Plant gene responses to changing carbohydrate status can vary markedly Some genes are induced, some are repressed, and others are minimally affected As in microorganisms, sugar-sensitive plant genes are part of an ancient system of cellular adjustment to critical nutrient availability However, in multicellular plants, sugar-regulated expression also provides a mechanism for control of resource distribution among tissues and organs Carbohydrate depletion upregulates genes for photosynthesis, remobilization, and export, while decreasing mRNAs for storage and utilization Abundant sugar levels exert opposite effects through a combination of gene repression and induction Long-term changes in metabolic activity, resource partitioning, and plant form result Sensitivity of carbohydrate-responsive gene expression to environmental and developmental signals further enhances its potential to aid acclimation The review addresses the above from molecular to whole-plant levels and considers emerging models for sensing and transducing carbohydrate signals to responsive genes

Carbohydrate-modulated gene expression in plants.

Summary
This review reports on the processes associated with carbon transfer and metabolism in leaves and growing organs and the role of long-distance transport and vascular links in the regulation of carbon partitioning in plants. Partitioning is clearly influenced by both the supply and demand for photosynthate and is moderated by vascular connections and the storage capacity of the leaves and pathway tissues. However there appears to be little more than circumstantial evidence either that short distance transfer of carbon within either the source or the sink, or that long-distance transport in the phloem, are limiting photosynthesis or growth directly. Although individual biochemical and physiological processes relating to photosynthesis and growth may be well understood, the factors primarily responsible for the control of carbon partitioning in plants have not been clearly identified. There is a need for a greater understanding of organ initiation and development (source and sink formation and potential size), the clear identification of whether growth is sink or source limited (including possible sink-controlled photosynthesis) and a detailed assessment of the role of storage in buffering developmental and environmental changes in sink and source activity. Also more information is needed on the role of hormonal and nutritional factors in regulating source and sink activity (organ interactions not directly associated with carbon transfer).

https://nph.onlinelibrary.wiley.com/doi/pdf/10.1111/j.1469-8137.1990.tb00524.x

Tansley Review No. 27 The control of carbon partitioning in plants

One of the key features of plants is their ability to reduce carbon dioxide in the presence of sunlight and water to sugars, and the subsequent transport of assimilated carbon to the nonphotosynthetic tissues (sink tissues). In most plants, the transported sugar is Suc, a nonreducing disaccharide,

Invertases. Primary structures, functions, and roles in plant development and sucrose partitioning.

The timing of the transition from vegetative growth to flowering is of paramount importance in agriculture, horticulture, and plant breeding because flowering is the first step of sexual reproduction. Studies to understand how this transition is controlled have occupied countless physiologists during the past half century and have produced an almost unmanageably large amount of information (Bernier et al., 1981a; Halevy, 1985-1989; Bernier, 1988; Kinet, 1993). A majority of plants use environmental cues to regulate the transition to flowering because all individuals of a species must flower synchronously for successful outcrossing and because all species must complete their sexual reproduction under favorable externa1 conditions. Any environmental variables exhibiting regular seasonal changes are potential factors that control the transition to flowering. The major factors are photoperiod, temperature, and water availability. Plants that do not require a particular photoperiod or temperature to flower, i.e., the so-called “autonomous-flowering” plants, are usually sensitive to irradiance. The environmental factors are perceived by different parts of the plant. Photoperiod and irradiance are perceived mainly by mature leaves in intact plants. Temperature is perceived by all plant parts, although low temperature (vernalization) is often perceived mainly by the shoot apex. Water availability is perceived by the root system. There are strong interactions between these different factors, so that each factor can change the threshold value for the effectiveness of the others. Plants, as opportunists, will thus make use of a different critical factor in different environments. Melilotus officinalis, for example, is a biennial with a vernalization requirement in temperate zones and an annual long-day (LD) plant with no cold requirement in arctic regions. In photoperiodic species, such as the short-day (SD) plant Pharbitis nil and the LD plant Silene armeria, flowering in unfavorable photoperiods can be caused by changing temperature, irradiance, or nutrition or by removing the roots. Similarly, in some late-flowering mutants of Arabidopsis, vernalization and an increase in the proportion of far-red light in the light source can substitute for one another in promoting the transition to flowering (Martinez-Zapater and Somerville, 1990; Bagnall, 1992). Clearly, there are alternate pathways to flowering in most, if

http://www.plantcell.org/content/plantcell/5/10/1147.full.pdf

Physiological Signals That Induce Flowering.

Extracellular invertase is the key enzyme of an apoplasmic phloem unloading pathway and catalyses the hydrolytic cleavage of the transport sugar sucrose released into the apoplast. This mechanism contributes to long-distance assimilate transport, provides the substrate to sustain heterotrophic growth and generates metabolic signals known to effect various processes of primary metabolism and defence responses. The essential function of extracellular invertase for supplying carbohydrates to sink organs was demonstrated by the finding that antisense repression of an anther-specific isoenzyme provides an efficient method for metabolic engineering of male sterility. The regulation of extracellular invertase by all classes of phytohormones indicates an essential link between the molecular mechanism of phytohormone action and primary metabolism. The up-regulation of extracellular invertase appears to be a common response to various biotic and abiotic stress-related stimuli such as pathogen infection and salt stress, in addition to specific stress-related reactions. Based on the observed co-ordinated regulation of source/sink relations and defence responses by sugars and stress-related stimuli, the identified activation of distinct subsets of MAP kinases provides a mechanism for signal integration and distribution within such complex networks. Sucrose derivatives not synthesized by higher plants, such as turanose, were shown to elicit responses distinctly different from metabolizable sugars and are rather perceived as stress-related stimuli.

