Publications by authors named "Meike Burow"

62 Publications

Cytosolic phosphofructokinases are important for sugar homeostasis in leaves of Arabidopsis thaliana.

Ann Bot 2021 Sep 22. Epub 2021 Sep 22.

Plant Physiology, University Bayreuth, Universitaetsstr. 30, 95440 Bayreuth, Germany.

Background And Aims: ATP-dependent phosphofructokinases (PFKs) catalyse phosphorylation of the carbon-1 position of fructose-6-phosphate, to form fructose-1,6-bisphosphate. In the cytosol, this is considered a key step in channelling carbon into glycolysis. Arabidopsis thaliana has seven genes encoding PFK isoforms, two chloroplastic and five cytosolic. This study focusses on the four major cytosolic isoforms of PFK in vegetative tissues of A. thaliana.

Methods: We have isolated homozygous knock-out individual mutants (pfk1, pfk3, pfk6, pfk7) and two double mutants (pfk1/7 and pfk3/6) and characterized their growth and metabolic phenotypes.

Key Results: In contrast to single mutants and the double mutant pfk3/6 for the hypoxia-responsive isoforms, the double mutant pfk1/7 had reduced PFK activity and shows a clear visual and metabolic phenotype with reduced shoot growth, early flowering, and elevated hexose levels. This mutant also has an altered ratio of short/long aliphatic glucosinolates and an altered root-shoot distribution. Surprisingly, this mutant does not show any major changes in short-term carbon flux and in levels of hexose-phosphates.

Conclusions: We conclude that the two isoforms PFK1 and PFK7 are important for sugar homeostasis in leaf metabolism and apparently source/sink relations in Arabidopsis, while PFK3 and PFK6 only play a minor role under normal growth conditions.
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http://dx.doi.org/10.1093/aob/mcab122DOI Listing
September 2021

Evolution of A bHLH Interaction Motif.

Int J Mol Sci 2021 Jan 5;22(1). Epub 2021 Jan 5.

DynaMo Center, Department of Plant and Environmental Sciences, University of Copenhagen, 1871 Frederiksberg C, Denmark.

Intrinsically disordered proteins and regions with their associated short linear motifs play key roles in transcriptional regulation. The disordered MYC-interaction motif (MIM) mediates interactions between MYC and MYB transcription factors in that are critical for constitutive and induced glucosinolate (GLS) biosynthesis. GLSs comprise a class of plant defense compounds that evolved in the ancestor of the Brassicales order. We used a diverse set of search strategies to discover additional occurrences of the MIM in other proteins and in other organisms and evaluate the findings by means of structural predictions, interaction assays, and biophysical experiments. Our search revealed numerous MIM instances spread throughout the angiosperm lineage. Experiments verify that several of the newly discovered MIM-containing proteins interact with MYC TFs. Only hits found within the same transcription factor family and having similar characteristics could be validated, indicating that structural predictions and sequence similarity are good indicators of whether the presence of a MIM mediates interaction. The experimentally validated MIMs are found in organisms outside the Brassicales order, showing that MIM function is broader than regulating GLS biosynthesis.
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http://dx.doi.org/10.3390/ijms22010447DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7794824PMC
January 2021

Induction and Priming of Plant Defense by Root-Associated Insect-Pathogenic Fungi.

J Chem Ecol 2021 Jan 12;47(1):112-122. Epub 2020 Nov 12.

Section for Organismal Biology, Department of Plant and Environmental Sciences, University of Copenhagen, Frederiksberg, Denmark.

Plants evolved in close contact with a myriad of microorganisms, some of which formed associations with their roots, benefitting from carbohydrates and other plant resources. In exchange, they evolved to influence important plant functions, e.g. defense against insect herbivores and other antagonists. Here, we test whether a fungus, Metarhizium brunneum, which is mostly known as an insect pathogen, can also associate with plant roots and contribute to above-ground plant defense. Cauliflower (Brassica oleracea var. botrytis) seeds were sown together with M. brunneum-inoculated rice grains, and the resulting plants subjected to leaf herbivory by the specialist Plutella xylostella. Activity of myrosinases, the enzymes activating glucosinolates, was measured before and after herbivory; larval consumption and plant weight at the end of experiments. Metarhizium brunneum clearly established in the plant roots, and after herbivory myrosinase activity was substantially higher in M. brunneum-treated plants than in controls; before herbivory, M. brunneum-treated and control plants did not differ. Leaf consumption was slightly lower in the M. brunneum-treated plants whereas total biomass and allocation to above- or below-ground parts was not affected by the Metarhizium treatment. Thus, M. brunneum associates with roots and primes the plant for a stronger or faster increase in myrosinase activity upon herbivory. Consistent with this, myrosinase function has been suggested to be rate-limiting for induction of the glucosinolate-myrosinase defense system. Our results show that M. brunneum, in addition to being an insect pathogen, can associate with plant roots and prime plant defense.
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http://dx.doi.org/10.1007/s10886-020-01234-xDOI Listing
January 2021

Root-type ferredoxin-NADP oxidoreductase isoforms in Arabidopsis thaliana: Expression patterns, location and stress responses.

Plant Cell Environ 2021 02 18;44(2):548-558. Epub 2020 Nov 18.

Department of Biochemistry, Molecular Plant Biology, University of Turku, Turku, Finland.

