All plant cells are surrounded by a cell wall that determines the directionality of cell growth and protects the cell against its environment. Plant cell walls are comprised primarily of ...polysaccharides and represent the largest sink for photosynthetically fixed carbon, both for individual plants and in the terrestrial biosphere as a whole. Cell wall synthesis is a highly sophisticated process, involving multiple enzymes and metabolic intermediates, intracellular trafficking of proteins and cell wall precursors, assembly of cell wall polymers into the extracellular matrix, remodeling of polymers and their interactions, and recycling of cell wall sugars. In this review we discuss how newly fixed carbon, in the form of UDP-glucose and other nucleotide sugars, contributes to the synthesis of cell wall polysaccharides, and how cell wall synthesis is influenced by the carbon status of the plant, with a focus on the model species Arabidopsis (Arabidopsis thaliana).
In this review we discuss how newly fixed carbon, in the form of UDP-glucose and other nucleotide sugars, contributes to the synthesis of cell wall polysaccharides, and how cell wall synthesis is influenced by the carbon status of the plant, with a focus on Arabidopsis thaliana.
Trehalose metabolism in plants Lunn, John Edward; Delorge, Ines; Figueroa, Carlos María ...
The Plant journal : for cell and molecular biology,
August 2014, Volume:
79, Issue:
4
Journal Article
Peer reviewed
Open access
Summary
Trehalose is a quantitatively important compatible solute and stress protectant in many organisms, including green algae and primitive plants. These functions have largely been replaced by ...sucrose in vascular plants, and trehalose metabolism has taken on new roles. Trehalose is a potential signal metabolite in plant interactions with pathogenic or symbiotic micro‐organisms and herbivorous insects. It is also implicated in responses to cold and salinity, and in regulation of stomatal conductance and water‐use efficiency. In plants, as in other eukaryotes and many prokaryotes, trehalose is synthesized via a phosphorylated intermediate, trehalose 6‐phosphate (Tre6P). A meta‐analysis revealed that the levels of Tre6P change in parallel with sucrose, which is the major product of photosynthesis and the main transport sugar in plants. We propose the existence of a bi‐directional network, in which Tre6P is a signal of sucrose availability and acts to maintain sucrose concentrations within an appropriate range. Tre6P influences the relative amounts of sucrose and starch that accumulate in leaves during the day, and regulates the rate of starch degradation at night to match the demand for sucrose. Mutants in Tre6P metabolism have highly pleiotropic phenotypes, showing defects in embryogenesis, leaf growth, flowering, inflorescence branching and seed set. It has been proposed that Tre6P influences plant growth and development via inhibition of the SNF1‐related protein kinase (SnRK1). However, current models conflict with some experimental data, and do not completely explain the pleiotropic phenotypes exhibited by mutants in Tre6P metabolism. Additional explanations for the diverse effects of alterations in Tre6P metabolism are discussed.
Many plants accumulate substantial starch reserves in their leaves during the day and remobilize them at night to provide carbon and energy for maintenance and growth. In this paper, we explore the ...role of a sugar-signaling metabolite, trehalose-6-phosphate (Tre6P), in regulating the accumulation and turnover of transitory starch in Arabidopsis (Arabidopsis thaliana) leaves. Ethanol-induced overexpression of trehalose-phosphate synthase 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 orthophosphate content than granules from noninduced control plants, consistent either with disruption of the phosphorylation-dephosphorylation cycle that is essential for efficient starch breakdown or with inhibition of starch hydrolysis by β-amylase. Nonaqueous fractionation of leaves showed that Tre6P is predominantly located in the cytosol, with estimated in vivo Tre6P concentrations of 4 to 7 μM in the cytosol, 0.2 to 0.5 μM in the chloroplasts, and 0.05 μM in the vacuole. It is proposed that Tre6P is a component in a signaling pathway that mediates the feedback regulation of starch breakdown by sucrose, potentially linking starch turnover to demand for sucrose by growing sink organs at night.
In climacteric fruit-bearing species, the onset of fruit ripening is marked by a transient rise in respiration rate and autocatalytic ethylene production, followed by rapid deterioration in fruit ...quality. In non-climacteric species, there is no increase in respiration or ethylene production at the beginning or during fruit ripening. Melon is unusual in having climacteric and non-climacteric varieties, providing an interesting model system to compare both ripening types. Transcriptomic analysis of developing melon fruits from Védrantais and Dulce (climacteric) and Piel de sapo and PI 161375 (non-climacteric) varieties was performed to understand the molecular mechanisms that differentiate the two fruit ripening types.
