Regina Feil

University of Nebraska at Lincoln, Lincoln, Nebraska, United States

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Publications (35)228.57 Total impact

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    ABSTRACT: Trehalose metabolism is essential for normal growth and development in higher plants. It is synthesized in a two-step pathway catalyzed by trehalose-6-phosphate (Tre6P) synthase (TPS) and trehalose phosphatase. Arabidopsis thaliana has 11 TPS or TPS-like proteins, which belong to two distinct clades: class I (AtTPS1-AtTPS4) and class II (AtTPS5-AtTPS11). Only AtTPS1 has previously been shown to have TPS activity. Null A. thaliana tps1 mutants fail to complete embryogenesis and rescued lines have stunted growth and delayed flowering, indicating that AtTPS1 is important throughout the life cycle. Here we show that expression of AtTPS2 or AtTPS4 enables the yeast tps1∆ tps2∆ mutant to grow on glucose and accumulate Tre6P and trehalose. Class II TPS genes did not complement the yeast mutant. Thus, A. thaliana has at least three catalytically active TPS isoforms, suggesting that loss of Tre6P production might not be the only reason for the growth defects of A. thaliana tps1 mutants.
    The Biochemical journal. 12/2014;
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    ABSTRACT: Mature leaves of plants transferred from low to high light typically increase their photosynthetic capacity. In Arabidopsis thaliana, this dynamic acclimation requires expression of GPT2, a glucose 6-phosphate/phosphate translocator. Here, we examine the impact of GPT2 on leaf metabolism and photosynthesis. Plants of wild-type and of a GPT2 knockout (gpt2.2) grown under low light achieved the same photosynthetic rate, despite having different metabolic and transcriptomic strategies. Immediately upon transfer to high light, gpt2.2 plants showed a higher rate of photosynthesis than wild-type (35%) however, over subsequent days, wild-type plants acclimated photosynthetic capacity, increasing photosynthesis 100 after 7 days. Wild-type plants accumulated more starch than gpt2.2 plants throughout acclimation. We suggest that GPT2 activity results in the net import of glucose 6-phosphate from cytosol to chloroplast, increasing starch synthesis. There was clear acclimation of metabolism, with short terms changes typically being reversed as plants acclimated. Distinct responses to light were seen in wild-type and gpt2.2 leaves. Significantly higher levels of sugar-phosphates were seen in gpt2.2. We suggest that GPT2 alters the distribution of metabolites between compartments and that this plays an essential role in allowing the cell to interpret environmental signals. This article is protected by copyright. All rights reserved.
    Plant Cell and Environment 12/2014; · 5.91 Impact Factor
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    Plant physiology 10/2014; · 7.39 Impact Factor
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    ABSTRACT: Extended darkness induces a transient increase in sugars and trehalose pathway gene expression. 2 4
    Journal of Experimental Botany 09/2014; In press. · 5.79 Impact Factor
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    ABSTRACT: The major component of starch is the branched glucan amylopectin. Structural features of amylopectin - the branching pattern and the chain length distribution - are thought to be key factors that enable it to form semi-crystalline starch granules. We varied both structural parameters by creating Arabidopsis mutants lacking combinations of starch synthases 1, 2 and 3 (to vary chain lengths) and the isoamylase 1 debranching enzyme (isa; to alter branching pattern). The isa mutant accumulates primarily phytoglycogen in leaf mesophyll cells, with only small amounts of starch in other cell types (epidermis and bundle sheath cells). This balance can be significantly shifted by mutating different starch synthases. Mutation of SS1 promoted starch synthesis, restoring granules in mesophyll cell plastids. Mutation of SS2 decreased starch synthesis, abolishing granules in epidermal and bundle sheath cells. Thus, the types of starch synthases present affect the crystallinity - and thus solubility - of the glucans made, compensating for or compounding the effects of an aberrant branching pattern. Interestingly, ss2 mutant plants contained small amounts of phytoglycogen in addition to aberrant starch. Likewise, ss2ss3 plants contained phytoglycogen, but were almost devoid of glucan despite retaining other SS isoforms. Surprisingly, in the ss2ss3isa triple mutants, glucan production was restored, indicating that in ss2ss3, starch synthase activity per se is not limiting but that the isoamylase suppresses glucan accumulation. We conclude that loss of only starch synthases can cause phytoglycogen production. This readily degraded by isoamylase and other enzymes so does not accumulate and was previously unnoticed.
