Quantitative assessment of crosstalk between the two isoprenoid biosynthesis pathways in plants by NMR spectroscopy

Schuhr, Christoph A.; Radykewicz, Tanja; Sagner, Silvia; Latzel, Christoph; Zenk, Meinhart H.; Arigoni, D.; Bacher, Adelbert; Rohdich, Felix; Eisenreich, Wolfgang

doi:10.1023/b:phyt.0000004180.25066.62

Cited by 136 publications

(80 citation statements)

References 31 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Several published studies support the hypothesis that IPP, GPP, and GGPP are transported between the cytosolic and plastidial compartments, with a preference for transport from the plastid to the cytosol (Hemmerlin et al, 2003;Skorupinska-Tudek et al, 2008). This observation corroborates in vivo observations (Kasahara et al, 2002(Kasahara et al, , 2004Laule et al, 2003;Sakakibara et al, 2005) with inhibitor-treated Arabidopsis seedlings, cell cultures of Madagascar periwinkle (Catharanthus roseus) (Schuhr et al, 2003), and BY-2 cells (Hemmerlin et al, 2003). However, in the two latter studies, exogenous MVA was, to some extent, incorporated into plastids and used to produce plastidial isoprenoids.…”

Section: Discussionsupporting

confidence: 75%

The Plastidial 2-C-Methyl-d-Erythritol 4-Phosphate Pathway Provides the Isoprenyl Moiety for Protein Geranylgeranylation in Tobacco BY-2 Cells

et al. 2009

View full text Add to dashboard Cite

Protein farnesylation and geranylgeranylation are important posttranslational modifications in eukaryotic cells. We visualized in transformed Nicotiana tabacum Bright Yellow-2 (BY-2) cells the geranylgeranylation and plasma membrane localization of GFP-BD-CVIL, which consists of green fluorescent protein (GFP) fused to the C-terminal polybasic domain (BD) and CVIL isoprenylation motif from the Oryza sativa calmodulin, CaM61. Treatment with fosmidomycin (Fos) or oxoclomazone (OC), inhibitors of the plastidial 2-C-methyl-D-erythritol 4-phosphate (MEP) pathway, caused mislocalization of the protein to the nucleus, whereas treatment with mevinolin, an inhibitor of the cytosolic mevalonate pathway, did not. The nuclear localization of GFP-BD-CVIL in the presence of MEP pathway inhibitors was completely reversed by all-transgeranylgeraniol (GGol). Furthermore, 1-deoxy-D-xylulose (DX) reversed the effects of OC, but not Fos, consistent with the hypothesis that OC blocks 1-deoxy-D-xylulose 5-phosphate synthesis, whereas Fos inhibits its conversion to 2-C-methyl-Derythritol 4-phosphate. By contrast, GGol and DX did not rescue the nuclear mislocalization of GFP-BD-CVIL in the presence of a protein geranylgeranyltransferase type 1 inhibitor. Thus, the MEP pathway has an essential role in geranylgeranyl diphosphate (GGPP) biosynthesis and protein geranylgeranylation in BY-2 cells. GFP-BD-CVIL is a versatile tool for identifying pharmaceuticals and herbicides that interfere either with GGPP biosynthesis or with protein geranylgeranylation.

show abstract

Section: Discussionsupporting

confidence: 75%

The Plastidial 2-C-Methyl-d-Erythritol 4-Phosphate Pathway Provides the Isoprenyl Moiety for Protein Geranylgeranylation in Tobacco BY-2 Cells

et al. 2009

View full text Add to dashboard Cite

show abstract

“…8C). The fact that some reduction was observed in the emission of (E,E)-a-farnesene by treatment of Col-0 with fosmidomycin and in the emission of (E)-b-ocimene upon treatment of Ws with lovastatin can be attributed to an exchange of terpenoid precursors between the cytosol and plastid, as described previously (Hemmerlin et al, 2003;Laule et al, 2003;Schuhr et al, 2003;Dudareva et al, 2005). Overall, our results are in agreement with the biosynthesis of (E)-b-ocimene and (E,E)-a-farnesene by Ws TPS02 in plastids and the formation of (E, E)-a-farnesene by the Col-0 TPS03 enzyme in the cytosol.…”

Section: Recombinant Tps02 and Tps03 Proteins Both Produce (E)-b-ocimsupporting

confidence: 69%

“…The presence of plastidial FPP was also inferred when a strawberry (Fragaria species) linalool/nerolidol synthase carrying a plastid-targeting peptide was expressed in Arabidopsis, causing the emission of a small amount of the sesquiterpene nerolidol together with linalool (Aharoni et al, 2003). A plastidial FPP pool might be the result of an import of FPP from the cytosol as a result of metabolic cross talk between both compartments (Schuhr et al, 2003) and/or the biosynthesis of FPP inside the organelle. The latter explanation is supported by the lower emission of (E,E)-a-farnesene in the presence of fosmidomycin, an inhibitor of the plastid-localized MEP pathway, than after treatment with lovastatin, an inhibitor of the cytosol-localized mevalonate pathway (Fig.…”

