Adaptation of hydroxymethylbutenyl diphosphate reductase enables volatile isoprenoid production
Volatile isoprenoids produced by plants are emitted in vast quantities into the atmosphere, with substantial effects on global carbon cycling. Yet, the molecular mechanisms regulating the balance between volatile and non-volatile isoprenoid production remain unknown. Isoprenoids are synthesised via...
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description | Volatile isoprenoids produced by plants are emitted in vast quantities into the atmosphere, with substantial effects on global carbon cycling. Yet, the molecular mechanisms regulating the balance between volatile and non-volatile isoprenoid production remain unknown. Isoprenoids are synthesised via sequential condensation of isopentenyl pyrophosphate (IPP) to dimethylallyl pyrophosphate (DMAPP), with volatile isoprenoids containing fewer isopentenyl subunits. The DMAPP:IPP ratio could affect the balance between volatile and non-volatile isoprenoids, but the plastidic DMAPP:IPP ratio is generally believed to be similar across different species. Here we demonstrate that the ratio of DMAPP:IPP produced by hydroxymethylbutenyl diphosphate reductase (HDR/IspH), the final step of the plastidic isoprenoid production pathway, is not fixed. Instead, this ratio varies greatly across HDRs from phylogenetically distinct plants, correlating with isoprenoid production patterns. Our findings suggest that adaptation of HDR plays a previously unrecognised role in determining in vivo carbon availability for isoprenoid emissions, directly shaping global biosphere-atmosphere interactions. |
doi_str_mv | 10.7554/eLife.48685 |
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A. ; Nielsen, Lars K. ; Vickers, Claudia E.</creator><creatorcontrib>Bongers, Mareike ; Perez-Gil, Jordi ; Hodson, Mark P. ; Schrubbers, Lars ; Wulff, Tune ; Sommer, Morten O. A. ; Nielsen, Lars K. ; Vickers, Claudia E.</creatorcontrib><description>Volatile isoprenoids produced by plants are emitted in vast quantities into the atmosphere, with substantial effects on global carbon cycling. Yet, the molecular mechanisms regulating the balance between volatile and non-volatile isoprenoid production remain unknown. Isoprenoids are synthesised via sequential condensation of isopentenyl pyrophosphate (IPP) to dimethylallyl pyrophosphate (DMAPP), with volatile isoprenoids containing fewer isopentenyl subunits. The DMAPP:IPP ratio could affect the balance between volatile and non-volatile isoprenoids, but the plastidic DMAPP:IPP ratio is generally believed to be similar across different species. Here we demonstrate that the ratio of DMAPP:IPP produced by hydroxymethylbutenyl diphosphate reductase (HDR/IspH), the final step of the plastidic isoprenoid production pathway, is not fixed. Instead, this ratio varies greatly across HDRs from phylogenetically distinct plants, correlating with isoprenoid production patterns. Our findings suggest that adaptation of HDR plays a previously unrecognised role in determining in vivo carbon availability for isoprenoid emissions, directly shaping global biosphere-atmosphere interactions.</description><identifier>ISSN: 2050-084X</identifier><identifier>EISSN: 2050-084X</identifier><identifier>DOI: 10.7554/eLife.48685</identifier><identifier>PMID: 32163032</identifier><language>eng</language><publisher>CAMBRIDGE: Elife Sciences Publications Ltd</publisher><subject>Acclimatization ; Air pollution ; Atmosphere ; Biochemistry and Chemical Biology ; Biology ; Biosphere ; BVOC ; Carbon ; Carbon cycle ; Climate change ; Competition ; E coli ; Emissions ; Enzymes ; Flowers & plants ; Gene Knockdown Techniques ; Genes ; HDR ; Isoprene ; isoprenoids ; Life Sciences & Biomedicine ; Life Sciences & Biomedicine - Other Topics ; MEP pathway ; Metabolic Networks and Pathways ; Metabolism ; Metabolites ; Metabolomics - methods ; Molecular modelling ; monoterpenes ; Oxidoreductases - genetics ; Oxidoreductases - metabolism ; Phylogeny ; Plant Biology ; Plants - classification ; Plants - genetics ; Plants - metabolism ; Proteomics - methods ; Ratios ; Reductase ; Science & Technology ; Short Report ; Terpenes ; Terpenes - metabolism ; VOCs ; Volatile organic compounds ; Volatile Organic Compounds - metabolism</subject><ispartof>eLife, 2020-03, Vol.9, Article 48685</ispartof><rights>2020, Bongers et al.