RNAi-mediated tocopherol deficiency impairs photoassimilate export in transgenic potato plants

Tocopherols (vitamin E) are lipophilic antioxidants presumed to play a key role in protecting chloroplast membranes and the photosynthetic apparatus from photooxidative damage. Additional nonantioxidant functions of tocopherols have been proposed after the recent finding that the Suc export defectiv...

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Veröffentlicht in:Plant physiology (Bethesda) 2004-07, Vol.135 (3), p.1256-1268
Hauptverfasser: Hofius, D, Hajirezaei, M.R, Geiger, M, Tschiersch, H, Melzer, M, Sonnewald, U
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container_title Plant physiology (Bethesda)
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creator Hofius, D
Hajirezaei, M.R
Geiger, M
Tschiersch, H
Melzer, M
Sonnewald, U
description Tocopherols (vitamin E) are lipophilic antioxidants presumed to play a key role in protecting chloroplast membranes and the photosynthetic apparatus from photooxidative damage. Additional nonantioxidant functions of tocopherols have been proposed after the recent finding that the Suc export defective1 maize (Zea mays) mutant (sxd1) carries a defect in tocopherol cyclase (TC) and thus is devoid of tocopherols. However, the corresponding vitamin E deficient1 Arabidopsis mutant (vte1) lacks a phenotype analogous to sxd1, suggesting differences in tocopherol function between C4 and C3 plants. Therefore, in this study, the potato (Solanum tuberosum) ortholog of SXD1 was isolated and functionally characterized. StSXD1 encoded a protein with high TC activity in vitro, and chloroplastic localization was demonstrated by transient expression of green fluorescent protein-tagged fusion constructs. RNAi-mediated silencing of StSXD1 in transgenic potato plants resulted in the disruption of TC activity and severe tocopherol deficiency similar to the orthologous sxd1 and vte1 mutants. The nearly complete absence of tocopherols caused a characteristic photoassimilate export-defective phenotype comparable to sxd1, which appeared to be a consequence of vascular-specific callose deposition observed in source leaves. CO2 assimilation rates and photosynthetic gene expression were decreased in source leaves in close correlation with excess sugar accumulation, suggesting a carbohydrate-mediated feedback inhibition rather than a direct impact of tocopherol deficiency on photosynthetic capacity. This conclusion is further supported by an increased photosynthetic capacity of young leaves regardless of decreased tocopherol levels. Our data provide evidence that tocopherol deficiency leads to impaired photoassimilate export from source leaves in both monocot and dicot plant species and suggest significant differences among C3 plants in response to tocopherol reduction.
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Additional nonantioxidant functions of tocopherols have been proposed after the recent finding that the Suc export defective1 maize (Zea mays) mutant (sxd1) carries a defect in tocopherol cyclase (TC) and thus is devoid of tocopherols. However, the corresponding vitamin E deficient1 Arabidopsis mutant (vte1) lacks a phenotype analogous to sxd1, suggesting differences in tocopherol function between C4 and C3 plants. Therefore, in this study, the potato (Solanum tuberosum) ortholog of SXD1 was isolated and functionally characterized. StSXD1 encoded a protein with high TC activity in vitro, and chloroplastic localization was demonstrated by transient expression of green fluorescent protein-tagged fusion constructs. RNAi-mediated silencing of StSXD1 in transgenic potato plants resulted in the disruption of TC activity and severe tocopherol deficiency similar to the orthologous sxd1 and vte1 mutants. The nearly complete absence of tocopherols caused a characteristic photoassimilate export-defective phenotype comparable to sxd1, which appeared to be a consequence of vascular-specific callose deposition observed in source leaves. CO2 assimilation rates and photosynthetic gene expression were decreased in source leaves in close correlation with excess sugar accumulation, suggesting a carbohydrate-mediated feedback inhibition rather than a direct impact of tocopherol deficiency on photosynthetic capacity. This conclusion is further supported by an increased photosynthetic capacity of young leaves regardless of decreased tocopherol levels. 