    Plant physiology 06/2014; · 7.39 Impact Factor
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    ABSTRACT: Non-aqueous fractionation is a technique for enrichment of different subcellular compartments derived from lyophilised material. It was developed to study the subcellular distribution of metabolites. Here we analyse the distribution of about 1000 proteins and 70 metabolites, including 22 phosphorylated intermediates in wild-type Arabidopsis rosette leaves, using non-aqueous gradients divided into 12 fractions. Good separation of plastidial, cytosolic and vacuolar metabolites and proteins was achieved but cytosolic, mitochondrial and peroxisomal proteins clustered together. There was considerable heterogeneity in the fractional distribution of transcription factors, ribosomal proteins and subunits of the vacuolar-ATPase, indicating diverse compartmental location. Within the plastid, sub-organellar separation of thylakoids and stromal proteins was observed. Metabolites from the Calvin-Benson cycle, photorespiration, starch and sucrose synthesis, glycolysis and tricarboxylic acid cycle grouped with their associated proteins of the respective compartment. Non-aqueous fractionation thus proved a powerful method for the study of the organellar, and in some cases sub-organellar, distribution of proteins and their association with metabolites. It remains the technique of choice for assignment of subcellular location to metabolites in intact plant tissues and thus the technique of choice for doing combined metabolite-protein analysis in the same tissue sample.
    Molecular &amp Cellular Proteomics 05/2014; · 7.25 Impact Factor
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    ABSTRACT: Trehalose 6-phosphate (Tre6P), the intermediate of trehalose biosynthesis, has a profound influence on plant metabolism, growth, and development. It has been proposed that Tre6P acts as a signal of sugar availability and is possibly specific for sucrose status. Short-term sugar-feeding experiments were carried out with carbon-starved Arabidopsis thaliana seedlings grown in axenic shaking liquid cultures. Tre6P increased when seedlings were exogenously supplied with sucrose, or with hexoses that can be metabolized to sucrose, such as glucose and fructose. Conditional correlation analysis and inhibitor experiments indicated that the hexose-induced increase in Tre6P was an indirect response dependent on conversion of the hexose sugars to sucrose. Tre6P content was affected by changes in nitrogen status, but this response was also attributable to parallel changes in sucrose. The sucrose-induced rise in Tre6P was unaffected by cordycepin but almost completely blocked by cycloheximide, indicating that de novo protein synthesis is necessary for the response. There was a strong correlation between Tre6P and sucrose even in lines that constitutively express heterologous trehalose-phosphate synthase or trehalose-phosphate phosphatase, although the Tre6P:sucrose ratio was shifted higher or lower, respectively. It is proposed that the Tre6P:sucrose ratio is a critical parameter for the plant and forms part of a homeostatic mechanism to maintain sucrose levels within a range that is appropriate for the cell type and developmental stage of the plant.
    Journal of Experimental Botany 01/2014; · 5.79 Impact Factor
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    ABSTRACT: In short photoperiods plants accumulate starch more rapidly in the light and degrade it more slowly at night, ensuring that their starch reserves last until dawn. To investigate the accompanying changes in the timing of growth, Arabidopsis was grown in a range of photoperiods and analysed for rosette biomass, photosynthesis, respiration, ribosome abundance, polysome loading, starch, and over 40 metabolites at dawn and dusk. The dataset was used to model growth rates in the daytime and night, and to identify metabolites that correlate with growth. Modelled growth rates and polysome loading were high in the daytime and at night in long photoperiods, but decreased at night in short photoperiods. Ribosome abundance was similar in all photoperiods. It is discussed how the amount of starch accumulated in the light period, the length of the night and maintenance costs interact to constrain growth at night in short photoperiods, and alter the strategy for optimising ribosome use. Significant correlations were found in the daytime and the night between growth rates and the levels of the sugar-signal trehalose 6-phosphate and the amino acid biosynthesis intermediate shikimate, identifying these metabolites as hubs in a network that coordinates growth with diurnal changes in the carbon supply.
