Molecular Characterization of the Fatty Alcohol Oxidation Pathway for Wax-Ester Mobilization in Germinated Jojoba Seeds
Jojoba (Simmondsia chinensis) is the only plant species known to use liquid wax esters (WEs) as a primary seed storage reserve. Upon germination, WE hydrolysis releases very-long-chain fatty alcohols, which must be oxidized to fatty adds by the sequential action of a fatty alcohol oxidase (FAO) and...
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| Veröffentlicht in: | Plant physiology (Bethesda) 2013-01, Vol.161 (1), p.72-80 |
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| creator | Rajangam, Alex S. Gidda, Satinder K. Craddock, Christian Mullen, Robert T. Dyer, John M. Eastmond, Peter J. |
| description | Jojoba (Simmondsia chinensis) is the only plant species known to use liquid wax esters (WEs) as a primary seed storage reserve. Upon germination, WE hydrolysis releases very-long-chain fatty alcohols, which must be oxidized to fatty adds by the sequential action of a fatty alcohol oxidase (FAO) and a fatty aldehyde dehydrogenase (FADH) before they can be β-oxidized. Here, we describe the cloning and characterization of genes for each of these two activities. Jojoba FAO and FADH are 52% and 68% identical to Arabidopsis (Arabidopsis thaliana ) FAO3 and ALDH3H1, respectively. The genes are expressed most strongly in the cotyledons of jojoba seedlings following germination, but transcripts can also be detected in vegetative tissues. Proteomic analysis indicated that the FAO and FADH proteins can be detected on wax bodies, but they localized to the endoplasmic reticulum when they were expressed as amino-terminal green fluorescent protein fusions in tobacco (Nicotiana tabacum) leaves. Recombinant jojoba FAO and FADH proteins are active on very-long-chain fatty alcohol and fatty aldehyde substrates, respectively, and have biochemical properties consistent with those previously reported in jojoba cotyledons. Coexpression of jojoba FAO and FADH in Arabidopsis enhanced the in vivo rate of fatty alcohol oxidation more than 4-fold. Taken together, our data suggest that jojoba FAO and FADH constitute the very-long-chain fatty alcohol oxidation pathway that is likely to be necessary for efficient WE mobilization following seed germination. |
| doi_str_mv | 10.1104/pp.112.208264 |
| format | Article |
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Upon germination, WE hydrolysis releases very-long-chain fatty alcohols, which must be oxidized to fatty adds by the sequential action of a fatty alcohol oxidase (FAO) and a fatty aldehyde dehydrogenase (FADH) before they can be β-oxidized. Here, we describe the cloning and characterization of genes for each of these two activities. Jojoba FAO and FADH are 52% and 68% identical to Arabidopsis (Arabidopsis thaliana ) FAO3 and ALDH3H1, respectively. The genes are expressed most strongly in the cotyledons of jojoba seedlings following germination, but transcripts can also be detected in vegetative tissues. Proteomic analysis indicated that the FAO and FADH proteins can be detected on wax bodies, but they localized to the endoplasmic reticulum when they were expressed as amino-terminal green fluorescent protein fusions in tobacco (Nicotiana tabacum) leaves. Recombinant jojoba FAO and FADH proteins are active on very-long-chain fatty alcohol and fatty aldehyde substrates, respectively, and have biochemical properties consistent with those previously reported in jojoba cotyledons. Coexpression of jojoba FAO and FADH in Arabidopsis enhanced the in vivo rate of fatty alcohol oxidation more than 4-fold. Taken together, our data suggest that jojoba FAO and FADH constitute the very-long-chain fatty alcohol oxidation pathway that is likely to be necessary for efficient WE mobilization following seed germination.