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Psychology ; gene expression regulation ; gene silencing ; isomerases ; Leaves ; Metabolism ; Molecular Sequence Data ; nucleotide sequences ; phenotype ; Phenotypes ; photosynthesis ; Photosynthesis, respiration. Anabolism, catabolism ; physiological transport ; Plant cells ; Plant physiology and development ; plant proteins ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Plants ; Plants, Genetically Modified - genetics ; Plants, Genetically Modified - metabolism ; potatoes ; recombinant proteins ; RNA ; RNA Interference - physiology ; RNA, Plant - genetics ; RNA, Small Interfering - genetics ; small interfering RNA ; Solanum tuberosum ; Solanum tuberosum - genetics ; Solanum tuberosum - metabolism ; starch crops ; Starches ; tissue distribution ; tocopherol cyclase ; Tocopherols ; Tocopherols - metabolism ; Transgenic plants ; Zea mays</subject><ispartof>Plant physiology (Bethesda), 2004-07, Vol.135 (3), p.1256-1268</ispartof><rights>Copyright 2004 American Society of Plant Biologists</rights><rights>2004 INIST-CNRS</rights><rights>Copyright © 2004, American Society of Plant Biologists 2004</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c525t-8b56cfd8339d839095887145b313daa86e497620a424c4cce8ae77eb1984ddc83</citedby><cites>FETCH-LOGICAL-c525t-8b56cfd8339d839095887145b313daa86e497620a424c4cce8ae77eb1984ddc83</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/4356488$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/4356488$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,776,780,799,881,27901,27902,57992,58225</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&amp;idt=15951113$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/15247386$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Hofius, D</creatorcontrib><creatorcontrib>Hajirezaei, M.R</creatorcontrib><creatorcontrib>Geiger, M</creatorcontrib><creatorcontrib>Tschiersch, H</creatorcontrib><creatorcontrib>Melzer, M</creatorcontrib><creatorcontrib>Sonnewald, U</creatorcontrib><title>RNAi-mediated tocopherol deficiency impairs photoassimilate export in transgenic potato plants</title><title>Plant physiology (Bethesda)</title><addtitle>Plant Physiol</addtitle><description>Tocopherols (vitamin E) are lipophilic antioxidants presumed to play a key role in protecting chloroplast membranes and the photosynthetic apparatus from photooxidative damage. Additional nonantioxidant functions of tocopherols have been proposed after the recent finding that the Suc export defective1 maize (Zea mays) mutant (sxd1) carries a defect in tocopherol cyclase (TC) and thus is devoid of tocopherols. However, the corresponding vitamin E deficient1 Arabidopsis mutant (vte1) lacks a phenotype analogous to sxd1, suggesting differences in tocopherol function between C4 and C3 plants. Therefore, in this study, the potato (Solanum tuberosum) ortholog of SXD1 was isolated and functionally characterized. StSXD1 encoded a protein with high TC activity in vitro, and chloroplastic localization was demonstrated by transient expression of green fluorescent protein-tagged fusion constructs. RNAi-mediated silencing of StSXD1 in transgenic potato plants resulted in the disruption of TC activity and severe tocopherol deficiency similar to the orthologous sxd1 and vte1 mutants. The nearly complete absence of tocopherols caused a characteristic photoassimilate export-defective phenotype comparable to sxd1, which appeared to be a consequence of vascular-specific callose deposition observed in source leaves. CO2 assimilation rates and photosynthetic gene expression were decreased in source leaves in close correlation with excess sugar accumulation, suggesting a carbohydrate-mediated feedback inhibition rather than a direct impact of tocopherol deficiency on photosynthetic capacity. This conclusion is further supported by an increased photosynthetic capacity of young leaves regardless of decreased tocopherol levels. 