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Metabolic flux analysis of plastidic isoprenoid biosynthesis in poplar leaves emitting and nonemitting isoprene.
Plant Physiol. 2014 May; 165(1):37-51.PP

Abstract

The plastidic 2-C-methyl-D-erythritol-4-phosphate (MEP) pathway is one of the most important pathways in plants and produces a large variety of essential isoprenoids. Its regulation, however, is still not well understood. Using the stable isotope 13C-labeling technique, we analyzed the carbon fluxes through the MEP pathway and into the major plastidic isoprenoid products in isoprene-emitting and transgenic isoprene-nonemitting (NE) gray poplar (Populus×canescens). We assessed the dependence on temperature, light intensity, and atmospheric [CO2]. Isoprene biosynthesis was by far (99%) the main carbon sink of MEP pathway intermediates in mature gray poplar leaves, and its production required severalfold higher carbon fluxes compared with NE leaves with almost zero isoprene emission. To compensate for the much lower demand for carbon, NE leaves drastically reduced the overall carbon flux within the MEP pathway. Feedback inhibition of 1-deoxy-D-xylulose-5-phosphate synthase activity by accumulated plastidic dimethylallyl diphosphate almost completely explained this reduction in carbon flux. Our data demonstrate that short-term biochemical feedback regulation of 1-deoxy-d-xylulose-5-phosphate synthase activity by plastidic dimethylallyl diphosphate is an important regulatory mechanism of the MEP pathway. Despite being relieved from the large carbon demand of isoprene biosynthesis, NE plants redirected only approximately 0.5% of this saved carbon toward essential nonvolatile isoprenoids, i.e. β-carotene and lutein, most probably to compensate for the absence of isoprene and its antioxidant properties.

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Authors+Show Affiliations

Ghirardo A
Research Unit Environmental Simulation, Institute of Biochemical Plant Pathology, Helmholtz Zentrum München, 85764 Neuherberg, Germany.
Wright LP
No affiliation info available
Bi Z
No affiliation info available
Rosenkranz M
No affiliation info available
Pulido P
No affiliation info available
Rodríguez-Concepción M
No affiliation info available
Niinemets Ü
No affiliation info available
Brüggemann N
No affiliation info available
Gershenzon J
No affiliation info available
Schnitzler JP
No affiliation info available

MeSH

ButadienesCarbonCarbon DioxideCarbon IsotopesDown-RegulationErythritolHemiterpenesIsotope LabelingLightMetabolic Flux AnalysisModels, BiologicalOrganophosphorus CompoundsPentanesPigments, BiologicalPlant LeavesPlastidsPopulusSugar PhosphatesTemperatureTransferases

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

24590857

Citation

Ghirardo, Andrea, et al. "Metabolic Flux Analysis of Plastidic Isoprenoid Biosynthesis in Poplar Leaves Emitting and Nonemitting Isoprene." Plant Physiology, vol. 165, no. 1, 2014, pp. 37-51.
Ghirardo A, Wright LP, Bi Z, et al. Metabolic flux analysis of plastidic isoprenoid biosynthesis in poplar leaves emitting and nonemitting isoprene. Plant Physiol. 2014;165(1):37-51.
Ghirardo, A., Wright, L. P., Bi, Z., Rosenkranz, M., Pulido, P., Rodríguez-Concepción, M., Niinemets, Ü., Brüggemann, N., Gershenzon, J., & Schnitzler, J. P. (2014). Metabolic flux analysis of plastidic isoprenoid biosynthesis in poplar leaves emitting and nonemitting isoprene. Plant Physiology, 165(1), 37-51. https://doi.org/10.1104/pp.114.236018
Ghirardo A, et al. Metabolic Flux Analysis of Plastidic Isoprenoid Biosynthesis in Poplar Leaves Emitting and Nonemitting Isoprene. Plant Physiol. 2014;165(1):37-51. PubMed PMID: 24590857.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Metabolic flux analysis of plastidic isoprenoid biosynthesis in poplar leaves emitting and nonemitting isoprene. AU - Ghirardo,Andrea, AU - Wright,Louwrance Peter, AU - Bi,Zhen, AU - Rosenkranz,Maaria, AU - Pulido,Pablo, AU - Rodríguez-Concepción,Manuel, AU - Niinemets,Ülo, AU - Brüggemann,Nicolas, AU - Gershenzon,Jonathan, AU - Schnitzler,Jörg-Peter, Y1 - 2014/03/03/ PY - 2014/3/5/entrez PY - 2014/3/5/pubmed PY - 2014/12/23/medline SP - 37 EP - 51 JF - Plant physiology JO - Plant Physiol VL - 165 IS - 1 N2 - The plastidic 2-C-methyl-D-erythritol-4-phosphate (MEP) pathway is one of the most important pathways in plants and produces a large variety of essential isoprenoids. Its regulation, however, is still not well understood. Using the stable isotope 13C-labeling technique, we analyzed the carbon fluxes through the MEP pathway and into the major plastidic isoprenoid products in isoprene-emitting and transgenic isoprene-nonemitting (NE) gray poplar (Populus×canescens). We assessed the dependence on temperature, light intensity, and atmospheric [CO2]. Isoprene biosynthesis was by far (99%) the main carbon sink of MEP pathway intermediates in mature gray poplar leaves, and its production required severalfold higher carbon fluxes compared with NE leaves with almost zero isoprene emission. To compensate for the much lower demand for carbon, NE leaves drastically reduced the overall carbon flux within the MEP pathway. Feedback inhibition of 1-deoxy-D-xylulose-5-phosphate synthase activity by accumulated plastidic dimethylallyl diphosphate almost completely explained this reduction in carbon flux. Our data demonstrate that short-term biochemical feedback regulation of 1-deoxy-d-xylulose-5-phosphate synthase activity by plastidic dimethylallyl diphosphate is an important regulatory mechanism of the MEP pathway. Despite being relieved from the large carbon demand of isoprene biosynthesis, NE plants redirected only approximately 0.5% of this saved carbon toward essential nonvolatile isoprenoids, i.e. β-carotene and lutein, most probably to compensate for the absence of isoprene and its antioxidant properties. SN - 1532-2548 UR - https://www.unboundmedicine.com/medline/citation/24590857/Metabolic_flux_analysis_of_plastidic_isoprenoid_biosynthesis_in_poplar_leaves_emitting_and_nonemitting_isoprene_ DB - PRIME DP - Unbound Medicine ER -