</description><identifier>ISSN: 0032-0889</identifier><identifier>ISSN: 1532-2548</identifier><identifier>EISSN: 1532-2548</identifier><identifier>DOI: 10.1104/pp.112.208264</identifier><identifier>PMID: 23166353</identifier><identifier>CODEN: PPHYA5</identifier><language>eng</language><publisher>Rockville, MD: American Society of Plant Biologists</publisher><subject>alcohol oxidase ; Alcohol Oxidoreductases - genetics ; Alcohol Oxidoreductases - metabolism ; aldehyde dehydrogenase ; Aldehyde Oxidoreductases - metabolism ; Aldehydes ; Arabidopsis - enzymology ; Arabidopsis - genetics ; Arabidopsis thaliana ; BIOCHEMISTRY AND METABOLISM ; Biological and medical sciences ; Cloning, Molecular ; Cotyledon - genetics ; Cotyledon - metabolism ; Cotyledons ; endoplasmic reticulum ; Endoplasmic Reticulum - metabolism ; Enzyme Activation ; Enzymes ; Epidermal cells ; Esters - metabolism ; Fatty acids ; Fatty alcohols ; Fatty Alcohols - metabolism ; Food and Agriculture Organization ; Fundamental and applied biological sciences. Psychology ; gene expression ; Gene Expression Regulation, Enzymologic ; Gene Expression Regulation, Plant ; genes ; Genes, Plant ; Germination ; green fluorescent protein ; hydrolysis ; jojoba ; leaves ; Magnoliopsida - enzymology ; Magnoliopsida - genetics ; Nicotiana - enzymology ; Nicotiana - genetics ; Nicotiana tabacum ; Oxidation ; Oxidation-Reduction ; Plant Leaves - enzymology ; Plant Leaves - genetics ; Plant physiology and development ; Plants, Genetically Modified - enzymology ; Plants, Genetically Modified - genetics ; Proteins ; proteomics ; Proteomics - methods ; Recombinant Fusion Proteins - genetics ; Recombinant Fusion Proteins - metabolism ; seed germination ; seed storage ; Seedlings ; Seeds - genetics ; Seeds - metabolism ; Simmondsia chinensis ; tissues ; tobacco ; wax esters ; Waxes ; Waxes - metabolism</subject><ispartof>Plant physiology (Bethesda), 2013-01, Vol.161 (1), p.72-80</ispartof><rights>2013 American Society of Plant Biologists</rights><rights>2014 INIST-CNRS</rights><rights>2013 American Society of Plant Biologists. All Rights Reserved. 2013</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c538t-858b6b82fb1cb43c58245b6fc9f986b532006c3ebf363babebc5da6f60d9e0fa3</citedby><cites>FETCH-LOGICAL-c538t-858b6b82fb1cb43c58245b6fc9f986b532006c3ebf363babebc5da6f60d9e0fa3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/41942667$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/41942667$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,778,782,801,883,27907,27908,58000,58233</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=27062894$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23166353$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Rajangam, Alex S.</creatorcontrib><creatorcontrib>Gidda, Satinder K.</creatorcontrib><creatorcontrib>Craddock, Christian</creatorcontrib><creatorcontrib>Mullen, Robert T.</creatorcontrib><creatorcontrib>Dyer, John M.</creatorcontrib><creatorcontrib>Eastmond, Peter J.</creatorcontrib><title>Molecular Characterization of the Fatty Alcohol Oxidation Pathway for Wax-Ester Mobilization in Germinated Jojoba Seeds</title><title>Plant physiology (Bethesda)</title><addtitle>Plant Physiol</addtitle><description>Jojoba (Simmondsia chinensis) is the only plant species known to use liquid wax esters (WEs) as a primary seed storage reserve. Upon germination, WE hydrolysis releases very-long-chain fatty alcohols, which must be oxidized to fatty adds by the sequential action of a fatty alcohol oxidase (FAO) and a fatty aldehyde dehydrogenase (FADH) before they can be β-oxidized. Here, we describe the cloning and characterization of genes for each of these two activities. Jojoba FAO and FADH are 52% and 68% identical to Arabidopsis (Arabidopsis thaliana ) FAO3 and ALDH3H1, respectively. The genes are expressed most strongly in the cotyledons of jojoba seedlings following