A Novel 2-Oxoacid-Dependent Dioxygenase Involved in the Formation of the Goiterogenic 2-Hydroxybut-3-enyl Glucosinolate and Generalist Insect Resistance in Arabidopsis
Glucosinolates are secondary metabolites found almost exclusively in the order Brassicales. They are synthesized from a variety of amino acids and can have numerous side chain modifications that control biological function. We investigated the biosynthesis of 2-hydroxybut-3-enyl glucosinolate, which...
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| Veröffentlicht in: | Plant physiology (Bethesda) 2008-12, Vol.148 (4), p.2096-2108 |
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| creator | Hansen, Bjarne G. Kerwin, Rachel E. Ober, James A. Lambrix, Virginia M. Mitchell-Olds, Thomas Gershenzon, Jonathan Halkier, Barbara A. Kliebenstein, Daniel J. |
| description | Glucosinolates are secondary metabolites found almost exclusively in the order Brassicales. They are synthesized from a variety of amino acids and can have numerous side chain modifications that control biological function. We investigated the biosynthesis of 2-hydroxybut-3-enyl glucosinolate, which has biological activities including toxicity to Caenorhabditis elegans, inhibition of seed germination, induction of goiter disease in mammals, and production of bitter flavors in Brassica vegetable crops. Arabidopsis (Arabidopsis thaliana) accessions contain three different patterns of 2-hydroxybut-3-enyl glucosinolate accumulation (present in leaves and seeds, seeds only, or absent) corresponding to three different alleles at a single locus, GSL-OH. Fine-scale mapping of the GSL-OH locus identified a 2-oxoacid-dependent dioxygenase encoded by At2g25450 required for the formation of both 2R- and 2S-2-hydroxybut-3-enyl glucosinolate from the precursor 3-butenyl glucosinolate precursor. Naturally occurring null mutations and T-DNA insertional mutations in At2g25450 exhibit a complete absence of 2-hydroxybut-3-enyl glucosinolate accumulation. Analysis of herbivory by the generalist lepidopteran Trichoplusia ni showed that production of 2-hydroxybut-3-enyl glucosinolate provides increased resistance. These results show that At2g25450 is necessary for the hydroxylation of but-3-enyl glucosinolate to 2-hydroxybut-3-enyl glucosinolate in planta and that this metabolite increases resistance to generalist herbivory. |
| doi_str_mv | 10.1104/pp.108.129981 |
| format | Article |
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They are synthesized from a variety of amino acids and can have numerous side chain modifications that control biological function. We investigated the biosynthesis of 2-hydroxybut-3-enyl glucosinolate, which has biological activities including toxicity to Caenorhabditis elegans, inhibition of seed germination, induction of goiter disease in mammals, and production of bitter flavors in Brassica vegetable crops. Arabidopsis (Arabidopsis thaliana) accessions contain three different patterns of 2-hydroxybut-3-enyl glucosinolate accumulation (present in leaves and seeds, seeds only, or absent) corresponding to three different alleles at a single locus, GSL-OH. Fine-scale mapping of the GSL-OH locus identified a 2-oxoacid-dependent dioxygenase encoded by At2g25450 required for the formation of both 2R- and 2S-2-hydroxybut-3-enyl glucosinolate from the precursor 3-butenyl glucosinolate precursor. Naturally occurring null mutations and T-DNA insertional mutations in At2g25450 exhibit a complete absence of 2-hydroxybut-3-enyl glucosinolate accumulation. Analysis of herbivory by the generalist lepidopteran Trichoplusia ni showed that production of 2-hydroxybut-3-enyl glucosinolate provides increased resistance. These results show that At2g25450 is necessary for the hydroxylation of but-3-enyl glucosinolate to 2-hydroxybut-3-enyl glucosinolate in planta and that this metabolite increases resistance to generalist herbivory.