    Molecular Plant 10/2013; · 6.61 Impact Factor
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    ABSTRACT: Many plants accumulate substantial starch reserves in their leaves during the day, and remobilise them at night to provide carbon and energy for maintenance and growth. In this paper we explore the role of a sugar signalling metabolite, trehalose-6-phosphate (Tre6P), in regulating the accumulation and turnover of transitory starch in Arabidopsis leaves. Ethanol-induced overexpression of trehalose-phosphate synthase (TPS) during the day increased Tre6P levels up to 11-fold. There was a transient increase in the rate of starch accumulation in the middle of the day, but this was not linked to reductive activation of ADP-glucose pyrophosphorylase. A 2 to 3-fold increase in Tre6P during the night led to significant inhibition of starch degradation. Maltose and maltotriose did not accumulate, suggesting that Tre6P affects an early step in the pathway of starch degradation in the chloroplasts. Starch granules isolated from induced plants had a higher Pi content than granules from non-induced control plants, consistent with either disruption of the phosphorylation-dephosphorylation cycle that is essential for efficient starch breakdown, or with inhibition of starch hydrolysis by β-amylase. Non-aqueous fractionation of leaves showed that Tre6P is predominantly located in the cytosol, with estimated in vivo Tre6P concentrations of 4-7 µM in the cytosol, 0.2-0.5 µM in the chloroplasts and 0.05 µM in the vacuole. It is proposed that Tre6P is a component in a signalling pathway that mediates feedback regulation of starch breakdown by sucrose, potentially linking starch turnover to demand for sucrose by growing sink organs at night.
    Plant physiology 09/2013; · 7.39 Impact Factor
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    ABSTRACT: Arabidopsis thaliana mutants lacking the SS4 isoform of starch synthase have strongly reduced numbers of starch granules per chloroplast, suggesting that SS4 is necessary for the normal generation of starch granules. To establish whether it plays a direct role in this process, we investigated the circumstances in which granules are formed in ss4 mutants. Starch granule numbers and distribution and the accumulation of starch synthase substrates and products were investigated during ss4 leaf development, and in ss4 mutants carrying mutations or transgenes that affect starch turnover or chloroplast volume. We found that immature ss4 leaves have no starch granules, but accumulate high concentrations of the starch synthase substrate ADPglucose. Granule numbers are partially restored by elevating the capacity for glucan synthesis (via expression of bacterial glycogen synthase) or by increasing the volumes of individual chloroplasts (via introduction of arc mutations). However, these granules are abnormal in distribution, size and shape. SS4 is an essential component of a mechanism that coordinates granule formation with chloroplast division during leaf expansion and determines the abundance and the flattened, discoid shape of leaf starch granules.
    New Phytologist 08/2013; · 6.55 Impact Factor
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    ABSTRACT: Starch synthase 4 (SS4) is required for proper starch granule initiation in Arabidopsis thaliana, although starch synthase 3 (SS3) can partially replace its function. Unlike other starch deficient mutants, ss4 and ss3/ss4 mutants grow poorly even under long-day conditions. They have less chlorophyll and carotenoids than wild type (WT) and lower maximal rates of photosynthesis. There is evidence of photo-oxidative damage of the photosynthetic apparatus in the mutants from chlorophyll a fluorescence parameters and their high levels of malondialdehyde. Metabolite profiling revealed that ss3/ss4 accumulates over 170 times more ADP-glucose than WT plants. Restricting ADP-glucose synthesis, by introducing mutations in the plastidial phosphoglucomutase (pgm1) or the small subunit of ADP-glucose pyrophosphorylase (aps1), largely restored photosynthetic capacity and growth in pgm1/ss3/ss4 and aps1/ss3/ss4 triple mutants. It is proposed that the accumulation of ADP-glucose in the ss3/ss4 mutant sequesters a large part of the plastidial pools of adenine nucleotides, which limits photophosphorylation leading to photo-oxidative stress, causing the chlorotic and stunted growth phenotypes of the plants.