Extracellular invertase: key metabolic enzyme and PR protein

Changes in lamina area, dimensions of epidermal and palisade cells, acid invertase activity and content of sucrose and hexose in the primary leaves of Phaseolus vulgaris L. were determined between emergence of the hypocotyl hook and the completion of leaf expansion. Growth in area and thickness of the primary leaf after emergence was attributable to the expansion of cells already present in the lamina at emergence. The major invertase in the expanding leaf was a readily soluble acid invertase; little insoluble invertase activity was detected. Soluble and insoluble fractions of leaf homogenates contained little neutral invertase activity. The specific activity of the soluble acid invertase increased rapidly during the early stages of leaf expansion, reaching a peak at the time of most rapid cell enlargement (5 d after emergence) and then declining as the leaf matured. Highly significant positive correlations were found between enzyme specific activity and the rates of cell and leaf enlargement. The early, rapid phase of lamina expansion was characterized by high concentrations of hexose sugar and low concentrations of sucrose. As the rates of leaf cell enlargement declined the concentration of hexose fell and that of sucrose increased. Between 5 d and 11 d after hypocotyl emergence, the hexose/sucrose ratio in the primary leaf decreased approximately 10-fold as the specific activity of acid invertase decreased. The results are discussed with reference to sources of carbon substrates for cell growth and to the sink/source transition during leaf development.

An Association Between Acid Invertase Activity and Cell Growth during Leaf Expansion in Phaseolus vulgaris L.

In the stem of Phaseolus vulgaris L. the specific activity of acid invertase was highest in the most rapidly elongating internode. Activity of the enzyme was very low in internodes which had completed their elongation, in young internodes before the onset of rapid elongation, and in the apical bud. From shortly after its emergence from the apical bud the elongation of internode 3 was attributable mainly to cell expansion. Total and specific activities of acid invertase in this internode rose to a maximum at the time of most rapid elongation and then declined. Transfer of plants to complete darkness, or treatment of plants with gibberellic acid (GA3), increased the rate of internode elongation and final internode length by stimulating cell expansion. Both treatments rapidly increased the total and specific activities of acid invertase in the responding internodes; peak activities of the enzyme occurred at the time of most rapid cell expansion. In light-grown plants, including those treated with GA3, rapid cell and internode elongation and high specific activities of acid invertase were associated with high concentrations of hexose sugar and low concentrations of sucrose. As cell growth rates and invertase activities declined, the concentration of hexose fell and that of sucrose rose. In plants transferred to darkness, stimulated cell elongation was accompanied by a rapid decrease in hexose concentration and the disappearance of sucrose, indicating rapid utilization of hexose. No sucrose was detected in the apical tissues of light-grown plants. The results are discussed in relation to the role of acid invertase in the provision of carbon substrates for cell growth.

Invertase Activity, Carbohydrate Metabolism and Cell Expansion in the Stem of Phaseolus vulgaris L.

During the development of roots, internodes and leaves, closely correlated changes occur in the rates of cell expansion, specific activities of acid invertase and concentrations of hexose sugars and sucrose. Rates of cell growth and acid invertase activities frequently exhibit closely coupled responses to environmental changes and to growth regulator treatments. The possibility is considered that, by controlling the availability of hexose substrates for cellular metabolism, acid invertase may regulate cell growth. Potential mechanisms regulating the in vivo activity of acid invertases are reviewed and attention is drawn to the need for more information on the sub-cellular localization of the enzyme.

Invertase activity in sinks undergoing cell expansion

The application of gibberellic acid (GA3,10 μM) as a root drench to 16-day-old plants of Phaseolus vulgaris L. cv. Masterpiece stimulated growth of the stem internodes and reduced root growth. GA3 treatment did not affect the export of 14C from a primary leaf to which [14C]-sucrose was applied, but greatly increased upward translocation to the elongation region of the stem at the expense of transport to the hypocotyl and root system. The observed changes in the patterns of growth and [14C]-labelled assimilate distribution were correlated with an increase in the specific activity of acid invertase in the elongating stem internodes and a decrease in invertase activity in the hypocotyl and root. Sucrose concentration in the elongating internodes fell substantially after treatment with GA3 while the concentration of hexose sugars increased. We suggest that by stimulating acid invertase synthesis in the elongating internodes, GA3 acts to establish a more favourable sucrose gradient between these sinks and source leaves. Under source-limiting conditions this, in turn, will lead to a reduced rate of assimilate translocation to competing sinks in the root system.

E. D. Arthur

Papers

An Association Between Acid Invertase Activity and Cell Growth during Leaf Expansion in Phaseolus vulgaris L.

Invertase Activity, Carbohydrate Metabolism and Cell Expansion in the Stem of Phaseolus vulgaris L.

Invertase activity in sinks undergoing cell expansion

Effects of gibberellic acid on patterns of carbohydrate distribution and acid invertase activity in Phaseolus vulgaris

Invertase and auxin-induced elongation in internodal segments of Phaseolus vulgaris