</description><identifier>ISSN: 0032-0889</identifier><identifier>ISSN: 1532-2548</identifier><identifier>EISSN: 1532-2548</identifier><identifier>DOI: 10.1104/pp.108.129981</identifier><identifier>PMID: 18945935</identifier><identifier>CODEN: PPHYA5</identifier><language>eng</language><publisher>Rockville, MD: American Society of Plant Biologists</publisher><subject>Agronomy. Soil science and plant productions ; Alleles ; Amino acids ; Animals ; Arabidopsis - enzymology ; Arabidopsis - metabolism ; Arabidopsis - physiology ; Arabidopsis Proteins - chemistry ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - physiology ; Biochemical Processes and Macromolecular Structures ; Biological and medical sciences ; Biosynthesis ; Chromosome Mapping ; Complementary DNA ; Dioxygenases - chemistry ; Dioxygenases - genetics ; Dioxygenases - physiology ; Enzymes ; Feeding Behavior ; Fundamental and applied biological sciences. Psychology ; Genetic loci ; Genetic Variation ; Genetics and breeding of economic plants ; Genotype ; Glucosinolates ; Glucosinolates - biosynthesis ; Herbivores ; Herbivory ; Insecta - physiology ; Metabolites ; Molecular structure ; Moths - physiology ; Mutagenesis, Insertional ; Mutation ; Pest animals ; Pest resistance ; Phytophagous insects ; Plant physiology and development ; Plants ; Promoter Regions, Genetic ; Quantitative trait loci ; Secondary metabolites ; Seed germination ; Seeds ; Sequence Analysis, DNA ; Varietal selection. Specialized plant breeding, plant breeding aims</subject><ispartof>Plant physiology (Bethesda), 2008-12, Vol.148 (4), p.2096-2108</ispartof><rights>Copyright 2008 American Society of Plant Biologists</rights><rights>2009 INIST-CNRS</rights><rights>Copyright American Society of Plant Biologists Dec 2008</rights><rights>Copyright © 2008, American Society of Plant Biologists</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c611t-32159f58c08d1ef3cd61207b8a9507980ccfa0d2f30bdae9b4b82cf66039bce63</citedby><cites>FETCH-LOGICAL-c611t-32159f58c08d1ef3cd61207b8a9507980ccfa0d2f30bdae9b4b82cf66039bce63</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/40066331$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/40066331$$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&idt=20980281$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/18945935$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Hansen, Bjarne G.</creatorcontrib><creatorcontrib>Kerwin, Rachel E.</creatorcontrib><creatorcontrib>Ober, James A.</creatorcontrib><creatorcontrib>Lambrix, Virginia M.</creatorcontrib><creatorcontrib>Mitchell-Olds, Thomas</creatorcontrib><creatorcontrib>Gershenzon, Jonathan</creatorcontrib><creatorcontrib>Halkier, Barbara A.</creatorcontrib><creatorcontrib>Kliebenstein, Daniel J.</creatorcontrib><title>A Novel 2-Oxoacid-Dependent Dioxygenase Involved in the Formation of the Goiterogenic 2-Hydroxybut-3-enyl Glucosinolate and Generalist Insect Resistance in Arabidopsis</title><title>Plant physiology (Bethesda)</title><addtitle>Plant Physiol</addtitle><description>Glucosinolates are secondary metabolites found almost exclusively in the order Brassicales. They are synthesized from a variety of amino acids and can have numerous side chain modifications that control biological function. We investigated the biosynthesis of 2-hydroxybut-3-enyl glucosinolate, which has biological activities including toxicity to Caenorhabditis elegans, inhibition of seed germination, induction of goiter disease in mammals, and production of bitter flavors in Brassica vegetable crops. Arabidopsis (Arabidopsis thaliana) accessions contain three different patterns of 2-hydroxybut-3-enyl glucosinolate accumulation (present in leaves and seeds, seeds only, or absent) corresponding to three different alleles at a single locus, GSL-OH. Fine-scale mapping of the GSL-OH locus identified a 2-oxoacid-dependent dioxygenase encoded by At2g25450 required for the formation of both 2R- and 2S-2-hydroxybut-3-enyl glucosinolate from the precursor 3-butenyl glucosinolate precursor. Naturally occurring null mutations and T-DNA insertional mutations in At2g25450 exhibit a complete absence of 2-hydroxybut-3-enyl glucosinolate accumulation. Analysis of herbivory by the generalist lepidopteran Trichoplusia ni showed that production of 2-hydroxybut-3-enyl glucosinolate provides increased resistance. These results show that At2g25450 is necessary for the hydroxylation of but-3-enyl glucosinolate to 2-hydroxybut-3-enyl glucosinolate in planta and that this metabolite increases resistance to generalist herbivory.