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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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. This appears to be a common strategy for Al tolerance among several plant species.</description><identifier>ISSN: 0022-0957</identifier><identifier>EISSN: 1460-2431</identifier><identifier>DOI: 10.1093/jxb/eru455</identifier><identifier>PMID: 25416794</identifier><language>eng</language><publisher>England: Oxford University Press</publisher><subject>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</subject><ispartof>Journal of experimental botany, 2015-02, Vol.66 (3), p.907-918</ispartof><rights>The Author 2014</rights><rights>The Author 2014. Published by Oxford University Press on behalf of the Society for Experimental Biology.</rights><rights>The Author 2014. 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Shahadat Hossain</creatorcontrib><creatorcontrib>Watanabe, Toshihiro</creatorcontrib><creatorcontrib>Maejima, Eriko</creatorcontrib><creatorcontrib>Sekimoto, Hitoshi</creatorcontrib><creatorcontrib>Yokota, Takao</creatorcontrib><creatorcontrib>Nakano, Takeshi</creatorcontrib><creatorcontrib>Toyomasu, Tomonobu</creatorcontrib><creatorcontrib>Tawaraya, Keitaro</creatorcontrib><creatorcontrib>Koyama, Hiroyuki</creatorcontrib><creatorcontrib>Uemura, Matsuo</creatorcontrib><creatorcontrib>Ishikawa, Satoru</creatorcontrib><creatorcontrib>Ikka, Takashi</creatorcontrib><creatorcontrib>Ishikawa, Akifumi</creatorcontrib><creatorcontrib>Kawamura, Takeshi</creatorcontrib><creatorcontrib>Murakami, Satoshi</creatorcontrib><creatorcontrib>Ueki, Nozomi</creatorcontrib><creatorcontrib>Umetsu, Asami</creatorcontrib><creatorcontrib>Kannari, Takayuki</creatorcontrib><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</title><title>Journal of experimental botany</title><addtitle>J Exp Bot</addtitle><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.</description><subject>Aluminum - metabolism</subject><subject>Cell Membrane - metabolism</subject><subject>Cloning, Molecular</subject><subject>Gene Expression</subject><subject>Magnoliopsida - genetics</subject><subject>Magnoliopsida - metabolism</subject><subject>Models, Biological</subject><subject>Molecular Sequence Data</subject><subject>Phospholipids - metabolism</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>RESEARCH PAPER</subject><subject>Sequence Analysis, DNA</subject><subject>Soil Pollutants - metabolism</subject><subject>Sterol 14-Demethylase - genetics</subject><subject>Sterol 14-Demethylase - metabolism</subject><subject>Sterols - metabolism</subject><issn>0022-0957</issn><issn>1460-2431</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVkUtvGyEUhVHVqnHSbrpvxDrSJDwG7NlEqqy8pEjNIl10NYKZi40FwwiYJP5F-ZvFcuqmCwTofOdc0EHoGyXnlDT8YvOiLyBOtRAf0IzWklSs5vQjmhHCWEUaMT9CxyltCCGCCPEZHTFRUzlv6hl6vbWrNUScMsTgcBeGDEPGEVaTUxl6rLd4-ftBUPxs83qnd8HbrArjwnMxjuuQynJ2tP3BbgfsweuoBkjYJqyK4n0YyphYUldbbELEyk3eDnbyOAcHBe5g50zwVC4Oj243JY3QWUhf0CejXIKvb_sJ-nV99bi8re5_3twtf9xXXU1IriRwLpUw2iwMYVzIHpTQlFFtGJXl3FPNOMhmYSjRXU8l0QtlZEHmjMwVP0GX-9xx0h76rvymvKUdo_UqbtugbPu_Mth1uwpPbc0ZFYKXgLN9QBdDShHMwUtJu6urLXW1-7oKfPp-2gH9208Bvu-BTcoh_tMlXzRF5n8A9aihtw</recordid><startdate>20150201</startdate><enddate>20150201</enddate><creator>Wagatsuma, Tadao</creator><creator>Khan, Md. 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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</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c400t-6e336a5fbf8f02356dea5b121bf216ea5d1b23e698f10bcd160b8af6b127207a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Aluminum - metabolism</topic><topic>Cell Membrane - metabolism</topic><topic>Cloning, Molecular</topic><topic>Gene Expression</topic><topic>Magnoliopsida - genetics</topic><topic>Magnoliopsida - metabolism</topic><topic>Models, Biological</topic><topic>Molecular Sequence Data</topic><topic>Phospholipids - metabolism</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - metabolism</topic><topic>RESEARCH PAPER</topic><topic>Sequence Analysis, DNA</topic><topic>Soil Pollutants - metabolism</topic><topic>Sterol 14-Demethylase - genetics</topic><topic>Sterol 14-Demethylase - metabolism</topic><topic>Sterols - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wagatsuma, Tadao</creatorcontrib><creatorcontrib>Khan, Md. 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Shahadat Hossain</au><au>Watanabe, Toshihiro</au><au>Maejima, Eriko</au><au>Sekimoto, Hitoshi</au><au>Yokota, Takao</au><au>Nakano, Takeshi</au><au>Toyomasu, Tomonobu</au><au>Tawaraya, Keitaro</au><au>Koyama, Hiroyuki</au><au>Uemura, Matsuo</au><au>Ishikawa, Satoru</au><au>Ikka, Takashi</au><au>Ishikawa, Akifumi</au><au>Kawamura, Takeshi</au><au>Murakami, Satoshi</au><au>Ueki, Nozomi</au><au>Umetsu, Asami</au><au>Kannari, Takayuki</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Higher sterol content regulated by CYP51 with concomitant lower phospholipid content in membranes is a common strategy for aluminium tolerance in several plant species</atitle><jtitle>Journal of experimental botany</jtitle><addtitle>J Exp Bot</addtitle><date>2015-02-01</date><risdate>2015</risdate><volume>66</volume><issue>3</issue><spage>907</spage><epage>918</epage><pages>907-918</pages><issn>0022-0957</issn><eissn>1460-2431</eissn><abstract>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.</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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