In Arabidopsis, two leaf-type ferredoxin-NADP oxidoreductase (LFNR) isoforms function in photosynthetic electron flow in reduction of NADP , while two root-type FNR (RFNR) isoforms catalyse reduction of ferredoxin in non-photosynthetic plastids. As the key to understanding, the function of RFNRs might lie in their spatial and temporal distribution in different plant tissues and cell types, we examined expression of RFNR1 and RFNR2 genes using β-glucuronidase (GUS) reporter lines and investigated accumulation of distinct RFNR isoforms using a GFP approach and Western blotting upon various stresses. We show that while RFNR1 promoter is active in leaf veins, root tips and in the stele of roots, RFNR2 promoter activity is present in leaf tips and root stele, epidermis and cortex. RFNR1 protein accumulates as a soluble protein within the plastids of root stele cells, while RFNR2 is mainly present in the outer root layers. Ozone treatment of plants enhanced accumulation of RFNR1, whereas low temperature treatment specifically affected RFNR2 accumulation in roots. We further discuss the physiological roles of RFNR1 and RFNR2 based on characterization of rfnr1 and rfnr2 knock-out plants and show that although the function of these proteins is partly redundant, the RFNR proteins are essential for plant development and survival.
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http://dx.doi.org/10.1111/pce.13932DOI Listing
February 2021

Heterologous microProtein expression identifies LITTLE NINJA, a dominant regulator of jasmonic acid signaling.

Proc Natl Acad Sci U S A 2020 10 8;117(42):26197-26205. Epub 2020 Oct 8.

Department of Plant and Environmental Sciences, University of Copenhagen, 1871 Frederiksberg C, Denmark;

MicroProteins are small, often single-domain proteins that are sequence-related to larger, often multidomain proteins. Here, we used a combination of comparative genomics and heterologous synthetic misexpression to isolate functional cereal microProtein regulators. Our approach identified LITTLE NINJA (LNJ), a microProtein that acts as a modulator of jasmonic acid (JA) signaling. Ectopic expression of in resulted in stunted plants that resembled the decuple () mutant. In fact, comparing the transcriptomes of transgenic overexpressor plants and revealed a large overlap of deregulated genes, suggesting that ectopic expression altered JA signaling. Transgenic Brachypodium plants with elevated expression levels showed deregulation of JA signaling as well and displayed reduced growth and enhanced production of side shoots (tiller). This tillering effect was transferable between grass species, and overexpression of in barley and rice caused similar traits. We used a clustered regularly interspaced short palindromic repeats (CRISPR) approach and created a LNJ-like protein in by deleting parts of the coding sentence of the gene that encodes a NINJA-domain protein. These mutants were also stunted in size and resembled Thus, similar genome-engineering approaches can be exploited as a future tool to create LNJ proteins and produce cereals with altered architectures.
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http://dx.doi.org/10.1073/pnas.2005198117DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7584889PMC
October 2020

Arabidopsis thaliana transcription factors MYB28 and MYB29 shape ammonium stress responses by regulating Fe homeostasis.

New Phytol 2021 01 4;229(2):1021-1035. Epub 2020 Oct 4.

Department of Plant Biology and Ecology, University of the Basque Country (UPV/EHU), Apdo. 644, Bilbao, E-48080, Spain.

Although ammonium (NH ) is a key intermediate of plant nitrogen metabolism, high concentrations of NH in the soil provoke physiological disorders that lead to the development of stress symptoms. Ammonium nutrition was shown to induce the accumulation of glucosinolates (GSLs) in leaves of different Brassicaceae species. To further understand the link between ammonium nutrition and GSLs, we analysed the ammonium stress response of Arabidopsis mutants impaired in GSL metabolic pathway. We showed that the MYB28 and MYB29 double mutant (myb28myb29), which is almost deprived of aliphatic GSLs, is highly hypersensitive to ammonium nutrition. Moreover, we evidenced that the stress symptoms developed were not a consequence of the lack of aliphatic GSLs. Transcriptomic analysis highlighted the induction of an iron (Fe) deficiency response in myb28myb29 under ammonium nutrition. Consistently, ammonium-grown myb28myb29 plants showed altered Fe accumulation and homeostasis. Interestingly, we showed overall that growing Arabidopsis with increased Fe availability relieved ammonium stress symptoms and that this was associated with MYB28 and MYB29 expression. Taken together, our data indicated that the control of Fe homeostasis was crucial for the Arabidopsis response to ammonium nutrition and evidenced that MYB28 and MYB29 play a role in this control.
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http://dx.doi.org/10.1111/nph.16918DOI Listing
January 2021

Diverse Allyl Glucosinolate Catabolites Independently Influence Root Growth and Development.

Plant Physiol 2020 07 22;183(3):1376-1390. Epub 2020 Apr 22.

Department of Plant Sciences, University of California, Davis, California 95616

Glucosinolates (GSLs) are sulfur-containing defense metabolites produced in the Brassicales, including the model plant Arabidopsis (). Previous work suggests that specific GSLs may function as signals to provide direct feedback regulation within the plant to calibrate defense and growth. These GSLs include allyl-GSL, a defense metabolite that is one of the most widespread GSLs in Brassicaceae and has also been associated with growth inhibition. Here we show that at least three separate potential catabolic products of allyl-GSL or closely related compounds affect growth and development by altering different mechanisms influencing plant development. Two of the catabolites, raphanusamic acid and 3-butenoic acid, differentially affect processes downstream of the auxin signaling cascade. Another catabolite, acrylic acid, affects meristem development by influencing the progression of the cell cycle. These independent signaling events propagated by the different catabolites enable the plant to execute a specific response that is optimal to any given environment.
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http://dx.doi.org/10.1104/pp.20.00170DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7333702PMC
July 2020

Insights into the community structure and lifestyle of the fungal root endophytes of tomato by combining amplicon sequencing and isolation approaches with phytohormone profiling.

FEMS Microbiol Ecol 2020 05;96(5)

Department of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, 1871 Frederiksberg C, Denmark.

Little is known about the influence of host genotype and phytohormones on the composition of fungal endophytic communities. We investigated the influence of host genotype and phytohormones on the structure of the fungal endophytic communities of tomato roots by amplicon sequencing of the ITS1 region and combined this approach with isolation and functional characterization of the isolates. A significant effect of the host genotype on the dominant fungal species was found by comparing the cultivars Castlemart and UC82B and, surprisingly, root pathogens were among the most abundant taxa. In contrast, smaller changes in the relative abundance of the dominant species were found in mutants impaired in jasmonic acid biosynthesis (def1) and ethylene biosynthesis (8338) compared to the respective wild types. However, def1 showed significantly higher species richness compared to the wild type. Analysis of the phytohormone profiles of these genotypes indicates that changes in the phytohormone balance may contribute to this difference in species richness. Assessing the lifestyle of isolated fungi on tomato seedlings revealed the presence of both beneficial endophytes and latent pathogens in roots of asymptomatic plants, suggesting that the interactions between members of the microbiome maintain the equilibrium in the community preventing pathogens from causing disease.
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http://dx.doi.org/10.1093/femsec/fiaa052DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7174037PMC
May 2020

Coordination of Glucosinolate Biosynthesis and Turnover Under Different Nutrient Conditions.