    Plant physiology 07/2013; · 7.39 Impact Factor
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    ABSTRACT: Full text URL: Trehalose is a non-reducing disaccharide that is used as an osmolyte, transport sugar, carbon reserve and stress protectant in a wide range of organisms. In plants, trehalose 6-phosphate (Tre6P), the intermediate of trehalose biosynthesis, is thought to be a signal of sucrose status. Trehalose itself may play a role in pathogenic and symbiotic plant-microbe interactions, in responses to abiotic stress and in developmental signalling, but its precise functions are unknown. A major obstacle to investigating its function is the technical difficulty of measuring the very low levels of trehalose usually found in plant tissues, as most of the established trehalose assays lack sufficient specificity and/or sensitivity. A kinetic assay for trehalose was established using recombinant Escherichia coli cytoplasmic trehalase (treF), which was shown to be highly specific for trehalose. Hydrolysis of trehalose to glucose is monitored fluorometrically and the trehalose content of the tissue extract is determined from an internal calibration curve. The assay is linear for 0.2-40 pmol trehalose, and recoveries of trehalose were >=88%. A. thaliana Col-0 rosettes contain about 20--30 nmol g-1FW of trehalose, increasing to about 50--60 nmol g-1FW in plants grown at 8[degree sign]C. Trehalose is not correlated with sucrose content, whereas a strong correlation between Tre6P and sucrose was confirmed. The trehalose contents of ear inflorescence primordia from the maize ramosa3 mutant and wild type plants were 6.6+/-2.6 nmol g-1FW and 19.0+/-12.7 nmol g-1FW, respectively. The trehalose:Tre6P ratios in the ramosa3 and wild-type primordia were 2.43+/-0.85 and 6.16+/-3.45, respectively. The fluorometric assay is highly specific for trehalose and sensitive enough to measure the trehalose content of very small amounts of plant tissue. Chilling induced a 2-fold accumulation of trehalose in A. thaliana rosettes, but the levels were too low to make a substantial quantitative contribution to osmoregulation. Trehalose is unlikely to function as a signal of sucrose status. The abnormal inflorescence branching phenotype of the maize ramosa3 mutant might be linked to a decrease in trehalose levels in the inflorescence primordia or a downward shift in the trehalose:Tre6P ratio.
    Plant Methods 06/2013; 9(1):21. · 2.59 Impact Factor
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    ABSTRACT: Photosynthesis is the basis for life, and its optimization is a key biotechnological aim given the problems of population explosion and environmental deterioration. We describe a method to resolve intracellular fluxes in intact Arabidopsis thaliana rosettes based on time-dependent labeling patterns in the metabolome. Plants photosynthesizing under limiting irradiance and ambient CO(2) in a custom-built chamber were transferred into a (13)CO(2)-enriched environment. The isotope labeling patterns of 40 metabolites were obtained using liquid or gas chromatography coupled to mass spectrometry. Labeling kinetics revealed striking differences between metabolites. At a qualitative level, they matched expectations in terms of pathway topology and stoichiometry, but some unexpected features point to the complexity of subcellular and cellular compartmentation. To achieve quantitative insights, the data set was used for estimating fluxes in the framework of kinetic flux profiling. We benchmarked flux estimates to four classically determined flux signatures of photosynthesis and assessed the robustness of the estimates with respect to different features of the underlying metabolic model and the time-resolved data set.
    The Plant Cell 02/2013; · 9.58 Impact Factor
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    ABSTRACT: The timing of the induction of flowering determines to a large extent the reproductive success of plants. Plants integrate diverse environmental and endogenous signals to ensure the timely transition from vegetative growth to flowering. Carbohydrates are thought to play a crucial role in the regulation of flowering, and trehalose-6-phosphate (T6P) has been suggested to function as a proxy for carbohydrate status in plants. The loss of TREHALOSE-6-PHOSPHATE SYNTHASE 1 (TPS1) causes Arabidopsis thaliana to flower extremely late, even under otherwise inductive environmental conditions. This suggests that TPS1 is required for the timely initiation of flowering. We show that the T6P pathway affects flowering both in the leaves and at the shoot meristem, and integrate TPS1 into the existing genetic framework of flowering-time control.
    Science 02/2013; 339(6120):704-7. · 31.48 Impact Factor
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    ABSTRACT: Changes in carbohydrate metabolism during grape berry development play a central role in shaping the final composition of the fruit. The present work aimed to identify metabolic switches during grape development and to provide insights into the timing of developmental regulation of carbohydrate metabolism. Metabolites from central carbon metabolism were measured using high-pressure anion-exchange chromatography coupled to tandem mass spectrometry and enzymatic assays during the development of grape berries from either field-grown vines or fruiting cuttings grown in the greenhouse. Principal component analysis readily discriminated the various stages of berry development, with similar trajectories for field-grown and greenhouse samples. This showed that each stage of fruit development had a characteristic metabolic profile and provided compelling evidence that the fruit-bearing cuttings are a useful model system to investigate regulation of central carbon metabolism in grape berry. The metabolites measured showed tight coordination within their respective pathways, clustering into sugars and sugar-phosphate metabolism, glycolysis, and the tricarboxylic acid cycle. In addition, there was a pronounced shift in metabolism around veraison, characterized by rapidly increasing sugar levels and decreasing organic acids. In contrast, glycolytic intermediates and sugar phosphates declined before veraison but remained fairly stable post-veraison. In summary, these detailed and comprehensive metabolite analyses revealed the timing of important switches in primary carbohydrate metabolism, which could be related to transcriptional and developmental changes within the berry to achieve an integrated understanding of grape berry development. The results are discussed in a meta-analysis comparing metabolic changes in climacteric versus non-climacteric fleshy fruits.
