Sugars not only fuel cellular carbon and energy metabolism but also play pivotal roles as signaling molecules. The experimental amenability of yeast as a unicellular model system has enabled the discovery of multiple sugar sensors and signaling pathways. In plants, different sugar signals are generated by photosynthesis and carbon metabolism in source and sink tissues to modulate growth, development, and stress responses. Genetic analyses have revealed extensive interactions between sugar and plant hormone signaling, and a central role for hexokinase (HXK) as a conserved glucose sensor. Diverse sugar signals activate multiple HXK-dependent and HXKindependent pathways and use different molecular mechanisms to control transcription, translation, protein stability and enzymatic activity. Important and complex roles for Snf1-related kinases (SnRKs), extracellular sugar sensors, and trehalose metabolism in plant sugar signaling are now also emerging.

https://molbio.mgh.harvard.edu/sheenweb/reprints/ARPB06sugar.pdf

Sugar Sensing and Signaling in Plants: Conserved and Novel Mechanisms

The concept that photosynthetic flux is influenced by the accumulation of photo-assimilate persisted for 100 years before receiving any strong experimental support. Precise analysis of the mechanisms of photosynthetic responses to sink activity required the development of a battery of appropriate molecular techniques and has benefited from contemporary interest in the effects of elevated CO2 on photosynthesis. Photosynthesis is one of the most highly integrated and regulated metabolic processes to maximize the use of available light, to minimize the damaging effects of excess light and to optimize the use of limiting carbon and nitrogen resources. Hypotheses of feedback regulation must take account of this integration. In the short term, departure from homeostasis can lead to redox signals, which cause rapid changes in the transcription of genes encoding photosystems I and II. End-product synthesis can exert short-term metabolic feedback control through Pi recycling. Beyond this, carbohydrate accumulation in leaves when there is an imbalance between source and sink at the whole plant level can lead to decreased expression of photosynthetic genes and accelerated leaf senescence. In a high CO2 world this may become a more prevalent feature of photosynthetic regulation. However, sink regulation of photosynthesis is highly dependent on the physiology of the rest of the plant. This physiological state regulates photosynthesis through signal transduction pathways that co-ordinate the plant carbon : nitrogen balance, which match photosynthetic capacity to growth and storage capacity and underpin and can override the direct short-term controls of photosynthesis by light and CO2. Photosynthate supply and phytohormones, particularly cytokinins, interact with nitrogen supply to control the expression of photosynthesis genes, the development of leaves and the whole plant nitrogen distribution, which provides the dominant basis for sink regulation of photosynthesis.

Sink regulation of photosynthesis

In addition to their essential roles as substrates in carbon and energy metabolism and in polymer biosynthesis, sugars have important hormone-like functions as primary messengers in signal transduction. The pivotal role of sugars as signaling molecules is well illustrated by the variety of sugar

/pdf/sugar-sensing-and-signaling-in-plants-2qcsw68ddt.pdf

Sugar Sensing and Signaling in Plants

In plants, carbon (C) molecules provide building blocks for biomass production, fuel for energy, and exert signalling roles to shape development and metabolism. Accordingly, plant growth is well correlated with light interception and energy conversion through photosynthesis. Because water deficits close stomata and thus reduce C entry, it has been hypothesised that droughted plants are under C starvation and their growth under C limitation. In this review, these points are questioned by combining literature review with experimental and modelling illustrations in various plant organs and species. First, converging evidence is gathered from the literature that water deficit generally increases C concentration in plant organs. The hypothesis is raised that this could be due to organ expansion (as a major C sink) being affected earlier and more intensively than photosynthesis (C source) and metabolism. How such an increase is likely to interact with C signalling is not known. Hence, the literature is reviewed for possible links between C and stress signalling that could take part in this interaction. Finally, the possible impact of water deficit-induced C accumulation on growth is questioned for various sink organs of several species by combining published as well as new experimental data or data generated using a modelling approach. To this aim, robust correlations between C availability and sink organ growth are reported in the absence of water deficit. Under water deficit, relationships weaken or are modified suggesting release of the influence of C availability on sink organ growth. These results are interpreted as the signature of a transition from source to sink growth limitation under water deficit.

/pdf/water-deficits-uncouple-growth-from-photosynthesis-increase-4n7vhk7pts.pdf

Water deficits uncouple growth from photosynthesis, increase C content, and modify the relationships between C and growth in sink organs

https://molbio.mgh.harvard.edu/sheenweb/reprints/Elena%2008%20Cell%20Review.pdf

Convergent energy and stress signaling

One of the major protein kinases (PK(III)) that phosphorylates serine-158 of spinach sucrose-phosphate synthase (SPS), which is responsible for light/dark modulation of activity, is known to be a member of the SNF1-related family of protein kinases. In the present study, we have developed a fluorescence-based continuous assay for measurement of PK(III) activity. Using the continuous assay, along with the fixed-time-point (32)P-incorporation assay, we demonstrate that PK(III) activity is inhibited by glucose-6-phosphate (Glc-6-P). Relative inhibition by Glc-6-P was increased by decreasing pH from 8. 5 to 5.5 and by reducing the concentration of Mg(2+) in the assay from 10 to 2 mM. Under likely physiological conditions (pH 7.0 and 2 mM Mg(2+)), 10 mM Glc-6-P inhibited kinase activity approximately 70%. Inhibition by Glc-6-P could not be ascribed to contaminants in the commercial preparations. Other metabolites inhibited PK(III) in the following order: Glc-6-P > mannose-6-P, fructose-1,6P(2) > ribose-5-P, 3-PGA, fructose-6-P. Inorganic phosphate, Glc, and AMP were not inhibitory, and free Glc did not reverse the inhibition by Glc-6-P. Because SNF1-related protein kinases are thought to function broadly in the regulation of enzyme activity and gene expression, Glc-6-P inhibition of PK(III) activity potentially provides a mechanism for metabolic regulation of the reactions catalyzed by these important protein kinases.

Zvi Plaut

Papers

Regulation of a plant SNF1-related protein kinase by glucose-6-phosphate.