Fruits were harvested at 15, 25, 35 days after pollination and at fruit maturity. Transcript profiling was performed using an oligo-based microarray with 75 K probes. Genes linked to characteristic traits of fruit ripening were differentially expressed between climacteric and non-climacteric types, as well as several transcription factor genes and genes encoding enzymes involved in sucrose catabolism. The expression patterns of some genes in PI 161375 fruits were either intermediate between. Piel de sapo and the climacteric varieties, or more similar to the latter. PI 161375 fruits also accumulated some carotenoids, a characteristic trait of climacteric varieties.
Simultaneous changes in transcript abundance indicate that there is coordinated reprogramming of gene expression during fruit development and at the onset of ripening in both climacteric and non-climacteric fruits. The expression patterns of genes related to ethylene metabolism, carotenoid accumulation, cell wall integrity and transcriptional regulation varied between genotypes and was consistent with the differences in their fruit ripening characteristics. There were differences between climacteric and non-climacteric varieties in the expression of genes related to sugar metabolism suggesting that they may be potential determinants of sucrose content and post-harvest stability of sucrose levels in fruit. Several transcription factor genes were also identified that were differentially expressed in both types, implicating them in regulation of ripening behaviour. The intermediate nature of PI 161375 suggested that classification of melon fruit ripening behaviour into just two distinct types is an over-simplification, and that in reality there is a continuous spectrum of fruit ripening behaviour.
Mal de Río Cuarto virus (MRCV) infects several monocotyledonous species including maize and wheat. Infected plants show shortened internodes, partial sterility, increased tillering and reduced root ...length. To better understand the molecular basis of the plant-virus interactions leading to these symptoms, we combined RNA sequencing with metabolite and hormone measurements.
More than 3000 differentially accumulated transcripts (DATs) were detected in MRCV-infected wheat plants at 21 days post inoculation compared to mock-inoculated plants. Infected plants exhibited decreased levels of TaSWEET13 transcripts, which are involved in sucrose phloem loading. Soluble sugars, starch, trehalose 6-phosphate (Tre6P), and organic and amino acids were all higher in MRCV-infected plants. In addition, several transcripts related to plant hormone metabolism, transport and signalling were increased upon MRCV infection. Transcripts coding for GA20ox, D14, MAX2 and SMAX1-like proteins involved in gibberellin biosynthesis and strigolactone signalling, were reduced. Transcripts involved in jasmonic acid, ethylene and brassinosteroid biosynthesis, perception and signalling and in auxin transport were also altered. Hormone measurements showed that jasmonic acid, brassinosteroids, abscisic acid and indole-3-acetic acid were significantly higher in infected leaves.
Our results indicate that MRCV causes a profound hormonal imbalance that, together with alterations in sugar partitioning, could account for the symptoms observed in MRCV-infected plants.
To investigate whether the transcriptional response to carbon (C) depletion and sucrose resupply depends on the duration and severity of the C depletion, Arabidopsis seedlings were grown in liquid ...culture and harvested 3, 6, 12, 24, 48 and 72 h after removing sucrose from the medium and 30 min after resupplying sucrose at each time. Expression profiling revealed early transcriptional inhibition of cell wall synthesis and remodelling of signalling, followed by induction of C recycling and photosynthesis and general inhibition of growth. The temporal sequence differed from the published response to progressive exhaustion of C during a night and extended night in vegetatively growing plants. The response to sucrose readdition was conserved across the C‐depletion time course. Intriguingly, the vast majority of rapidly responding transcripts decreased rather than increased. The majority of transcripts that respond rapidly to sucrose and many transcripts that respond during C depletion also decrease after treating seedlings with the transcriptional inhibitor cordycepin A. Comparison with published responses to overexpression of otsA, AKIN10 and bZIP11 revealed that many genes that respond to C depletion, and especially sucrose resupply, respond to one or more of these C‐signalling components. Thus, multiple factors contribute to C responsiveness, including many signalling components, transcriptional regulation and transcript turnover.