Section: Subcellular Compartmentalization Of the Tps02 And Tps03 Protmentioning

confidence: 99%

Variation of Herbivore-Induced Volatile Terpenes among Arabidopsis Ecotypes Depends on Allelic Differences and Subcellular Targeting of Two Terpene Synthases, TPS02 and TPS03

et al. 2010

View full text Add to dashboard Cite

When attacked by insects, plants release mixtures of volatile compounds that are beneficial for direct or indirect defense. Natural variation of volatile emissions frequently occurs between and within plant species, but knowledge of the underlying molecular mechanisms is limited. We investigated intraspecific differences of volatile emissions induced from rosette leaves of 27 accessions of Arabidopsis (Arabidopsis thaliana) upon treatment with coronalon, a jasmonate mimic eliciting responses similar to those caused by insect feeding. Quantitative variation was found for the emission of the monoterpene (E)-b-ocimene, the sesquiterpene (E,E)-a-farnesene, the irregular homoterpene 4,8,12-trimethyltridecatetra-1,3,7,11-ene, and the benzenoid compound methyl salicylate. Differences in the relative emissions of (E)-b-ocimene and (E,E)-a-farnesene from accession Wassilewskija (Ws), a high-(E)-b-ocimene emitter, and accession Columbia (Col-0), a trace-(E)-b-ocimene emitter, were attributed to allelic variation of two closely related, tandem-duplicated terpene synthase genes, TPS02 and TPS03. The Ws genome contains a functional allele of TPS02 but not of TPS03, while the opposite is the case for Col-0. Recombinant proteins of the functional Ws TPS02 and Col-0 TPS03 genes both showed (E)-b-ocimene and (E,E)-a-farnesene synthase activities. However, differential subcellular compartmentalization of the two enzymes in plastids and the cytosol was found to be responsible for the ecotype-specific differences in (E)-b-ocimene/(E,E)-a-farnesene emission. Expression of the functional TPS02 and TPS03 alleles is induced in leaves by elicitor and insect treatment and occurs constitutively in floral tissues. Our studies show that both pseudogenization in the TPS family and subcellular segregation of functional TPS enzymes control the variation and plasticity of induced volatile emissions in wild plant species.

show abstract

“…The concomitant modulation of the activity of the MVA and MEP pathways is a subject of extensive studies; the rate of precursor exchange may reach 100% and 80% from the plastids to the cytoplasm and vice versa (Hemmerlin and Bach, 2000;Schuhr et al, 2003), although these values were observed upon inhibitor treatment. Various intermediates (e.g.…”

Section: Discussionmentioning

confidence: 99%

Modeling of Dolichol Mass Spectra Isotopic Envelopes as a Tool to Monitor Isoprenoid Biosynthesis

et al. 2017

View full text Add to dashboard Cite

The cooperation of the mevalonate (MVA) and methylerythritol phosphate (MEP) pathways, operating in parallel in plants to generate isoprenoid precursors, has been studied extensively. Elucidation of the isoprenoid metabolic pathways is indispensable for the rational design of plant and microbial systems for the production of industrially valuable terpenoids. Here, we describe a new method, based on numerical modeling of mass spectra of metabolically labeled dolichols (Dols), designed to quantitatively follow the cooperation of MVA and MEP reprogrammed upon osmotic stress (sorbitol treatment) in Arabidopsis (Arabidopsis thaliana). The contribution of the MEP pathway increased significantly (reaching 100%) exclusively for the dominating Dols, while for long-chain Dols, the relative input of the MEP and MVA pathways remained unchanged, suggesting divergent sites of synthesis for dominating and long-chain Dols. The analysis of numerically modeled Dol mass spectra is a novel method to follow modulation of the concomitant activity of isoprenoid-generating pathways in plant cells; additionally, it suggests an exchange of isoprenoid intermediates between plastids and peroxisomes.Isopentenyl diphosphate (IPP), the building block of isoprenoids, the most numerous class of secondary metabolites, is derived in plants from two pathways operating in parallel: the cytoplasmic mevalonate (MVA) and the plastidic methylerythritol phosphate (MEP) pathways (Rohmer, 1999;Pulido et al., 2012).Analysis of over 130 isoprenoids has shown that, in angiosperms under standard growth conditions, carotenoids and chlorophyll phytyl chains on the one hand and phytosterols on the other are made nearly exclusively via a single pathway (MEP and MVA, respectively), while numerous other isoprenoids, including dolichols (Dols; Skorupinska-Tudek et al., 2008), are of mixed origin (Hemmerlin et al., 2012).The cooperation of the two pathways (often called cross talk) is considered essential for plant adaptive responses to biotic and abiotic stresses. Consequently, their relative contributions to the formation of IPP are modulated, and the expression of particular genes of the MVA and MEP pathways is frequently correlated with stress (pathogen attack, elicitation, wounding, etc.;Hemmerlin et al., 2012) or plant development (Opitz et al., 2014). Interestingly, the effect of stress on the regulation of the MEP-MVA balance has so far been analyzed only qualitatively.Several methodologies have been employed to unravel the relative contributions of the MVA and MEP pathways to isoprenoids, such as metabolic labeling with isotopically labeled precursors (stable isotopes or radioisotopes were used), followed by structural analysis of the product of interest or blockage of the pathway (chemical, with pathway-specific inhibitors, or genetic), followed by quantification of the isoprenoid intermediates and/or end products. The advantages

show abstract

Quantitative assessment of crosstalk between the two isoprenoid biosynthesis pathways in plants by NMR spectroscopy

Cited by 136 publications

References 31 publications

The Plastidial 2-C-Methyl-d-Erythritol 4-Phosphate Pathway Provides the Isoprenyl Moiety for Protein Geranylgeranylation in Tobacco BY-2 Cells

The Plastidial 2-C-Methyl-d-Erythritol 4-Phosphate Pathway Provides the Isoprenyl Moiety for Protein Geranylgeranylation in Tobacco BY-2 Cells

Variation of Herbivore-Induced Volatile Terpenes among Arabidopsis Ecotypes Depends on Allelic Differences and Subcellular Targeting of Two Terpene Synthases, TPS02 and TPS03

Modeling of Dolichol Mass Spectra Isotopic Envelopes as a Tool to Monitor Isoprenoid Biosynthesis

Contact Info

Product

Resources

About