germination, but transcripts can also be detected in vegetative tissues. Proteomic analysis indicated that the FAO and FADH proteins can be detected on wax bodies, but they localized to the endoplasmic reticulum when they were expressed as amino-terminal green fluorescent protein fusions in tobacco (Nicotiana tabacum) leaves. Recombinant jojoba FAO and FADH proteins are active on very-long-chain fatty alcohol and fatty aldehyde substrates, respectively, and have biochemical properties consistent with those previously reported in jojoba cotyledons. Coexpression of jojoba FAO and FADH in Arabidopsis enhanced the in vivo rate of fatty alcohol oxidation more than 4-fold. Taken together, our data suggest that jojoba FAO and FADH constitute the very-long-chain fatty alcohol oxidation pathway that is likely to be necessary for efficient WE mobilization following seed germination.</description><subject>alcohol oxidase</subject><subject>Alcohol Oxidoreductases - genetics</subject><subject>Alcohol Oxidoreductases - metabolism</subject><subject>aldehyde dehydrogenase</subject><subject>Aldehyde Oxidoreductases - metabolism</subject><subject>Aldehydes</subject><subject>Arabidopsis - enzymology</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis thaliana</subject><subject>BIOCHEMISTRY AND METABOLISM</subject><subject>Biological and medical sciences</subject><subject>Cloning, Molecular</subject><subject>Cotyledon - genetics</subject><subject>Cotyledon - metabolism</subject><subject>Cotyledons</subject><subject>endoplasmic reticulum</subject><subject>Endoplasmic Reticulum - metabolism</subject><subject>Enzyme Activation</subject><subject>Enzymes</subject><subject>Epidermal cells</subject><subject>Esters - metabolism</subject><subject>Fatty acids</subject><subject>Fatty alcohols</subject><subject>Fatty Alcohols - metabolism</subject><subject>Food and Agriculture Organization</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>gene expression</subject><subject>Gene Expression Regulation, Enzymologic</subject><subject>Gene Expression Regulation, Plant</subject><subject>genes</subject><subject>Genes, Plant</subject><subject>Germination</subject><subject>green fluorescent protein</subject><subject>hydrolysis</subject><subject>jojoba</subject><subject>leaves</subject><subject>Magnoliopsida - enzymology</subject><subject>Magnoliopsida - genetics</subject><subject>Nicotiana - enzymology</subject><subject>Nicotiana - genetics</subject><subject>Nicotiana tabacum</subject><subject>Oxidation</subject><subject>Oxidation-Reduction</subject><subject>Plant Leaves - enzymology</subject><subject>Plant Leaves - genetics</subject><subject>Plant physiology and development</subject><subject>Plants, Genetically Modified - enzymology</subject><subject>Plants, Genetically Modified - genetics</subject><subject>Proteins</subject><subject>proteomics</subject><subject>Proteomics - methods</subject><subject>Recombinant Fusion Proteins - genetics</subject><subject>Recombinant Fusion Proteins - metabolism</subject><subject>seed germination</subject><subject>seed storage</subject><subject>Seedlings</subject><subject>Seeds - genetics</subject><subject>Seeds - metabolism</subject><subject>Simmondsia chinensis</subject><subject>tissues</subject><subject>tobacco</subject><subject>wax esters</subject><subject>Waxes</subject><subject>Waxes - metabolism</subject><issn>0032-0889</issn><issn>1532-2548</issn><issn>1532-2548</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkc1vEzEQxVcIREPhyBHkCxKXLf7YdbwXpCpqC6hVkQBxtMZemzhy1lvboU3_-jraNMCJ07P0fvPkmVdVrwk-IQQ3H8axKD2hWFDePKlmpGW0pm0jnlYzjMsbC9EdVS9SWmGMCSPN8-qIMsI5a9msur0K3uiNh4gWS4igs4nuHrILAwoW5aVB55DzFp16HZbBo-s710_2V8jLW9giGyL6CXf1WSqz6Coo5x8T3IAuTFy7AbLp0ZewCgrQN2P69LJ6ZsEn82qvx9WP87Pvi0_15fXF58XpZa1bJnItWqG4EtQqolXDdCto0ypudWc7wVXZFWOumVGWcaZAGaXbHrjluO8MtsCOq49T7rhRa9NrM-QIXo7RrSFuZQAn_3UGt5S_wm9ZrkOpmJeA9_uAGG42JmW5dkkb72EwYZMk3V2VYNKS_6KEzhnDDW1wQesJ1TGkFI09_IhguetVjmNRKqdeC__27zUO9GORBXi3ByBp8DbCoF36w80xp6LbBb2ZuFXKIR78hnQN5XzOHgAn_rcV</recordid><startdate>20130101</startdate><enddate>20130101</enddate><creator>Rajangam, Alex S.