    Journal of Experimental Botany 01/2013; · 5.79 Impact Factor
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    ABSTRACT: Introduction of microbial trehalose biosynthesis enzymes has been reported to enhance abiotic stress resistance in plants, but also resulted in undesirable traits. Here we present an approach for engineering drought stress tolerance by modifying the endogenous trehalase activity in Arabidopsis thaliana. AtTRE1 encodes the Arabidopsis trehalase, the only enzyme known in this species to specifically hydrolyze trehalose into glucose. AtTRE1 over-expressing and Attre1 mutant lines were constructed and tested for their performance in drought stress assays. AtTRE1 over-expressing plants had decreased trehalose levels and recovered better after drought stress, whereas Attre1 mutants had elevated trehalose contents and exhibited a drought susceptible phenotype. Leaf detachment assays showed that Attre1 mutants lose water faster than wild type plants, whereas AtTRE1 over-expressing plants have a better water retaining capacity. In vitro studies revealed that ABA-mediated closure of stomata is impaired in Attre1 lines, whereas the AtTRE1 over-expressors are more sensitive towards ABA-dependent stomatal closure. This observation is further supported by the altered leaf temperatures seen in trehalase modified plantlets during in vivo drought stress studies. Our results show that over-expression of plant trehalase improves drought stress tolerance in Arabidopsis and that trehalase plays a role in the regulation of stomatal closure in plant drought stress response.
    Plant physiology 01/2013; · 7.39 Impact Factor
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    ABSTRACT: The crucial role of carbohydrate in plant growth and morphogenesis is widely recognized. In this study we describe the characterization of nana, a dwarf Arabidopsis thaliana mutant impaired in carbohydrate metabolism. We show that the nana dwarf phenotype was accompanied by altered leaf morphology and a delayed flowering time. Our genetic and molecular data indicate that the mutation in nana is due to a T-DNA insertion in the promoter region of a gene encoding a chloroplast-located aspartyl protease that alters its pattern of expression. Overexpression of the gene (oxNANA) phenocopies the mutation. Both nana and oxNANA display alterations in carbohydrate content, and the extent of these changes varies depending on growth light intensity. In particular, in low light soluble sugars levels are lower and do not show the daily fluctuations observed in wild type plants. Moreover, nana and oxNANA are defective in expression of some genes implicated in sugar metabolism and photosynthetic light harvesting. Interestingly, some chloroplast-encoded genes as well as genes, whose products seem to be involved in the retrograde signaling, appear to be down-regulated. These findings suggest that the NANA aspartic protease has an important regulatory function in chloroplasts that not only influences photosynthetic carbon metabolism but also plastid and nuclear gene expression.
    Plant physiology 09/2012; · 7.39 Impact Factor
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    ABSTRACT: Trehalose is a nonreducing sugar used as a reserve carbohydrate and stress protectant in a variety of organisms. While higher plants typically do not accumulate high levels of trehalose, they encode large families of putative trehalose biosynthesis genes. Trehalose biosynthesis in plants involves a two-step reaction in which trehalose-6-phosphate (T6P) is synthesized from UDP-glucose and glucose-6-phosphate (catalyzed by T6P synthase [TPS]), and subsequently dephosphorylated to produce the disaccharide trehalose (catalyzed by T6P phosphatase [TPP]). In Arabidopsis (Arabidopsis thaliana), 11 genes encode proteins with both TPS- and TPP-like domains but only one of these (AtTPS1) appears to be an active (TPS) enzyme. In addition, plants contain a large family of smaller proteins with a conserved TPP domain. Here, we present an in-depth analysis of the 10 TPP genes and gene products in Arabidopsis (TPPA-TPPJ). Collinearity analysis revealed that all of these genes originate from whole-genome duplication events. Heterologous expression in yeast (Saccharomyces cerevisiae) showed that all encode active TPP enzymes with an essential role for some conserved residues in the catalytic domain. These results suggest that the TPP genes function in the regulation of T6P levels, with T6P emerging as a novel key regulator of growth and development in higher plants. Extensive gene expression analyses using a complete set of promoter-β-glucuronidase/green fluorescent protein reporter lines further uncovered cell- and tissue-specific expression patterns, conferring spatiotemporal control of trehalose metabolism. Consistently, phenotypic characterization of knockdown and overexpression lines of a single TPP, AtTPPG, points to unique properties of individual TPPs in Arabidopsis, and underlines the intimate connection between trehalose metabolism and abscisic acid signaling.