Front Plant Sci 2019 6;10:1560. Epub 2019 Dec 6.

DynaMo Center, Department of Plant and Environmental Sciences, University of Copenhagen, Frederiksberg, Denmark.

Dynamically changing environmental conditions promote a complex regulation of plant metabolism and balanced resource investments to development and defense. Plants of the Brassicales order constitutively allocate carbon, nitrogen, and sulfur to synthesize glucosinolates as their primary defense metabolites. Previous findings support a model in which steady-state levels of glucosinolates in intact tissues are determined by biosynthesis and turnover through a yet uncharacterized turnover pathway. To investigate glucosinolate turnover in the absence of tissue damage, we quantified exogenously applied allyl glucosinolate and endogenous glucosinolates under different nutrient conditions. Our data shows that, in seedlings of accession Columbia-0, glucosinolate biosynthesis and turnover are coordinated according to nutrient availability. Whereas exogenous carbon sources had general quantitative effects on glucosinolate accumulation, sulfur or nitrogen limitation resulted in distinct changes in glucosinolate profiles, indicating that these macronutrients provide different regulatory inputs. Raphanusamic acid, a breakdown product that can potentially be formed from all glucosinolate structures appears not to reflect turnover rates, but instead correlates with increased accumulation of endogenous glucosinolates. Thus, raphanusamic acid could represent a metabolic checkpoint that allows glucosinolate-producing plants to measure the flux through the biosynthetic and/or turnover pathways and thereby to dynamically adjust glucosinolate accumulation in response to internal and external signals.
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http://dx.doi.org/10.3389/fpls.2019.01560DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6909823PMC
December 2019

Differential partitioning of thiols and glucosinolates between shoot and root in Chinese cabbage upon excess zinc exposure.

J Plant Physiol 2020 Jan 26;244:153088. Epub 2019 Nov 26.

DynaMo Center, Department of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, 1871 Frederiksberg C, Denmark.

Zinc (Zn) is one of the important elements of plant growth, however, at elevated level it is toxic. Exposure of Chinese cabbage to elevated Zn concentrations (5 and 10 μM ZnCl) resulted in enhancement of total sulfur and organic sulfur concentration. Transcript level of APS reductase (APR) as a key enzyme in biosynthesis of primary sulfur compounds (cysteine and thiols), was up-regulated in both shoot and root upon exposure to elevated Zn, which was accompanied by an increase in the concentration of cysteine in both tissues. In contrast, the concentration of thiols increased only in the root by 5.5 and 15-fold at 5 and 10 μM Zn, respectively, which was in accompanied by an upregulation of ATP sulfurylase, an enzyme responsible for activation of sulfate. An elevated content of glucosinolates, mostly indolic glucosinolates, only in the shoot of plants exposed to excess level of Zn coincided with an increase in gene expression of key biosynthetic enzymes and regulators (CYP79B3, CYP83B1, MYB34). Thus distinct acuumulation patterns of sulfur containing compounds in root and shoot of Chinese cabbage may be a strategy for Chinese cabbage to combat with exposure to excess Zn.
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http://dx.doi.org/10.1016/j.jplph.2019.153088DOI Listing
January 2020

Glucosinolate structural diversity, identification, chemical synthesis and metabolism in plants.

Phytochemistry 2020 Jan 23;169:112100. Epub 2019 Nov 23.

Department of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, 1871, Frederiksberg C, Denmark. Electronic address:

The glucosinolates (GSLs) is a well-defined group of plant metabolites characterized by having an S-β-d-glucopyrano unit anomerically connected to an O-sulfated (Z)-thiohydroximate function. After enzymatic hydrolysis, the sulfated aglucone can undergo rearrangement to an isothiocyanate, or form a nitrile or other products. The number of GSLs known from plants, satisfactorily characterized by modern spectroscopic methods (NMR and MS) by mid-2018, is 88. In addition, a group of partially characterized structures with highly variable evidence counts for approximately a further 49. This means that the total number of characterized GSLs from plants is somewhere between 88 and 137. The diversity of GSLs in plants is critically reviewed here, resulting in significant discrepancies with previous reviews. In general, the well-characterized GSLs show resemblance to C-skeletons of the amino acids Ala, Val, Leu, Trp, Ile, Phe/Tyr and Met, or to homologs of Ile, Phe/Tyr or Met. Insufficiently characterized, still hypothetic GSLs include straight-chain alkyl GSLs and chain-elongated GSLs derived from Leu. Additional reports (since 2011) of insufficiently characterized GSLs are reviewed. Usually the crucial missing information is correctly interpreted NMR, which is the most effective tool for GSL identification. Hence, modern use of NMR for GSL identification is also reviewed and exemplified. Apart from isolation, GSLs may be obtained by organic synthesis, allowing isotopically labeled GSLs and any kind of side chain. Enzymatic turnover of GSLs in plants depends on a considerable number of enzymes and other protein factors and furthermore depends on GSL structure. Identification of GSLs must be presented transparently and live up to standard requirements in natural product chemistry. Unfortunately, many recent reports fail in these respects, including reports based on chromatography hyphenated to MS. In particular, the possibility of isomers and isobaric structures is frequently ignored. Recent reports are re-evaluated and interpreted as evidence of the existence of "isoGSLs", i.e. non-GSL isomers of GSLs in plants. For GSL analysis, also with MS-detection, we stress the importance of using authentic standards.
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http://dx.doi.org/10.1016/j.phytochem.2019.112100DOI Listing
January 2020

Metabolic engineering of Synechocystis sp. PCC 6803 for the production of aromatic amino acids and derived phenylpropanoids.