There have been many studies of the response of gene expression to chronic C starvation, but little is known about the temporal response during progressive C depletion. In studies with Arabidopsis seedlings in liquid culture, we report progressive changes in transcript levels, with early repression of cell wall synthesis and slower repression of growth‐related processes and induction of catabolism and photosynthesis. The response to sucrose resupply was conserved and dominated by transcripts that decreased. Many transcripts that respond during C depletion and most of the transcripts that respond to sucrose readdition also decrease after treating seedlings with the transcriptional inhibitor cordycepin A, revealing an important role for transcript turnover in the response to sucrose.
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.
Sugars are simple carbohydrates composed primarily of carbon, hydrogen, and oxygen. They play a central role in metabolism as sources of energy and as building blocks for synthesis of structural and ...nonstructural polymers. Many different techniques have been used to measure sugars, including refractometry, colorimetric and enzymatic assays, gas chromatography, high-performance liquid chromatography, and nuclear magnetic resonance spectroscopy. In this chapter we describe a method that combines an initial separation of sugars by high-performance anion-exchange chromatography (HPAEC) with detection and quantification by tandem mass spectrometry (MS/MS). This combination of techniques provides exquisite specificity, allowing measurement of a diverse range of high- and low-abundance sugars in biological samples. This method can also be used for isotopomer analysis in stable-isotope labeling experiments to measure metabolic fluxes.
Evolution of Sucrose Synthesis LUNN, John Edward
Plant physiology (Bethesda),
04/2002, Volume:
128, Issue:
4
Journal Article
Peer reviewed
Open access
Cyanobacteria and proteobacteria (purple bacteria) are the only prokaryotes known to synthesize sucrose (Suc). Suc-P synthase, Suc-phosphatase (SPP), and Suc synthase activities have previously been ...detected in several cyanobacteria, and genes coding for Suc-P synthase (sps) and Suc synthase (sus) have been cloned from Synechocystis sp. PCC 6803 and Anabaena (Nostoc) spp., respectively. An open reading frame in the Synechocystis genome encodes a predicted 27-kD polypeptide that shows homology to the maize (Zea mays) SPP. Heterologous expression of this putative spp gene in Escherichia coli, reported here, confirmed that this open reading frame encodes a functional SPP enzyme. The Synechocystis SPP is highly specific for Suc-$6^{\text{F}}$-P (Km = 7.5 μM) and is Mg2+ dependent (Ka = 70 μM), with a specific activity of 46 μmol $\text{min}^{-1}\ \text{mg}^{-1}$ protein. Like the maize SPP, the Synechocystis SPP belongs to the haloacid dehalogenase superfamily of phosphatases/hydrolases. Searches of sequenced microbial genomes revealed homologs of the Synechocystis sps gene in several other cyanobacteria (Nostoc punctiforme, Prochlorococcus marinus strains MED4 and MIT9313, and Synechococcus sp. WH8012), and in three proteobacteria (Acidithiobacillus ferrooxidans, Magnetococcus sp. MC1, and Nitrosomonas europaea). Homologs of the Synechocystis spp gene were found in Magnetococcus sp. MC1 and N. punctiforme, and of the Anabaena sus gene in N. punctiforme and N. europaea. From analysis of these sequences, it is suggested that Suc synthesis originated in the proteobacteria or a common ancestor of the proteobacteria and cyanobacteria.
Plants respond to low carbon supply by massive reprogramming of the transcriptome and metabolome. We show here that the carbon starvation-induced NAC (for NO APICAL MERISTEM/ARABIDOPSIS TRANSCRIPTION ...ACTIVATION FACTOR/CUP-SHAPED COTYLEDON) transcription factor Arabidopsis (Arabidopsis thaliana)Transcription Activation Factor1(ATAF1) plays an important role in this physiological process. We identifiedTREHALASE1, the only trehalase-encoding gene in Arabidopsis, as a direct downstream target of ATAF1. Overexpression of ATAF1 activatesTREHALASE1expression and leads to reduced trehalose-6-phosphate levels and a sugar starvation metabolome. In accordance with changes in expression of starch biosynthesis- and breakdown-related genes, starch levels are generally reduced inATAF1overexpressors but elevated inataf1knockout plants. At the global transcriptome level, genes affected by ATAF1 are broadly associated with energy and carbon starvation responses. Furthermore, transcriptional responses triggered by ATAF1 largely overlap with expression patterns observed in plants starved for carbon or energy supply. Collectively, our data highlight the existence of a positively acting feedforward loop betweenATAF1expression, which is induced by carbon starvation, and the depletion of cellular carbon/energy pools that is triggered by the transcriptional regulation of downstream gene regulatory networks by ATAF1.
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