</description><subject>Agronomy. Soil science and plant productions</subject><subject>Alleles</subject><subject>Amino acids</subject><subject>Animals</subject><subject>Arabidopsis - enzymology</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis - physiology</subject><subject>Arabidopsis Proteins - chemistry</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - physiology</subject><subject>Biochemical Processes and Macromolecular Structures</subject><subject>Biological and medical sciences</subject><subject>Biosynthesis</subject><subject>Chromosome Mapping</subject><subject>Complementary DNA</subject><subject>Dioxygenases - chemistry</subject><subject>Dioxygenases - genetics</subject><subject>Dioxygenases - physiology</subject><subject>Enzymes</subject><subject>Feeding Behavior</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Genetic loci</subject><subject>Genetic Variation</subject><subject>Genetics and breeding of economic plants</subject><subject>Genotype</subject><subject>Glucosinolates</subject><subject>Glucosinolates - biosynthesis</subject><subject>Herbivores</subject><subject>Herbivory</subject><subject>Insecta - physiology</subject><subject>Metabolites</subject><subject>Molecular structure</subject><subject>Moths - physiology</subject><subject>Mutagenesis, Insertional</subject><subject>Mutation</subject><subject>Pest animals</subject><subject>Pest resistance</subject><subject>Phytophagous insects</subject><subject>Plant physiology and development</subject><subject>Plants</subject><subject>Promoter Regions, Genetic</subject><subject>Quantitative trait loci</subject><subject>Secondary metabolites</subject><subject>Seed germination</subject><subject>Seeds</subject><subject>Sequence Analysis, DNA</subject><subject>Varietal selection. 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Soil science and plant productions</topic><topic>Alleles</topic><topic>Amino acids</topic><topic>Animals</topic><topic>Arabidopsis - enzymology</topic><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis - physiology</topic><topic>Arabidopsis Proteins - chemistry</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - physiology</topic><topic>Biochemical Processes and Macromolecular Structures</topic><topic>Biological and medical sciences</topic><topic>Biosynthesis</topic><topic>Chromosome Mapping</topic><topic>Complementary DNA</topic><topic>Dioxygenases - chemistry</topic><topic>Dioxygenases - genetics</topic><topic>Dioxygenases - physiology</topic><topic>Enzymes</topic><topic>Feeding Behavior</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Genetic loci</topic><topic>Genetic Variation</topic><topic>Genetics and breeding of economic plants</topic><topic>Genotype</topic><topic>Glucosinolates</topic><topic>Glucosinolates - biosynthesis</topic><topic>Herbivores</topic><topic>Herbivory</topic><topic>Insecta - physiology</topic><topic>Metabolites</topic><topic>Molecular structure</topic><topic>Moths - physiology</topic><topic>Mutagenesis, Insertional</topic><topic>Mutation</topic><topic>Pest animals</topic><topic>Pest resistance</topic><topic>Phytophagous insects</topic><topic>Plant physiology and development</topic><topic>Plants</topic><topic>Promoter Regions, Genetic</topic><topic>Quantitative trait loci</topic><topic>Secondary metabolites</topic><topic>Seed germination</topic><topic>Seeds</topic><topic>Sequence Analysis, DNA</topic><topic>Varietal selection. 