Metab Eng 2020 01 10;57:129-139. Epub 2019 Nov 10.

Copenhagen Plant Science Center, Department of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, DK-1871, Frederiksberg C, Copenhagen, Denmark. Electronic address:

In light of the climate change challenge, the advantageous trait of using solar energy and carbon dioxide to produce organic molecules has granted cyanobacteria deserved interest as hosts for metabolic engineering. Importantly, these organisms do not directly compete with agricultural resources. Aromatic amino acids and derived phenylpropanoids are of high importance because they are used by the pharmaceutical, food, cosmetic, and agricultural industries as precursors of active ingredients. Amino acids are traditionally produced by extraction from protein hydrolysates, chemical synthesis or fermentation pathways using heterotrophic microorganisms. In this work we demonstrate for the first time the efficient overproduction of phenylalanine and tyrosine from CO in a Synechocystis sp. PCC 6803 strain heterologously expressing the feedback-inhibition-resistant AroG and TyrA enzymes from E. coli. Production titers reached 904 ± 53 mg/gDW (580 ± 34 mg/L) of phenylalanine and 64 ± 3.7 mg/gDW (41 ± 2.3 mg/L) of tyrosine after 10 days of photoautotrophic growth. We estimate that the production of the two amino acids corresponds to 56% of the total fixed carbon. Phenylalanine and tyrosine are the precursors for phenylpropanoids, thus, we tested the functionality of several phenylpropanoid biosynthetic enzymes in the generated cyanobacterium strains and successfully achieved the production of 470 ± 70 mg/gDW (207 mg/L) of p-coumaric acid, 267 ± 31 mg/gDW (114 mg/L) of cinnamic acid and 47.4 ± 13.9 mg/gDW (12.6 mg/L) of caffeic acid after 6 days of photoautotrophic growth. All compounds were secreted to the growth medium. Our work enlarges the repertoire and yield of heterologous chemicals produced by Synechocystis and contributes to extend the molecular knowledge about this cyanobacterium.
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http://dx.doi.org/10.1016/j.ymben.2019.11.002DOI Listing
January 2020

PROTEIN PHOSPHATASE 2A-B' Controls Resistance and Developmental Leaf Senescence.

Plant Physiol 2020 02 28;182(2):1161-1181. Epub 2019 Oct 28.

Molecular Plant Biology, University of Turku, FI-20014 Turku, Finland

Plants optimize their growth and survival through highly integrated regulatory networks that coordinate defensive measures and developmental transitions in response to environmental cues. Protein phosphatase 2A (PP2A) is a key signaling component that controls stress reactions and growth at different stages of plant development, and the PP2A regulatory subunit PP2A-B'γ is required for negative regulation of pathogenesis responses and for maintenance of cell homeostasis in short-day conditions. Here, we report molecular mechanisms by which PP2A-B'γ regulates resistance and leaf senescence in Arabidopsis (). We extend the molecular functionality of PP2A-B'γ to a protein kinase-phosphatase interaction with the defense-associated calcium-dependent protein kinase CPK1 and present indications this interaction may function to control CPK1 activity. In presenescent leaf tissues, PP2A-B'γ is also required to negatively control the expression of salicylic acid-related defense genes, which have recently proven vital in plant resistance to necrotrophic fungal pathogens. In addition, we find the premature leaf yellowing of - depends on salicylic acid biosynthesis via SALICYLIC ACID INDUCTION DEFICIENT2 and bears the hallmarks of developmental leaf senescence. We propose PP2A-B'γ age-dependently controls salicylic acid-related signaling in plant immunity and developmental leaf senescence.
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http://dx.doi.org/10.1104/pp.19.00893DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6997707PMC
February 2020

IDDomainSpotter: Compositional bias reveals domains in long disordered protein regions-Insights from transcription factors.

Protein Sci 2020 01 11;29(1):169-183. Epub 2019 Nov 11.

Structural Biology and NMR Laboratory, Department of Biology, University of Copenhagen, Copenhagen, Denmark.

Protein domains constitute regions of distinct structural properties and molecular functions that are retained when removed from the rest of the protein. However, due to the lack of tertiary structure, the identification of domains has been largely neglected for long (>50 residues) intrinsically disordered regions. Here we present a sequence-based approach to assess and visualize domain organization in long intrinsically disordered regions based on compositional sequence biases. An online tool to find putative intrinsically disordered domains (IDDomainSpotter) in any protein sequence or sequence alignment using any particular sequence trait is available at http://www.bio.ku.dk/sbinlab/IDDomainSpotter. Using this tool, we have identified a putative domain enriched in hydrophilic and disorder-promoting residues (Pro, Ser, and Thr) and depleted in positive charges (Arg and Lys) bordering the folded DNA-binding domains of several transcription factors (p53, GCR, NAC46, MYB28, and MYB29). This domain, from two different MYB transcription factors, was characterized biophysically to determine its properties. Our analyses show the domain to be extended, dynamic and highly disordered. It connects the DNA-binding domain to other disordered domains and is present and conserved in several transcription factors from different families and domains of life. This example illustrates the potential of IDDomainSpotter to predict, from sequence alone, putative domains of functional interest in otherwise uncharacterized disordered proteins.
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http://dx.doi.org/10.1002/pro.3754DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6933863PMC
January 2020

Specificity of MYB interactions relies on motifs in ordered and disordered contexts.

Nucleic Acids Res 2019 10;47(18):9592-9608

DynaMo Center, Department of Plant and Environmental Sciences, University of Copenhagen, 1871 Frederiksberg C, Denmark.

