expression
Magnoliopsida - genetics
Magnoliopsida - metabolism
Models, Biological
Molecular Sequence Data
Phospholipids - metabolism
Plant Proteins - genetics
Plant Proteins - metabolism
RESEARCH PAPER
Sequence Analysis, DNA
Soil Pollutants - metabolism
Sterol 14-Demethylase - genetics
Sterol 14-Demethylase - metabolism
Sterols - metabolism
title Higher sterol content regulated by CYP51 with concomitant lower phospholipid content in membranes is a common strategy for aluminium tolerance in several plant species
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