    Plant physiology 08/2012; 160(2):884-96. · 7.39 Impact Factor
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    ABSTRACT: Low temperatures damage many temperate crops, including grapevine, which, when exposed to chilling, can be affected by symptoms ranging from reduced yield up to complete infertility. We have previously demonstrated that Burkholderia phytofirmans PsJN, a plant growth-promoting rhizobacteria (PGPR) that colonizes grapevine, is able to reduce chilling-induced damage. We hypothesized that the induced tolerance may be explained at least partly by the impact of bacteria on grapevine photosynthesis or carbohydrate metabolism during cold acclimation. To investigate this hypothesis, we monitored herein the fluctuations of photosynthesis parameters (net photosynthesis [P(n)], intercellular CO(2) concentration, stomatal conductances, ΦPSII, and total chlorophyll concentration), starch, soluble sugars (glucose, fructose, saccharose, mannose, raffinose, and maltose), and their precursors during 5 days of chilling exposure (4°C) on grapevine plantlets. Bacterization affects photosynthesis in a non-stomatal dependent pattern and reduced long-term impact of chilling on P(n). Furthermore, all studied carbohydrates known to be involved in cold stress tolerance accumulate in non-chilled bacterized plantlets, although some of them remained more concentrated in the latter after chilling exposure. Overall, our results suggest that modification of carbohydrate metabolism in bacterized grapevine plantlets may be one of the major effects by which this PGPR reduces chilling-induced damage.
    Molecular Plant-Microbe Interactions 04/2012; 25(4):496-504. · 4.46 Impact Factor
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    ABSTRACT: During the last decade, there has been growing interest in the role of trehalose metabolism in tolerance to abiotic stress in higher plants, especially cold stress. So far, this metabolism has not yet been studied in Vitis vinifera L., despite the economic importance of this crop. The goal of this paper was to investigate the involvement of trehalose metabolism in the response of grapevine to chilling stress, and to compare the response in plants bacterised with Burkholderia phytofirmans strain PsJN, a plant growth-promoting rhizobacterium that confers grapevine chilling tolerance, with mock-inoculated plants. In silico analysis revealed that the V. vinifera L. genome contains genes encoding the enzymes responsible for trehalose synthesis and degradation. Transcript analysis showed that these genes were differentially expressed in various plant organs, and we also characterised their response to chilling. Both trehalose and trehalose 6-phosphate (T6P) were present in grapevine tissues and showed a distinct pattern of accumulation upon chilling. Our results suggest a role for T6P as the main active molecule in the metabolism upon chilling, with a possible link with sucrose metabolism. Furthermore, plants colonised by B. phytofirmans and cultivated at 26°C accumulated T6P and trehalose in stems and leaves at concentrations similar to non-bacterised plants exposed to chilling temperatures for 1 day. Overall, our data suggest that T6P and trehalose accumulate upon chilling stress in grapevine and might participate in the resistance to chilling stress conferred by B. phytofirmans.
    Planta 02/2012; 236(2):355-69. · 3.38 Impact Factor

Publication Stats

890 Citations
228.57 Total Impact Points


  • 2014
    • University of Nebraska at Lincoln
      • Department of Agronomy and Horticulture
      Lincoln, Nebraska, United States
  • 2006–2014
    • Max Planck Institute of Molecular Plant Physiology
      • Division of Molecular Physiology
      Potsdam, Brandenburg, Germany
  • 2013
    • University of Leuven
      Louvain, Flemish, Belgium
    • Laboratório Nacional de Ciência e Tecnologia do Bioetanol
      Conceição de Campinas, São Paulo, Brazil
  • 2009–2013
    • John Innes Centre
      • Department of Metabolic Biology
      Norwich, England, United Kingdom
  • 2012
    • Scuola Superiore Sant'Anna
      • Institute of Life Sciences
      Pisa, Tuscany, Italy
    • Vlaams Instituut voor Biotechnologie
      • Department of Plant Systems Biology, UGent
      Gand, Flemish, Belgium