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Psychology</subject><subject>gene expression regulation</subject><subject>gene silencing</subject><subject>isomerases</subject><subject>Leaves</subject><subject>Metabolism</subject><subject>Molecular Sequence Data</subject><subject>nucleotide sequences</subject><subject>phenotype</subject><subject>Phenotypes</subject><subject>photosynthesis</subject><subject>Photosynthesis, respiration. Anabolism, catabolism</subject><subject>physiological transport</subject><subject>Plant cells</subject><subject>Plant physiology and development</subject><subject>plant proteins</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Plants</subject><subject>Plants, Genetically Modified - genetics</subject><subject>Plants, Genetically Modified - metabolism</subject><subject>potatoes</subject><subject>recombinant proteins</subject><subject>RNA</subject><subject>RNA Interference - physiology</subject><subject>RNA, Plant - genetics</subject><subject>RNA, Small Interfering - genetics</subject><subject>small interfering RNA</subject><subject>Solanum tuberosum</subject><subject>Solanum tuberosum - genetics</subject><subject>Solanum tuberosum - metabolism</subject><subject>starch crops</subject><subject>Starches</subject><subject>tissue distribution</subject><subject>tocopherol cyclase</subject><subject>Tocopherols</subject><subject>Tocopherols - metabolism</subject><subject>Transgenic plants</subject><subject>Zea mays</subject><issn>0032-0889</issn><issn>1532-2548</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2004</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkj1vFDEQhi0EIpdASYfADXR7-HPXLiiiiABSBBKQFsvnnb1ztLt2bB8i_x6f9hRCReOx9D4zmpl3EHpByZpSIt7FuK5hTQTXrHuEVlRy1jAp1GO0IqT-iVL6BJ3mfEMIoZyKp-iESiY6rtoV-vnty7lvJui9LdDjElyIO0hhxD0M3nmY3R32U7Q-ZRx3oQSbs5_8WHEMv2NIBfsZl2TnvIXZOxxDsSXgONq55GfoyWDHDM-P8QxdX374cfGpufr68fPF-VXjJJOlURvZuqFXnOv6aKKlUh0VcsMp761VLQjdtYxYwYQTzoGy0HWwoVqJvneKn6H3S92439RhHMy1o9HE5Ceb7kyw3vyrzH5ntuGXkVQTIWv-22N-Crd7yMVMPjsY6xAQ9tm0bcclYfq_INWdbqU8gM0CuhRyTjDcN0OJOThnYjSHsDhX-VcPJ_hLH62qwJsjYLOz41A37nx-wGlJKeWVe7lwN7mEdK8LLluhDpt6vciDDcZuUy1x_Z3VwyBECy6qBX8AD3q2Ew</recordid><startdate>20040701</startdate><enddate>20040701</enddate><creator>Hofius, D</creator><creator>Hajirezaei, M.R</creator><creator>Geiger, M</creator><creator>Tschiersch, H</creator><creator>Melzer, M</creator><creator>Sonnewald, U</creator><general>American Society of Plant Biologists</general><general>American Society of Plant Physiologists</general><scope>FBQ</scope><scope>IQODW</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QO</scope><scope>8FD</scope><scope>FR3</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20040701</creationdate><title>RNAi-mediated tocopherol deficiency impairs photoassimilate export in transgenic potato plants</title><author>Hofius, D ; Hajirezaei, M.R ; Geiger, M ; Tschiersch, H ; Melzer, M ; Sonnewald, U</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c525t-8b56cfd8339d839095887145b313daa86e497620a424c4cce8ae77eb1984ddc83</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2004</creationdate><topic>Amino acids</topic><topic>Arabidopsis</topic><topic>assimilation (physiology)</topic><topic>Biochemical Processes and Macromolecular Structures</topic><topic>Biological and medical sciences</topic><topic>callose</topic><topic>chloroplasts</topic><topic>Chloroplasts - enzymology</topic><topic>Chloroplasts - genetics</topic><topic>Complementary DNA</topic><topic>Corn</topic><topic>enzyme activity</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>gene expression regulation</topic><topic>gene silencing</topic><topic>isomerases</topic><topic>Leaves</topic><topic>Metabolism</topic><topic>Molecular Sequence Data</topic><topic>nucleotide sequences</topic><topic>phenotype</topic><topic>Phenotypes</topic><topic>photosynthesis</topic><topic>Photosynthesis, respiration. Anabolism, catabolism</topic><topic>physiological transport</topic><topic>Plant cells</topic><topic>Plant physiology and development</topic><topic>plant proteins</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - metabolism</topic><topic>Plants</topic><topic>Plants, Genetically Modified - genetics</topic><topic>Plants, Genetically Modified - metabolism</topic><topic>potatoes</topic><topic>recombinant proteins</topic><topic>RNA</topic><topic>RNA Interference - physiology</topic><topic>RNA, Plant - genetics</topic><topic>RNA, Small Interfering - genetics</topic><topic>small interfering RNA</topic><topic>Solanum tuberosum</topic><topic>Solanum tuberosum - genetics</topic><topic>Solanum tuberosum - metabolism</topic><topic>starch crops</topic><topic>Starches</topic><topic>tissue distribution</topic><topic>tocopherol cyclase</topic><topic>Tocopherols</topic><topic>Tocopherols - metabolism</topic><topic>Transgenic plants</topic><topic>Zea mays</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Hofius, D</creatorcontrib><creatorcontrib>Hajirezaei, M.R</creatorcontrib><creatorcontrib>Geiger, M</creatorcontrib><creatorcontrib>Tschiersch, H</creatorcontrib><creatorcontrib>Melzer, M</creatorcontrib><creatorcontrib>Sonnewald, U</creatorcontrib><collection>AGRIS</collection><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Biotechnology