Physical interactions between members of the MYB and bHLH transcription factor (TF) families regulate many important biological processes in plants. Not all reported MYB-bHLH interactions can be explained by the known binding sites in the R3 repeat of the MYB DNA-binding domain. Noteworthy, most of the sequence diversity of MYB TFs lies in their non-MYB regions, which contain orphan small subgroup-defining motifs not yet linked to molecular functions. Here, we identified the motif mediating interaction between MYB TFs from subgroup 12 and their bHLH partners. Unlike other known MYB-bHLH interactions, the motif locates to the centre of the predicted disordered non-MYB region. We characterised the core motif, which enabled accurate prediction of previously unknown bHLH-interacting MYB TFs in Arabidopsis thaliana, and we confirmed its functional importance in planta. Our results indicate a correlation between the MYB-bHLH interaction affinity and the phenotypic output controlled by the TF complex. The identification of an interaction motif outside R3 indicates that MYB-bHLH interactions must have arisen multiple times, independently and suggests many more motifs of functional relevance to be harvested from subgroup-specific studies.
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http://dx.doi.org/10.1093/nar/gkz691DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6765112PMC
October 2019

R2R3 MYB Transcription Factors - Functions outside the DNA-Binding Domain.

Trends Plant Sci 2019 10 26;24(10):934-946. Epub 2019 Jul 26.

DynaMo Center, Department of Plant and Environmental Sciences, University of Copenhagen, Copenhagen, Denmark; Copenhagen Plant Science Centre, Department of Plant and Environmental Sciences, University of Copenhagen, Copenhagen, Denmark. Electronic address:

Several transcription factor (TF) families, including the MYB family, regulate a wide array of biological processes. TFs contain DNA-binding domains (DBDs) and regulatory regions; although information on protein structure is scarce for plant MYB TFs, various in silico methods suggest that the non-MYB regions contain extensive intrinsically disordered regions (IDRs). Although IDRs do not fold into stable globular structures, they comprise functional regions including interaction motifs, and recent research has shown that IDRs perform crucial biological roles. We map here domain organization, disorder predictions, and functional regions across the entire Arabidopsis thaliana R2R3 MYB TF family, and highlight where an increased research focus will be necessary to shape a new understanding of structure-function relationships in plant TFs.
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http://dx.doi.org/10.1016/j.tplants.2019.07.003DOI Listing
October 2019

Defining optimal electron transfer partners for light-driven cytochrome P450 reactions.

Metab Eng 2019 09 12;55:33-43. Epub 2019 May 12.

Copenhagen Plant Science Center, Department of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, 1871, Frederiksberg C, Denmark. Electronic address:

Plants and cyanobacteria are promising heterologous hosts for metabolic engineering, and particularly suited for expression of cytochrome P450 (P450s), enzymes that catalyse key steps in biosynthetic pathways leading to valuable natural products such as alkaloids, terpenoids and phenylpropanoids. P450s are often difficult to express and require a membrane-bound NADPH-dependent reductase, complicating their use in metabolic engineering and bio-production. We previously demonstrated targeting of heterologous P450s to thylakoid membranes both in N. benthamiana chloroplasts and cyanobacteria, and functional substitution of their native reductases with the photosynthetic apparatus via the endogenous soluble electron carrier ferredoxin. However, because ferredoxin acts as a sorting hub for photosynthetic reducing power, there is fierce competition for reducing equivalents, which limits photosynthesis-driven P450 output. This study compares the ability of four electron carriers to increase photosynthesis-driven P450 activity. These carriers, three plant ferredoxins and a flavodoxin-like engineered protein derived from cytochrome P450 reductase, show only modest differences in their electron transfer to our model P450, CYP79A1 in vitro. However, only the flavodoxin-like carrier supplies appreciable reducing power in the presence of competition for reduced ferredoxin, because it possesses a redox potential that renders delivery of reducing equivalents to endogenous processes inefficient. We further investigate the efficacy of these electron carrier proteins in vivo by expressing them transiently in N. benthamiana fused to CYP79A1. All but one of the fusion enzymes show improved sequestration of photosynthetic reducing power. Fusion with the flavodoxin-like carrier offers the greatest improvement in this comparison - nearly 25-fold on a per protein basis. Thus, this study demonstrates that synthetic electron transfer pathways with optimal redox potentials can alleviate the problem of endogenous competition for reduced ferredoxin and sets out a new metabolic engineering strategy useful for producing valuable natural products.
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http://dx.doi.org/10.1016/j.ymben.2019.05.003DOI Listing
September 2019

An Arabidopsis TIR-Lectin Two-Domain Protein Confers Defense Properties against .

Plant Physiol 2019 04 14;179(4):1298-1314. Epub 2019 Feb 14.

Centro de Biotecnología y Genómica de Plantas, Universidad Politécnica de Madrid-Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria, Campus de Montegancedo, 28223 Madrid, Spain

Plant immunity depends on fast and specific transcriptional reprogramming triggered by the perception of biotic stresses. Numerous studies have been conducted to better understand the response of plants to the generalist herbivore two-spotted spider mite (). However, how plants perceive mites and how this perception is translated into changes in gene expression are largely unknown. In this work, we identified a gene induced in Arabidopsis () upon spider mite attack that encodes a two-domain protein containing predicted lectin and Toll/Interleukin-1 receptor domains. The gene, previously named , belongs to the Phloem Protein2 family. Biotic assays showed that PP2-A5 confers tolerance to Overexpression or knockout of leads to transcriptional reprogramming that alters the balance of hormone accumulation and corresponding signaling pathways. The nucleocytoplasmic location of this protein supports a direct interaction with regulators of gene transcription, suggesting that the combination of two putative signaling domains in a single protein may provide a novel mechanism for regulating gene expression. Together, our results suggest that PP2-A5 improves the ability to defend against by participating in the tight regulation of hormonal cross talk upon mite feeding. Further research is needed to determine the mechanism by which this two-domain protein functions and to clarify its molecular role in signaling following a spider mite attack.
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http://dx.doi.org/10.1104/pp.18.00951DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6446783PMC
April 2019

Dynamic Modeling of Indole Glucosinolate Hydrolysis and Its Impact on Auxin Signaling.

Front Plant Sci 2018 26;9:550. Epub 2018 Apr 26.