</creator><creator>Gidda, Satinder K.</creator><creator>Craddock, Christian</creator><creator>Mullen, Robert T.</creator><creator>Dyer, John M.</creator><creator>Eastmond, Peter J.</creator><general>American Society of Plant Biologists</general><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>7X8</scope><scope>7S9</scope><scope>L.6</scope><scope>5PM</scope></search><sort><creationdate>20130101</creationdate><title>Molecular Characterization of the Fatty Alcohol Oxidation Pathway for Wax-Ester Mobilization in Germinated Jojoba Seeds</title><author>Rajangam, Alex S. ; Gidda, Satinder K. ; Craddock, Christian ; Mullen, Robert T. ; Dyer, John M. ; Eastmond, Peter J.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c538t-858b6b82fb1cb43c58245b6fc9f986b532006c3ebf363babebc5da6f60d9e0fa3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>alcohol oxidase</topic><topic>Alcohol Oxidoreductases - genetics</topic><topic>Alcohol Oxidoreductases - metabolism</topic><topic>aldehyde dehydrogenase</topic><topic>Aldehyde Oxidoreductases - metabolism</topic><topic>Aldehydes</topic><topic>Arabidopsis - enzymology</topic><topic>Arabidopsis - genetics</topic><topic>Arabidopsis thaliana</topic><topic>BIOCHEMISTRY AND METABOLISM</topic><topic>Biological and medical sciences</topic><topic>Cloning, Molecular</topic><topic>Cotyledon - genetics</topic><topic>Cotyledon - metabolism</topic><topic>Cotyledons</topic><topic>endoplasmic reticulum</topic><topic>Endoplasmic Reticulum - metabolism</topic><topic>Enzyme Activation</topic><topic>Enzymes</topic><topic>Epidermal cells</topic><topic>Esters - metabolism</topic><topic>Fatty acids</topic><topic>Fatty alcohols</topic><topic>Fatty Alcohols - metabolism</topic><topic>Food and Agriculture Organization</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>gene expression</topic><topic>Gene Expression Regulation, Enzymologic</topic><topic>Gene Expression Regulation, Plant</topic><topic>genes</topic><topic>Genes, Plant</topic><topic>Germination</topic><topic>green fluorescent protein</topic><topic>hydrolysis</topic><topic>jojoba</topic><topic>leaves</topic><topic>Magnoliopsida - enzymology</topic><topic>Magnoliopsida - genetics</topic><topic>Nicotiana - enzymology</topic><topic>Nicotiana - genetics</topic><topic>Nicotiana tabacum</topic><topic>Oxidation</topic><topic>Oxidation-Reduction</topic><topic>Plant Leaves - enzymology</topic><topic>Plant Leaves - genetics</topic><topic>Plant physiology and development</topic><topic>Plants, Genetically Modified - enzymology</topic><topic>Plants, Genetically Modified - genetics</topic><topic>Proteins</topic><topic>proteomics</topic><topic>Proteomics - methods</topic><topic>Recombinant Fusion Proteins - genetics</topic><topic>Recombinant Fusion Proteins - metabolism</topic><topic>seed germination</topic><topic>seed storage</topic><topic>Seedlings</topic><topic>Seeds - genetics</topic><topic>Seeds - metabolism</topic><topic>Simmondsia chinensis</topic><topic>tissues</topic><topic>tobacco</topic><topic>wax esters</topic><topic>Waxes</topic><topic>Waxes - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Rajangam, Alex S.</creatorcontrib><creatorcontrib>Gidda, Satinder K.</creatorcontrib><creatorcontrib>Craddock, Christian</creatorcontrib><creatorcontrib>Mullen, Robert T.</creatorcontrib><creatorcontrib>Dyer, John M.</creatorcontrib><creatorcontrib>Eastmond, Peter J.</creatorcontrib><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>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - 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>Rajangam, Alex S.</au><au>Gidda, Satinder K.</au><au>Craddock, Christian</au><au>Mullen, Robert T.