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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Main Authors: Mareike Bongers, Jordi Perez-Gil, Mark P Hodson, Lars Schrübbers, Tune Wulff, Morten OA Sommer, Lars K Nielsen, Claudia E Vickers
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2020-03-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/48685
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author Mareike Bongers
Jordi Perez-Gil
Mark P Hodson
Lars Schrübbers
Tune Wulff
Morten OA Sommer
Lars K Nielsen
Claudia E Vickers
author_facet Mareike Bongers
Jordi Perez-Gil
Mark P Hodson
Lars Schrübbers
Tune Wulff
Morten OA Sommer
Lars K Nielsen
Claudia E Vickers
author_sort Mareike Bongers
collection DOAJ
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.
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spelling doaj.art-3da291e036554f8f9d8e3953b74937f22022-12-22T03:24:36ZengeLife Sciences Publications LtdeLife2050-084X2020-03-01910.7554/eLife.48685Adaptation of hydroxymethylbutenyl diphosphate reductase enables volatile isoprenoid productionMareike Bongers0https://orcid.org/0000-0003-4739-3852Jordi Perez-Gil1https://orcid.org/0000-0002-5632-9556Mark P Hodson2https://orcid.org/0000-0002-5436-1886Lars Schrübbers3Tune Wulff4https://orcid.org/0000-0002-8822-1048Morten OA Sommer5Lars K Nielsen6https://orcid.org/0000-0001-8191-3511Claudia E Vickers7https://orcid.org/0000-0002-0792-050XNovo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, Lyngby, Denmark; Australian Institute for Bioengineering and Nanotechnology, The University of Queensland, Brisbane, AustraliaAustralian Institute for Bioengineering and Nanotechnology, The University of Queensland, Brisbane, Australia; Centre for Research in Agricultural Genomics (CRAG) CSIC-IRTA-UAB-UB, Campus UAB Bellaterra, Barcelona, SpainAustralian Institute for Bioengineering and Nanotechnology, The University of Queensland, Brisbane, Australia; Metabolomics Australia, Australian Institute for Bioengineering and Nanotechnology, The University of Queensland, Brisbane, Australia; School of Pharmacy, The University of Queensland, Brisbane, AustraliaNovo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, Lyngby, DenmarkNovo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, Lyngby, DenmarkNovo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, Lyngby, DenmarkNovo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, Lyngby, Denmark; Australian Institute for Bioengineering and Nanotechnology, The University of Queensland, Brisbane, AustraliaAustralian Institute for Bioengineering and Nanotechnology, The University of Queensland, Brisbane, Australia; CSIRO Synthetic Biology Future Science Platform, Brisbane, AustraliaVolatile 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.https://elifesciences.org/articles/48685isoprenoidsBVOCMEP pathwayIsopreneHDRmonoterpenes
spellingShingle Mareike Bongers
Jordi Perez-Gil
Mark P Hodson
Lars Schrübbers
Tune Wulff
Morten OA Sommer
Lars K Nielsen
Claudia E Vickers
Adaptation of hydroxymethylbutenyl diphosphate reductase enables volatile isoprenoid production
eLife
isoprenoids
BVOC
MEP pathway
Isoprene
HDR
monoterpenes
title Adaptation of hydroxymethylbutenyl diphosphate reductase enables volatile isoprenoid production
title_full Adaptation of hydroxymethylbutenyl diphosphate reductase enables volatile isoprenoid production
title_fullStr Adaptation of hydroxymethylbutenyl diphosphate reductase enables volatile isoprenoid production
title_full_unstemmed Adaptation of hydroxymethylbutenyl diphosphate reductase enables volatile isoprenoid production
title_short Adaptation of hydroxymethylbutenyl diphosphate reductase enables volatile isoprenoid production
title_sort adaptation of hydroxymethylbutenyl diphosphate reductase enables volatile isoprenoid production
topic isoprenoids
BVOC
MEP pathway
Isoprene
HDR
monoterpenes
url https://elifesciences.org/articles/48685
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