DynaMo Center, Copenhagen Plant Science Centre, Department of Plant and Environmental Sciences, University of Copenhagen, Frederiksberg, Denmark.

Plants release chemicals to deter attackers. relies on multiple defense compounds, including indol-3-ylmethyl glucosinolate (I3G), which upon hydrolysis initiated by myrosinase enzymes releases a multitude of bioactive compounds, among others, indole-3-acetonitrile and indole-3-acetoisothiocyanate. The highly unstable isothiocyanate rapidly reacts with other molecules. One of the products, indole-3-carbinol, was reported to inhibit auxin signaling through binding to the TIR1 auxin receptor. On the contrary, the nitrile product of I3G hydrolysis can be converted by nitrilase enzymes to form the primary auxin molecule, indole-3-acetic acid, which activates TIR1. This suggests that auxin signaling is subject to both antagonistic and protagonistic effects of I3G hydrolysis upon attack. We hypothesize that I3G hydrolysis and auxin signaling form an incoherent feedforward loop and we build a mathematical model to examine the regulatory network dynamics. We use molecular docking to investigate the possible antagonistic properties of different I3G hydrolysis products by competitive binding to the TIR1 receptor. Our simulations reveal an uncoupling of auxin concentration and signaling, and we determine that enzyme activity and antagonist binding affinity are key parameters for this uncoupling. The molecular docking predicts that several I3G hydrolysis products strongly antagonize auxin signaling. By comparing a tissue disrupting attack - e.g., by chewing insects or necrotrophic pathogens that causes rapid release of I3G hydrolysis products - to sustained cell-autonomous I3G hydrolysis, e.g., upon infection by biotrophic pathogens, we find that each scenario gives rise to distinct auxin signaling dynamics. This suggests that plants have different defense versus growth strategies depending on the nature of the attack.
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http://dx.doi.org/10.3389/fpls.2018.00550DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5932361PMC
April 2018

Comparison of the Relative Potential for Epigenetic and Genetic Variation To Contribute to Trait Stability.

G3 (Bethesda) 2018 05 4;8(5):1733-1746. Epub 2018 May 4.

DynaMo Center, Copenhagen Plant Science Centre, Department of Plant and Environmental Sciences, University of Copenhagen, Copenhagen, Denmark

The theoretical ability of epigenetic variation to influence the heritable variation of complex traits is gaining traction in the study of adaptation. This theory posits that epigenetic marks can control adaptive phenotypes but the relative potential of epigenetic variation in comparison to genetic variation in these traits is not presently understood. To compare the potential of epigenetic and genetic variation in adaptive traits, we analyzed the influence of DNA methylation variation on the accumulation of chemical defense compounds glucosinolates from the order Brassicales. Several decades of work on glucosinolates has generated extensive knowledge about their synthesis, regulation, genetic variation and contribution to fitness establishing this pathway as a model pathway for complex adaptive traits. Using high-throughput phenotyping with a randomized block design of derived epigenetic Recombinant Inbred Lines, we measured the correlation between DNA methylation variation and mean glucosinolate variation and within line stochastic variation. Using this information, we identified epigenetic Quantitative Trait Loci that contained specific Differentially Methylated Regions associated with glucosinolate traits. This showed that variation in DNA methylation correlates both with levels and variance of glucosinolates and flowering time with trait-specific loci. By conducting a meta-analysis comparing the results to different genetically variable populations, we conclude that the influence of DNA methylation variation on these adaptive traits is much lower than the corresponding impact of standing genetic variation. As such, selective pressure on these traits should mainly affect standing genetic variation to lead to adaptation.
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http://dx.doi.org/10.1534/g3.118.200127DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5940164PMC
May 2018

Unravelling Protein-Protein Interaction Networks Linked to Aliphatic and Indole Glucosinolate Biosynthetic Pathways in Arabidopsis.

Front Plant Sci 2017 29;8:2028. Epub 2017 Nov 29.

Department of Plant and Environmental Sciences, Faculty of Science, DynaMo Center, University of Copenhagen, Frederiksberg, Denmark.

Within the cell, biosynthetic pathways are embedded in protein-protein interaction networks. In Arabidopsis, the biosynthetic pathways of aliphatic and indole glucosinolate defense compounds are well-characterized. However, little is known about the spatial orchestration of these enzymes and their interplay with the cellular environment. To address these aspects, we applied two complementary, untargeted approaches-split-ubiquitin yeast 2-hybrid and co-immunoprecipitation screens-to identify proteins interacting with CYP83A1 and CYP83B1, two homologous enzymes specific for aliphatic and indole glucosinolate biosynthesis, respectively. Our analyses reveal distinct functional networks with substantial interconnection among the identified interactors for both pathway-specific markers, and add to our knowledge about how biochemical pathways are connected to cellular processes. Specifically, a group of protein interactors involved in cell death and the hypersensitive response provides a potential link between the glucosinolate defense compounds and defense against biotrophic pathogens, mediated by protein-protein interactions.
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http://dx.doi.org/10.3389/fpls.2017.02028DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5712850PMC
November 2017

An evolutionarily young defense metabolite influences the root growth of plants via the ancient TOR signaling pathway.

Elife 2017 12 12;6. Epub 2017 Dec 12.

DynaMo Center, Copenhagen Plant Science Center, Department of Plant and Environmental Sciences, University of Copenhagen, Copenhagen, Denmark.

To optimize fitness a plant should monitor its metabolism to appropriately control growth and defense. Primary metabolism can be measured by the universally conserved TOR (Target of Rapamycin) pathway to balance growth and development with the available energy and nutrients. Recent work suggests that plants may measure defense metabolites to potentially provide a strategy ensuring fast reallocation of resources to coordinate plant growth and defense. There is little understanding of mechanisms enabling defense metabolite signaling. To identify mechanisms of defense metabolite signaling, we used glucosinolates, an important class of plant defense metabolites. We report novel signaling properties specific to one distinct glucosinolate, 3-hydroxypropylglucosinolate across plants and fungi. This defense metabolite, or derived compounds, reversibly inhibits root growth and development. 3-hydroxypropylglucosinolate signaling functions via genes in the ancient TOR pathway. If this event is not unique, this raises the possibility that other evolutionarily new plant metabolites may link to ancient signaling pathways.
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http://dx.doi.org/10.7554/eLife.29353DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5730369PMC
December 2017

Localization of the glucosinolate biosynthetic enzymes reveals distinct spatial patterns for the biosynthesis of indole and aliphatic glucosinolates.