</au><au>Dyer, John M.</au><au>Eastmond, Peter J.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Molecular Characterization of the Fatty Alcohol Oxidation Pathway for Wax-Ester Mobilization in Germinated Jojoba Seeds</atitle><jtitle>Plant physiology (Bethesda)</jtitle><addtitle>Plant Physiol</addtitle><date>2013-01-01</date><risdate>2013</risdate><volume>161</volume><issue>1</issue><spage>72</spage><epage>80</epage><pages>72-80</pages><issn>0032-0889</issn><issn>1532-2548</issn><eissn>1532-2548</eissn><coden>PPHYA5</coden><abstract>Jojoba (Simmondsia chinensis) is the only plant species known to use liquid wax esters (WEs) as a primary seed storage reserve. Upon germination, WE hydrolysis releases very-long-chain fatty alcohols, which must be oxidized to fatty adds by the sequential action of a fatty alcohol oxidase (FAO) and a fatty aldehyde dehydrogenase (FADH) before they can be β-oxidized. Here, we describe the cloning and characterization of genes for each of these two activities. Jojoba FAO and FADH are 52% and 68% identical to Arabidopsis (Arabidopsis thaliana ) FAO3 and ALDH3H1, respectively. The genes are expressed most strongly in the cotyledons of jojoba seedlings following germination, but transcripts can also be detected in vegetative tissues. Proteomic analysis indicated that the FAO and FADH proteins can be detected on wax bodies, but they localized to the endoplasmic reticulum when they were expressed as amino-terminal green fluorescent protein fusions in tobacco (Nicotiana tabacum) leaves. Recombinant jojoba FAO and FADH proteins are active on very-long-chain fatty alcohol and fatty aldehyde substrates, respectively, and have biochemical properties consistent with those previously reported in jojoba cotyledons. Coexpression of jojoba FAO and FADH in Arabidopsis enhanced the in vivo rate of fatty alcohol oxidation more than 4-fold. Taken together, our data suggest that jojoba FAO and FADH constitute the very-long-chain fatty alcohol oxidation pathway that is likely to be necessary for efficient WE mobilization following seed germination.</abstract><cop>Rockville, MD</cop><pub>American Society of Plant Biologists</pub><pmid>23166353</pmid><doi>10.1104/pp.112.208264</doi><tpages>9</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | alcohol oxidase Alcohol Oxidoreductases - genetics Alcohol Oxidoreductases - metabolism aldehyde dehydrogenase Aldehyde Oxidoreductases - metabolism Aldehydes Arabidopsis - enzymology Arabidopsis - genetics Arabidopsis thaliana BIOCHEMISTRY AND METABOLISM Biological and medical sciences Cloning, Molecular Cotyledon - genetics Cotyledon - metabolism Cotyledons endoplasmic reticulum Endoplasmic Reticulum - metabolism Enzyme Activation Enzymes Epidermal cells Esters - metabolism Fatty acids Fatty alcohols Fatty Alcohols - metabolism Food and Agriculture Organization Fundamental and applied biological sciences. Psychology gene expression Gene Expression Regulation, Enzymologic Gene Expression Regulation, Plant genes Genes, Plant Germination green fluorescent protein hydrolysis jojoba leaves Magnoliopsida - enzymology Magnoliopsida - genetics Nicotiana - enzymology Nicotiana - genetics Nicotiana tabacum Oxidation Oxidation-Reduction Plant Leaves - enzymology Plant Leaves - genetics Plant physiology and development Plants, Genetically Modified - enzymology Plants, Genetically Modified - genetics Proteins proteomics Proteomics - methods Recombinant Fusion Proteins - genetics Recombinant Fusion Proteins - metabolism seed germination seed storage Seedlings Seeds - genetics Seeds - metabolism Simmondsia chinensis tissues tobacco wax esters Waxes Waxes - metabolism |
| title | Molecular Characterization of the Fatty Alcohol Oxidation Pathway for Wax-Ester Mobilization in Germinated Jojoba Seeds |
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