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They are synthesized from a variety of amino acids and can have numerous side chain modifications that control biological function. We investigated the biosynthesis of 2-hydroxybut-3-enyl glucosinolate, which has biological activities including toxicity to Caenorhabditis elegans, inhibition of seed germination, induction of goiter disease in mammals, and production of bitter flavors in Brassica vegetable crops. Arabidopsis (Arabidopsis thaliana) accessions contain three different patterns of 2-hydroxybut-3-enyl glucosinolate accumulation (present in leaves and seeds, seeds only, or absent) corresponding to three different alleles at a single locus, GSL-OH. Fine-scale mapping of the GSL-OH locus identified a 2-oxoacid-dependent dioxygenase encoded by At2g25450 required for the formation of both 2R- and 2S-2-hydroxybut-3-enyl glucosinolate from the precursor 3-butenyl glucosinolate precursor. Naturally occurring null mutations and T-DNA insertional mutations in At2g25450 exhibit a complete absence of 2-hydroxybut-3-enyl glucosinolate accumulation. Analysis of herbivory by the generalist lepidopteran Trichoplusia ni showed that production of 2-hydroxybut-3-enyl glucosinolate provides increased resistance. These results show that At2g25450 is necessary for the hydroxylation of but-3-enyl glucosinolate to 2-hydroxybut-3-enyl glucosinolate in planta and that this metabolite increases resistance to generalist herbivory.</abstract><cop>Rockville, MD</cop><pub>American Society of Plant Biologists</pub><pmid>18945935</pmid><doi>10.1104/pp.108.129981</doi><tpages>13</tpages><oa>free_for_read</oa></addata></record> |
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| identifier | ISSN: 0032-0889 |
| ispartof | Plant physiology (Bethesda), 2008-12, Vol.148 (4), p.2096-2108 |
| issn | 0032-0889 1532-2548 1532-2548 |
| language | eng |
| recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_2593654 |
| source | Jstor Complete Legacy; Oxford University Press Journals All Titles (1996-Current); MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals |
| subjects | Agronomy. Soil science and plant productions Alleles Amino acids Animals Arabidopsis - enzymology Arabidopsis - metabolism Arabidopsis - physiology Arabidopsis Proteins - chemistry Arabidopsis Proteins - genetics Arabidopsis Proteins - physiology Biochemical Processes and Macromolecular Structures Biological and medical sciences Biosynthesis Chromosome Mapping Complementary DNA Dioxygenases - chemistry Dioxygenases - genetics Dioxygenases - physiology Enzymes Feeding Behavior Fundamental and applied biological sciences. Psychology Genetic loci Genetic Variation Genetics and breeding of economic plants Genotype Glucosinolates Glucosinolates - biosynthesis Herbivores Herbivory Insecta - physiology Metabolites Molecular structure Moths - physiology Mutagenesis, Insertional Mutation Pest animals Pest resistance Phytophagous insects Plant physiology and development Plants Promoter Regions, Genetic Quantitative trait loci Secondary metabolites Seed germination Seeds Sequence Analysis, DNA Varietal selection. Specialized plant breeding, plant breeding aims |
| title | A Novel 2-Oxoacid-Dependent Dioxygenase Involved in the Formation of the Goiterogenic 2-Hydroxybut-3-enyl Glucosinolate and Generalist Insect Resistance in Arabidopsis |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-20T19%3A54%3A33IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-jstor_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=A%20Novel%202-Oxoacid-Dependent%20Dioxygenase%20Involved%20in%20the%20Formation%20of%20the%20Goiterogenic%202-Hydroxybut-3-enyl%20Glucosinolate%20and%20Generalist%20Insect%20Resistance%20in%20Arabidopsis&rft.jtitle=Plant%20physiology%20(Bethesda)&rft.au=Hansen,%20Bjarne%20G.&rft.date=2008-12-01&rft.volume=148&rft.issue=4&rft.spage=2096&rft.epage=2108&rft.pages=2096-2108&rft.issn=0032-0889&rft.eissn=1532-2548&rft.coden=PPHYA5&rft_id=info:doi/10.1104/pp.108.129981&rft_dat=%3Cjstor_pubme%3E40066331%3C/jstor_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=218623954&rft_id=info:pmid/18945935&rft_jstor_id=40066331&rfr_iscdi=true |