Physiol Plant 2018 Jun 11;163(2):138-154. Epub 2018 Jan 11.

DynaMo Center, Department of Plant and Environmental Sciences, Faculty of Science, University of Copenhagen, 1871 Frederiksberg C, Denmark.

Glucosinolates constitute the primary defense metabolites in Arabidopsis thaliana (Arabidopsis). Indole and aliphatic glucosinolates, biosynthesized from tryptophan and methionine, respectively, are known to serve distinct biological functions. Although all genes in the biosynthetic pathways are identified, and it is known where glucosinolates are stored, it has remained elusive where glucosinolates are produced at the cellular and tissue level. To understand how the spatial organization of the different glucosinolate biosynthetic pathways contributes to their distinct biological functions, we investigated the localization of enzymes of the pathways under constitutive conditions and, for indole glucosinolates, also under induced conditions, by analyzing the spatial distribution of several fluorophore-tagged enzymes at the whole plant and the cellular level. We show that key steps in the biosynthesis of the different types of glucosinolates are localized in distinct cells in separate as well as overlapping vascular tissues. The presence of glucosinolate biosynthetic enzymes in parenchyma cells of the vasculature may assign new defense-related functions to these cell types. The knowledge gained in this study is an important prerequisite for understanding the orchestration of chemical defenses from site of synthesis to site of storage and potential (re)mobilization upon attack.
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http://dx.doi.org/10.1111/ppl.12672DOI Listing
June 2018

Nitrogen - essential macronutrient and signal controlling flowering time.

Physiol Plant 2018 Feb 23;162(2):251-260. Epub 2017 Nov 23.

DynaMo Center, Department of Plant and Environmental Sciences, University of Copenhagen, Frederiksberg, Denmark.

Nitrogen, as limiting nutrient for plant growth and crop yield, is a main component of fertilizers and heavily used in modern agriculture. Early reports from over-application of fertilizers in crop production have shown to repress the transition from vegetative to reproductive phase. For the model plant Arabidopsis thaliana, there is evidence that low nitrogen conditions promote early flowering, while high nitrogen as well as nitrogen starvation conditions display the opposite effect. To gain a better understanding of how nitrogen affects the onset of flowering, we reviewed the existing literature for A. thaliana and carried out a meta-analysis on available transcriptomics data, seeking for potential genes and pathways involved in both nitrogen responses and flowering time control. With this strategy, we aimed at identifying potential gateways for integration of nitrogen signaling and potential regulators that might link the regulatory networks controlling nitrogen and flowering in A. thaliana. We found that photoperiodic pathway genes have high potential to be involved in nitrogen-dependent flowering.
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http://dx.doi.org/10.1111/ppl.12664DOI Listing
February 2018

Tat proteins as novel thylakoid membrane anchors organize a biosynthetic pathway in chloroplasts and increase product yield 5-fold.

Metab Eng 2017 11 28;44:108-116. Epub 2017 Sep 28.

Copenhagen Plant Science Center, Center for Synthetic Biology "bioSYNergy", Department of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, DK-1871 Frederiksberg C, Denmark. Electronic address:

Photosynthesis drives the production of ATP and NADPH, and acts as a source of carbon for primary metabolism. NADPH is also used in the production of many natural bioactive compounds. These are usually synthesized in low quantities and are often difficult to produce by chemical synthesis due to their complex structures. Some of the crucial enzymes catalyzing their biosynthesis are the cytochromes P450 (P450s) situated in the endoplasmic reticulum (ER), powered by electron transfers from NADPH. Dhurrin is a cyanogenic glucoside and its biosynthesis involves a dynamic metabolon formed by two P450s, a UDP-glucosyltransferase (UGT) and a P450 oxidoreductase (POR). Its biosynthetic pathway has been relocated to the chloroplast where ferredoxin, reduced through the photosynthetic electron transport chain, serves as an efficient electron donor to the P450s, bypassing the involvement of POR. Nevertheless, translocation of the pathway from the ER to the chloroplast creates other difficulties, such as the loss of metabolon formation and intermediate diversion into other metabolic pathways. We show here that co-localization of these enzymes in the thylakoid membrane leads to a significant increase in product formation, with a concomitant decrease in off-pathway intermediates. This was achieved by exchanging the membrane anchors of the dhurrin pathway enzymes to components of the Twin-arginine translocation pathway, TatB and TatC, which have self-assembly properties. Consequently, we show 5-fold increased titers of dhurrin and a decrease in the amounts of intermediates and side products in Nicotiana benthamiana. Further, results suggest that targeting the UGT to the membrane is a key factor to achieve efficient substrate channeling.
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http://dx.doi.org/10.1016/j.ymben.2017.09.014DOI Listing
November 2017

Transcriptome and Metabolite Changes during Hydrogen Cyanamide-Induced Floral Bud Break in Sweet Cherry.

Front Plant Sci 2017 17;8:1233. Epub 2017 Jul 17.

Plant Biochemistry Laboratory, Department of Plant and Environmental Sciences, University of CopenhagenFrederiksberg, Denmark.

