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Characterization of a Unique Pair of Ferredoxin and Ferredoxin NADP+ Reductase Isoforms That Operates in Non-Photosynthetic Glandular Trichomes

Journal Article · · Plants

Our recent investigations indicated that isoforms of ferredoxin (Fd) and ferredoxin NADP+ reductase (FNR) play essential roles for the reductive steps of the 2C-methyl-D-erythritol 4-phosphate (MEP) pathway of terpenoid biosynthesis in peppermint glandular trichomes (GTs). Based on an analysis of several transcriptome data sets, we demonstrated the presence of transcripts for a leaf-type FNR (L-FNR), a leaf-type Fd (Fd I), a root-type FNR (R-FNR), and two root-type Fds (Fd II and Fd III) in several members of the mint family (Lamiaceae). The present study reports on the biochemical characterization of all Fd and FNR isoforms of peppermint (Mentha × piperita L.). The redox potentials of Fd and FNR isoforms were determined using photoreduction methods. Based on a diaphorase assay, peppermint R-FNR had a substantially higher specificity constant (kcat/Km) for NADPH than L-FNR. Similar results were obtained with ferricyanide as an electron acceptor. When assayed for NADPH–cytochrome c reductase activity, the specificity constant with the Fd II and Fd III isoforms (when compared to Fd I) was slightly higher for L-FNR and substantially higher for R-FNR. Based on real-time quantitative PCR assays with samples representing various peppermint organs and cell types, the Fd II gene was expressed very highly in metabolically active GTs (but also present at lower levels in roots), whereas Fd III was expressed at low levels in both roots and GTs. Our data provide evidence that high transcript levels of Fd II, and not differences in the biochemical properties of the encoded enzyme when compared to those of Fd III, are likely to support the formation of copious amounts of monoterpene via the MEP pathway in peppermint GTs. This work has laid the foundation for follow-up studies to further investigate the roles of a unique R-FNR–Fd II pair in non-photosynthetic GTs of the Lamiaceae.

Research Organization:
Washington State Univ., Pullman, WA (United States)
Sponsoring Organization:
USDOE; USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division (CSGB)
Grant/Contract Number:
SC0001553
OSTI ID:
2283262
Alternate ID(s):
OSTI ID: 2342157
Journal Information:
Plants, Journal Name: Plants Journal Issue: 3 Vol. 13; ISSN PLANCD; ISSN 2223-7747
Publisher:
MDPI AGCopyright Statement
Country of Publication:
Netherlands
Language:
English

References (67)