Research Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Plant physiology (Bethesda)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Hofius, D</au><au>Hajirezaei, M.R</au><au>Geiger, M</au><au>Tschiersch, H</au><au>Melzer, M</au><au>Sonnewald, U</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>RNAi-mediated tocopherol deficiency impairs photoassimilate export in transgenic potato plants</atitle><jtitle>Plant physiology (Bethesda)</jtitle><addtitle>Plant Physiol</addtitle><date>2004-07-01</date><risdate>2004</risdate><volume>135</volume><issue>3</issue><spage>1256</spage><epage>1268</epage><pages>1256-1268</pages><issn>0032-0889</issn><eissn>1532-2548</eissn><coden>PPHYA5</coden><abstract>Tocopherols (vitamin E) are lipophilic antioxidants presumed to play a key role in protecting chloroplast membranes and the photosynthetic apparatus from photooxidative damage. Additional nonantioxidant functions of tocopherols have been proposed after the recent finding that the Suc export defective1 maize (Zea mays) mutant (sxd1) carries a defect in tocopherol cyclase (TC) and thus is devoid of tocopherols. However, the corresponding vitamin E deficient1 Arabidopsis mutant (vte1) lacks a phenotype analogous to sxd1, suggesting differences in tocopherol function between C4 and C3 plants. Therefore, in this study, the potato (Solanum tuberosum) ortholog of SXD1 was isolated and functionally characterized. StSXD1 encoded a protein with high TC activity in vitro, and chloroplastic localization was demonstrated by transient expression of green fluorescent protein-tagged fusion constructs. RNAi-mediated silencing of StSXD1 in transgenic potato plants resulted in the disruption of TC activity and severe tocopherol deficiency similar to the orthologous sxd1 and vte1 mutants. The nearly complete absence of tocopherols caused a characteristic photoassimilate export-defective phenotype comparable to sxd1, which appeared to be a consequence of vascular-specific callose deposition observed in source leaves. CO2 assimilation rates and photosynthetic gene expression were decreased in source leaves in close correlation with excess sugar accumulation, suggesting a carbohydrate-mediated feedback inhibition rather than a direct impact of tocopherol deficiency on photosynthetic capacity. This conclusion is further supported by an increased photosynthetic capacity of young leaves regardless of decreased tocopherol levels. Our data provide evidence that tocopherol deficiency leads to impaired photoassimilate export from source leaves in both monocot and dicot plant species and suggest significant differences among C3 plants in response to tocopherol reduction.</abstract><cop>Rockville, MD</cop><pub>American Society of Plant Biologists</pub><pmid>15247386</pmid><doi>10.1104/pp.104.043927</doi><tpages>13</tpages><oa>free_for_read</oa></addata></record>
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source Jstor Complete Legacy; Oxford University Press Journals All Titles (1996-Current); MEDLINE; EZB-FREE-00999 freely available EZB journals
subjects Amino acids
Arabidopsis
assimilation (physiology)
Biochemical Processes and Macromolecular Structures
Biological and medical sciences
callose
chloroplasts
Chloroplasts - enzymology
Chloroplasts - genetics
Complementary DNA
Corn
enzyme activity
Fundamental and applied biological sciences. Psychology
gene expression regulation
gene silencing
isomerases
Leaves
Metabolism
Molecular Sequence Data
nucleotide sequences
phenotype
Phenotypes
photosynthesis
Photosynthesis, respiration. Anabolism, catabolism
physiological transport
Plant cells
Plant physiology and development
plant proteins
Plant Proteins - genetics
Plant Proteins - metabolism
Plants
Plants, Genetically Modified - genetics
Plants, Genetically Modified - metabolism
potatoes
recombinant proteins
RNA
RNA Interference - physiology
RNA, Plant - genetics
RNA, Small Interfering - genetics
small interfering RNA
Solanum tuberosum
Solanum tuberosum - genetics
Solanum tuberosum - metabolism
starch crops
Starches
tissue distribution
tocopherol cyclase
Tocopherols
Tocopherols - metabolism
Transgenic plants
Zea mays
title RNAi-mediated tocopherol deficiency impairs photoassimilate export in transgenic potato plants
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