Release of bud dormancy in perennial woody plants is a temperature-dependent process and thus flowering in these species is heavily affected by climate change. The lack of cold winters in temperate growing regions often results in reduced flowering and low fruit yields. This is likely to decrease the availability of fruits and nuts of the spp. in the near future. In order to maintain high yields, it is crucial to gain detailed knowledge on the molecular mechanisms controlling the release of bud dormancy. Here, we studied these mechanisms using sweet cherry ( L.), a crop where the agrochemical hydrogen cyanamide (HC) is routinely used to compensate for the lack of cold winter temperatures and to induce flower opening. In this work, dormant flower buds were sprayed with hydrogen cyanamide followed by deep RNA sequencing, identifying three main expression patterns in response to HC. These transcript level results were validated by quantitative real time polymerase chain reaction and supported further by phytohormone profiling (ABA, SA, IAA, CK, ethylene, JA). Using these approaches, we identified the most up-regulated pathways: the cytokinin pathway, as well as the jasmonate and the hydrogen cyanide pathway. Our results strongly suggest an inductive effect of these metabolites in bud dormancy release and provide a stepping stone for the characterization of key genes in bud dormancy release.
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http://dx.doi.org/10.3389/fpls.2017.01233DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5511853PMC
July 2017

How does a plant orchestrate defense in time and space? Using glucosinolates in Arabidopsis as case study.

Curr Opin Plant Biol 2017 08 30;38:142-147. Epub 2017 May 30.

DynaMo Center, Department of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, 1871 Frederiksberg C, Denmark. Electronic address:

The sessile nature of plants has caused plants to develop means to defend themselves against attacking organisms. Multiple strategies range from physical barriers to chemical warfare including pre-formed anticipins as well as phytoalexins produced only upon attack. While phytoalexins require rapid induction, constitutive defenses can impose ecological costs if they deter pollinators or attract specialized herbivores. In the model Arabidopsis thaliana, the well-characterized glucosinolate anticipins are categorized into different classes, aliphatic and indole glucosinolates, depending on their amino acid precursor. Using glucosinolates in Arabidopsis as case study, we will discuss how plants orchestrate synthesis, storage and activation of pre-formed defense compounds spatially and temporally.
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http://dx.doi.org/10.1016/j.pbi.2017.04.009DOI Listing
August 2017

An NPF transporter exports a central monoterpene indole alkaloid intermediate from the vacuole.

Nat Plants 2017 01 13;3:16208. Epub 2017 Jan 13.

The John Innes Centre, Department of Biological Chemistry, Norwich Research Park, Norwich NR4 7UK, UK.

Plants sequester intermediates of metabolic pathways into different cellular compartments, but the mechanisms by which these molecules are transported remain poorly understood. Monoterpene indole alkaloids, a class of specialized metabolites that includes the anticancer agent vincristine, antimalarial quinine and neurotoxin strychnine, are synthesized in several different cellular locations. However, the transporters that control the movement of these biosynthetic intermediates within cellular compartments have not been discovered. Here we present the discovery of a tonoplast localized nitrate/peptide family (NPF) transporter from Catharanthus roseus, CrNPF2.9, that exports strictosidine, the central intermediate of this pathway, into the cytosol from the vacuole. This discovery highlights the role that intracellular localization plays in specialized metabolism, and sets the stage for understanding and controlling the central branch point of this pharmacologically important group of compounds.
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http://dx.doi.org/10.1038/nplants.2016.208DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5238941PMC
January 2017

Genome Wide Association Mapping in Arabidopsis thaliana Identifies Novel Genes Involved in Linking Allyl Glucosinolate to Altered Biomass and Defense.

Front Plant Sci 2016 12;7:1010. Epub 2016 Jul 12.

Department of Plant Sciences, University of California, DavisDavis, CA, USA; DynaMo Center, University of CopenhagenCopenhagen, Denmark.

A key limitation in modern biology is the ability to rapidly identify genes underlying newly identified complex phenotypes. Genome wide association studies (GWAS) have become an increasingly important approach for dissecting natural variation by associating phenotypes with genotypes at a genome wide level. Recent work is showing that the Arabidopsis thaliana defense metabolite, allyl glucosinolate (GSL), may provide direct feedback regulation, linking defense metabolism outputs to the growth, and defense responses of the plant. However, there is still a need to identify genes that underlie this process. To start developing a deeper understanding of the mechanism(s) that modulate the ability of exogenous allyl GSL to alter growth and defense, we measured changes in plant biomass and defense metabolites in a collection of natural 96 A. thaliana accessions fed with 50 μM of allyl GSL. Exogenous allyl GSL was introduced exclusively to the roots and the compound transported to the leaf leading to a wide range of heritable effects upon plant biomass and endogenous GSL accumulation. Using natural variation we conducted GWAS to identify a number of new genes which potentially control allyl responses in various plant processes. This is one of the first instances in which this approach has been successfully utilized to begin dissecting a novel phenotype to the underlying molecular/polygenic basis.
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http://dx.doi.org/10.3389/fpls.2016.01010DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4940622PMC
July 2016

CB5C affects the glucosinolate profile in Arabidopsis thaliana.

Plant Signal Behav 2016 08;11(8):e1160189

a Department of Plant and Environmental Sciences, DynaMo Center of Excellence & Copenhagen Plant Science Center , University of Copenhagen , Denmark.

Cytochrome b5 (CB5) proteins are small heme-binding proteins, that influence cytochrome P450 activity. While only one CB5 isoform is found in mammals, higher plants have several isoforms of these proteins. The roles of the many CB5 isoforms in plants remain unknown. We hypothesized that CB5 proteins support the cytochrome P450 enzymes of plant specialized metabolism and found CB5C from Arabidopsis thaliana to co-express with glucosinolate biosynthetic genes. We characterized the glucosinolate profiles of 2 T-DNA insertion mutants of CB5C, and found that long-chained aliphatic glucosinolates were reduced in one of the mutant lines - a phenotype that was exaggerated upon methyl-jasmonate treatment. These results support the hypothesis, that CB5C influences glucosinolate biosynthesis, however, the mode of action remains unknown. Furthermore, the mutants differed in their biomass response to methyl jasmonate treatment. Thereby, our results highlight the varying effects of T-DNA insertion sites, as the 2 analyzed alleles show different phenotypes.
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http://dx.doi.org/10.1080/15592324.2016.1160189DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5022417PMC
August 2016
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