Isoprenoid Biosynthesis through the Methylerythritol Phosphate Pathway: The (E)-4-Hydroxy-3-methylbut-2-enyl Diphosphate Synthase (GcpE) is a [4Fe–4S] Protein journal November 2002
Terpene Biosynthesis: Modularity Rules journal November 2011
Synthesis and Electrochemical Properties of Structurally Modified Flavin Compounds journal October 2008
Oxygenic Photosynthesis: The Light Reactions book January 1996
Plant Metabolism book January 2014
Light-regulated expression of the Arabidopsis thaliana ferredoxin gene requires sequences upstream and downstream of the transcription initiation site journal January 1995
Monoterpene and sesquiterpene biosynthesis in glandular trichomes of peppermint (Mentha x piperita) rely exclusively on plastid-derived isopentenyl diphosphate journal August 1995
Ferredoxin: the central hub connecting photosystem I to cellular metabolism journal March 2018
Structural basis for the isotype-specific interactions of ferredoxin and ferredoxin: NADP+ oxidoreductase: an evolutionary switch between photosynthetic and heterotrophic assimilation journal January 2017
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding journal May 1976
Novel forms of ferredoxin and ferredoxin-NADP reductase from spinach roots journal November 1990
Two new staining procedures for quantitative estimation of proteins on electrophoretic strips journal January 1963
Photoreduction of NADP+ by a chloroplast photosystem II preparation: effect of light intensity journal August 1989
Isoprenoid biosynthesis via the methylerythritol phosphate pathway: the ( E )-4-hydroxy-3-methylbut-2-enyl diphosphate reductase (LytB/IspH) from Escherichia coli is a [4Fe-4S] protein journal April 2003
A photochemical procedure for reduction of oxidation-reduction proteins employing deazariboflavin as catalyst. journal August 1977
Complex Formation between Ferredoxin Triphosphopyridine Nucleotide Reductase and Electron Transfer Proteins journal February 1969
Monoterpenoid essential oils are not of mevalonoid origin journal June 1997
[22] Ferredoxin-NADP+ oxidoreductase book January 1980
Physicochemical nature of interfaces controlling ferredoxin NADP+ reductase activity through its interprotein interactions with ferredoxin journal October 2015
Domain exchange between isoforms of ferredoxin-NADP+ reductase produces a functional enzyme journal January 2004
Proteomics of terpenoid biosynthesis and secretion in trichomes of higher plant species journal August 2016
Selection and validation of reference genes for quantitative real-time PCR in Rosmarinus officinalis L. in various tissues and under elicitation journal July 2019
Isoprenoid biosynthesis in plant chloroplasts via the MEP pathway: Direct thylakoid/ferredoxin-dependent photoreduction of GcpE/IspG journal February 2006
Multiple Levels of Regulation Determine Monoterpenoid Essential Oil Compositional Variation in the Mint Family journal January 2015
Breaking new ground in the regulation of the early steps of plant isoprenoid biosynthesis journal June 2015
A raison d’être for two distinct pathways in the early steps of plant isoprenoid biosynthesis? journal April 2012
Isoprenoid generating systems in plants — A handy toolbox how to assess contribution of the mevalonate and methylerythritol phosphate pathways to the biosynthetic process journal July 2016
Assessing Flux Distribution Associated with Metabolic Specialization of Glandular Trichomes journal July 2018
Structural studies on the interaction between ferredoxin and ferredoxin-NADP+ reductase journal May 1988
Biochemical and Crystallographic Characterization of Ferredoxin−NADP + Reductase from Nonphotosynthetic Tissues , journal December 2001
Lys75 of Anabaena Ferredoxin−NADP+ Reductase Is a Critical Residue for Binding Ferredoxin and Flavodoxin during Electron Transfer journal September 1998
Tricine–SDS-PAGE journal May 2006
Differential electron flow around photosystem I by two C4-photosynthetic-cell-specific ferredoxins journal October 2000
Methylerythritol 4-phosphate (MEP) pathway metabolic regulation journal January 2014
ELEKTRONENMIKROSKOPISCHE UNTERSUCHUNGEN AN DEN DRÜSENSCHUPPEN VON MENTHA PIPERITA L. 1 journal November 1965
A systems biology approach identifies the biochemical mechanisms regulating monoterpenoid essential oil composition in peppermint journal February 2008
Improving peppermint essential oil yield and composition by metabolic engineering journal September 2011
Metabolic engineering of essential oil yield and composition in mint by altering expression of deoxyxylulose phosphate reductoisomerase and menthofuran synthase journal June 2001
Probing essential oil biosynthesis and secretion by functional evaluation of expressed sequence tags from mint glandular trichomes journal March 2000
Probing the Function of the Invariant Glutamyl Residue 312 in Spinach Ferredoxin-NADP+ Reductase journal December 1998
Comparison of the Electrostatic Binding Sites on the Surface of Ferredoxin for Two Ferredoxin-dependent Enzymes, Ferredoxin-NADP + Reductase and Sulfite Reductase journal October 1999
Differential response of genes for ferredoxin and ferredoxin : NADP+ oxidoreductase to nitrate and light in maize leaves journal January 2003
Molecular mechanism of negative cooperativity of ferredoxin-NADP + reductase by ferredoxin and NADP(H): role of the ion pair of ferredoxin Arg40 of and FNR Glu154 journal September 2022
OligoCalc: an online oligonucleotide properties calculator journal May 2007
A Post Genomic Characterization of Arabidopsis Ferredoxins journal December 2003
Mathematical Modeling-Guided Evaluation of Biochemical, Developmental, Environmental, and Genotypic Determinants of Essential Oil Composition and Yield in Peppermint Leaves journal February 2010
Complementary DNA Cloning and Characterization of Ferredoxin Localized in Bundle-Sheath Cells of Maize Leaves journal February 1999
Differential Interaction of Maize Root Ferredoxin:NADP + Oxidoreductase with Photosynthetic and Non-Photosynthetic Ferredoxin Isoproteins journal July 2000
Distribution of Peltate Glandular Trichomes on Developing Leaves of Peppermint journal October 2000
Development of Peltate Glandular Trichomes of Peppermint journal October 2000
An Investigation of the Storage and Biosynthesis of Phenylpropenes in Sweet Basil journal February 2001
Bioenergetics of Monoterpenoid Essential Oil Biosynthesis in Nonphotosynthetic Glandular Trichomes journal August 2017
Localization of Ferredoxin Isoproteins in Mesophyll and Bundle Sheath Cells in Maize Leaf journal April 1989
Molecular Cloning and Differential Expression of the Maize Ferredoxin Gene Family journal May 1991
Expression of Maize Ferredoxin cDNA in Escherichia coli: Comparison of Photosynthetic and Nonphotosynthetic Ferredoxin Isoproteins and their Chimeric Molecule journal December 1991
Electrostatic forces involved in orienting Anabaena ferredoxin during binding to Anabaena ferredoxin:NAdp + reductase: Site-specific mutagenesis, transient kinetic measurements, and electrostatic surface potentials journal January 1999
Induction of ferredoxin‐NADP+ oxidoreductase and ferredoxin synthesis in pea root plastids during nitrate assimilation journal March 1993
Mutations of Glu92 in Ferredoxin I from Spinach Leaves Produce Proteins Fully Functional in Electron Transfer but Less Efficient in Supporting NADP+ Photoreduction journal March 1996
Analysis of the Oxidation-Reduction Potentials of Recombinant Ferredoxin-NADP+ Reductase from Spinach Chloroplasts journal August 1996
Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes journal June 2002
NormiRazor: tool applying GPU-accelerated computing for determination of internal references in microRNA transcription studies journal September 2020
Serious Overestimation in Quantitative PCR by Circular (Supercoiled) Plasmid Standard: Microalgal pcna as the Model Gene journal March 2010
Selection and validation of appropriate reference genes for quantitative real-time PCR analysis in Salvia hispanica journal November 2017
The MIQE Guidelines: Minimum Information for Publication of Quantitative Real-Time PCR Experiments journal February 2009
Flavoprotein Protocols book July 1999
Determination of Flavin Potential in Proteins by Xanthine/Xanthine Oxidase Method journal January 2020
PDB Entry - 1GAQ: Crystal Structure of the Complex Between Ferredoxin and Ferredoxin-NADP+Reductase other February 2001

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