</rights><rights>2020, Bongers et al. 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A.</creatorcontrib><creatorcontrib>Nielsen, Lars K.</creatorcontrib><creatorcontrib>Vickers, Claudia E.</creatorcontrib><title>Adaptation of hydroxymethylbutenyl diphosphate reductase enables volatile isoprenoid production</title><title>eLife</title><addtitle>ELIFE</addtitle><addtitle>Elife</addtitle><description>Volatile isoprenoids produced by plants are emitted in vast quantities into the atmosphere, with substantial effects on global carbon cycling. Yet, the molecular mechanisms regulating the balance between volatile and non-volatile isoprenoid production remain unknown. Isoprenoids are synthesised via sequential condensation of isopentenyl pyrophosphate (IPP) to dimethylallyl pyrophosphate (DMAPP), with volatile isoprenoids containing fewer isopentenyl subunits. The DMAPP:IPP ratio could affect the balance between volatile and non-volatile isoprenoids, but the plastidic DMAPP:IPP ratio is generally believed to be similar across different species. Here we demonstrate that the ratio of DMAPP:IPP produced by hydroxymethylbutenyl diphosphate reductase (HDR/IspH), the final step of the plastidic isoprenoid production pathway, is not fixed. Instead, this ratio varies greatly across HDRs from phylogenetically distinct plants, correlating with isoprenoid production patterns. Our findings suggest that adaptation of HDR plays a previously unrecognised role in determining in vivo carbon availability for isoprenoid emissions, directly shaping global biosphere-atmosphere interactions.</description><subject>Acclimatization</subject><subject>Air pollution</subject><subject>Atmosphere</subject><subject>Biochemistry and Chemical Biology</subject><subject>Biology</subject><subject>Biosphere</subject><subject>BVOC</subject><subject>Carbon</subject><subject>Carbon cycle</subject><subject>Climate change</subject><subject>Competition</subject><subject>E coli</subject><subject>Emissions</subject><subject>Enzymes</subject><subject>Flowers & plants</subject><subject>Gene Knockdown Techniques</subject><subject>Genes</subject><subject>HDR</subject><subject>Isoprene</subject><subject>isoprenoids</subject><subject>Life Sciences & Biomedicine</subject><subject>Life Sciences & Biomedicine - Other Topics</subject><subject>MEP pathway</subject><subject>Metabolic Networks and Pathways</subject><subject>Metabolism</subject><subject>Metabolites</subject><subject>Metabolomics - methods</subject><subject>Molecular modelling</subject><subject>monoterpenes</subject><subject>Oxidoreductases - genetics</subject><subject>Oxidoreductases - metabolism</subject><subject>Phylogeny</subject><subject>Plant Biology</subject><subject>Plants - classification</subject><subject>Plants - genetics</subject><subject>Plants - metabolism</subject><subject>Proteomics - methods</subject><subject>Ratios</subject><subject>Reductase</subject><subject>Science & Technology</subject><subject>Short Report</subject><subject>Terpenes</subject><subject>Terpenes - metabolism</subject><subject>VOCs</subject><subject>Volatile organic compounds</subject><subject>Volatile Organic Compounds - metabolism</subject><issn>2050-084X</issn><issn>2050-084X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>AOWDO</sourceid><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNks1vFCEYhydGY5vak3cziRcTsxWG74tJs_GjySZeNPFGGHinw2Z2GIGpzn8vu1vX1pNcIPDw8AK_qnqJ0ZVgjL6Dje_gikou2ZPqvEEMrZCk358-GJ9VlyltUWmCSonV8-qMNJgTRJrzSl87M2WTfRjr0NX94mL4tewg98vQzhnGZaidn_qQpt5kqCO42WaToIbRtAOk-i4MZfsAtU9hijAG7-ophj1WpC-qZ50ZElze9xfVt48fvq4_rzZfPt2srzcrSwXLKwOKNZZb5KhFSgC2SrZGMCPLVLmns03XStRxRJACZ7gqV3DcKmQRgpaRi-rm6HXBbPUU_c7ERQfj9WEixFttYvZ2AE2caRQGRHgRd7JTTgJRjLSCKiK6prjeH13T3O7AWRhzNMMj6eOV0ff6NtxpgbhgfF_Mm3tBDD9mSFnvfLIwDGaEMCfdEMEFoZjuz3r9D7oNcxzLUxVKUkGZakSh3h4pG0NKEbpTMRjpfQ70IQf6kINCv3pY_4n98-t_dT-hDV2yHkYLJ6wEhWGlKBb7zOBCy_-n1_4YpnWYx0x-A9LA0ak</recordid><startdate>20200312</startdate><enddate>20200312</enddate><creator>Bongers, Mareike</creator><creator>Perez-Gil, Jordi</creator><creator>Hodson, Mark P.</creator><creator>Schrubbers, Lars</creator><creator>Wulff, Tune</creator><creator>Sommer, Morten O. 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A.</au><au>Nielsen, Lars K.</au><au>Vickers, Claudia E.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Adaptation of hydroxymethylbutenyl diphosphate reductase enables volatile isoprenoid production</atitle><jtitle>eLife</jtitle><stitle>ELIFE</stitle><addtitle>Elife</addtitle><date>2020-03-12</date><risdate>2020</risdate><volume>9</volume><artnum>48685</artnum><issn>2050-084X</issn><eissn>2050-084X</eissn><abstract>Volatile isoprenoids produced by plants are emitted in vast quantities into the atmosphere, with substantial effects on global carbon cycling. Yet, the molecular mechanisms regulating the balance between volatile and non-volatile isoprenoid production remain unknown. Isoprenoids are synthesised via sequential condensation of isopentenyl pyrophosphate (IPP) to dimethylallyl pyrophosphate (DMAPP), with volatile isoprenoids containing fewer isopentenyl subunits. The DMAPP:IPP ratio could affect the balance between volatile and non-volatile isoprenoids, but the plastidic DMAPP:IPP ratio is generally believed to be similar across different species. Here we demonstrate that the ratio of DMAPP:IPP produced by hydroxymethylbutenyl diphosphate reductase (HDR/IspH), the final step of the plastidic isoprenoid production pathway, is not fixed. Instead, this ratio varies greatly across HDRs from phylogenetically distinct plants, correlating with isoprenoid production patterns. Our findings suggest that adaptation of HDR plays a previously unrecognised role in determining in vivo carbon availability for isoprenoid emissions, directly shaping global biosphere-atmosphere interactions.</abstract><cop>CAMBRIDGE</cop><pub>Elife Sciences Publications Ltd</pub><pmid>32163032</pmid><doi>10.7554/eLife.48685</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0003-4005-5674</orcidid><orcidid>https://orcid.org/0000-0002-5436-1886</orcidid><orcidid>https://orcid.org/0000-0002-8822-1048</orcidid><orcidid>https://orcid.org/0000-0001-8191-3511</orcidid><orcidid>https://orcid.org/0000-0002-5632-9556</orcidid><orcidid>https://orcid.org/0000-0002-0792-050X</orcidid><orcidid>https://orcid.org/0000-0003-4739-3852</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Acclimatization Air pollution Atmosphere Biochemistry and Chemical Biology Biology Biosphere BVOC Carbon Carbon cycle Climate change Competition E coli Emissions Enzymes Flowers & plants Gene Knockdown Techniques Genes HDR Isoprene isoprenoids Life Sciences & Biomedicine Life Sciences & Biomedicine - Other Topics MEP pathway Metabolic Networks and Pathways Metabolism Metabolites Metabolomics - methods Molecular modelling monoterpenes Oxidoreductases - genetics Oxidoreductases - metabolism Phylogeny Plant Biology Plants - classification Plants - genetics Plants - metabolism Proteomics - methods Ratios Reductase Science & Technology Short Report Terpenes Terpenes - metabolism VOCs Volatile organic compounds Volatile Organic Compounds - metabolism |
title | Adaptation of hydroxymethylbutenyl diphosphate reductase enables volatile isoprenoid production |
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