The primary products of photosynthesis is sugars. Sugars provide energy and structural material for defense responses in plants and may also act as a signal molecules interacting with the hormonal signaling network regulating the plant immune system. Some sugars act as a priming agents inducing plant resistance to pathogens (Morkunas and Ratajczak 2014). Elicitor-induced signal transduction pathways lead to (Garcia-Brugger et al., 2006):
- The reinforcement of cell walls
- The production of antimicrobial metabolites (phytoalexins), pathogenesis-related (PR) proteins and enzymes of oxidative stress protection
- Lignification
- The hypersensitive response (HR) a form of programmed cell death at the infection site.
Most of these reaction occur within few hours after infection. Carbohydrates satisfy the requirement for ATP, NADPH and metabolites. Soluble carbohydrate can control the expression of various metabolic and defense-related genes (Rolland et al., 2006). Reorganization of the cytoskeleton (Takemoto and Hardham 2004) require ATP which has been generated by respiration. Reactive oxygen species (ROS) generation by plasmalemma oxidase is driven by NADPH. Defense-related callose deposition consume large amounts of glucose units and is presumably one of the strongest sink reactions in plant cells (Essmann et al., 2008).
Plants are made up of sugar exporting (source i.e. photosynthetically active leaf) and sugar importing (sink) tissues and organs (roots, flowers, seeds etc.). Sugar signals are generated from different sources at different locations (Rolland et al., 2006). Solute movement towards the phloem occur through the symplasm via plasmodesmata by either volume flow of solution or solute diffusion in the absence of solvent movement. Alternatively intercellular transfer can proceed via apoplast by crossing the cell wall-membrane (Giaquinta 1983). Sugar efflux system can be hijacked by pathogens for access to nutrition from hosts (Chen 2014). In sink tissue sucrose can be imported into cells through plasmodesmata (symplastic transport) or the cell wall (apoplastic transport). In most plant the transported sugar is sucrose a nonreducing disaccharide in which glucose and fructose are linked (α1– β2). Depending on the physiological activities and biochemical need of the heterotrophic tissues, sucrose is channelled into various pathway in different subcellular compartments. It may enter glycolysis and the tricarboxylic acid cycle for the production of ATP and NADH (Sturm 1999). The carbon of disaccharide may be used for the biosynthesis of primary metabolites. Sucrose may convert into polymer such as starch, triacylglycerides or polypeptide for long term storage or into secondary compounds, enabling plants to cope with predators and pests (Sturm 1999).
Sugars act as nutrient and metabolite signaling molecule that activate hormone crosstalk transduction pathway resulting in modification of gene expression and proteomic patterns. Various metabolic reaction and regulation directly link soluble sugars (sucrose, glucose and fructose) with the production of ROS such as mitochondrial respiration and photosynthesis regulation (Couee et al., 2006). Genetic analysis reveal interactions between sugars and plant hormone signaling and a central role of hexokinase as a conserved glucose sensor. Diverse sugar signals activate multiple hexokinase-dependent and hexokinase-independent pathways and use different molecular mechanisms to control transcription, translation, protein stability and enzymatic activity (Rolland et al., 2006).
Utilization of sucrose as source of carbon and energy depends on its cleavage into hexoses. Invertase is a hydrolase cleaving sucrose into two monosaccharides (Sturm 1999). Role of invertase in the generation of hexoses may supply energy for defense reactions and act as signals inducing defense gene expression (Swarbrick et al., 2006). Invertase regulate sucrose:hexose ratio linked to sugar signaling (Bolouri – Moghaddam and Van den Ende 2012). The initial induction of an extracellular invertase by wounding or pathogen infection results in elevated sugar concentration which in turn is responsible for transcriptional repression of photosynthetic genes and for activation of defense-related genes (Ehness et al., 1997). It is speculated that glucose function as an extracellular indicator for pathogen infection.
Herbers et al. (1996a) proposed that sugar signaling for both activation of defense-related genes and repression of photosynthetic gene is associated with sensing mechanism located at the secretory membrane system, at endoplasmic reticulum or Golgi apparatus. Hexose sensing in the secretory pathway is essential for mediating the activation of defense-related genes (Herbers et al., 1996a). PR-protein PR-Q and PAR-1 were found to be inducible by glucose, fructose and sucrose in a SA-independent manner (Herbers et al., 1996b). Extracellular invertase is a cell wall bound enzyme and catalyses the irreversible cleavage of sucrose released into the apoplast via sucrose transporters (Roitsch et al., 2003). This mechanism generates metabolic signal known to effect various processes of primary metabolism and defense responses. Invertase activity can satisfy the increased demand for carbohydrate as an energy source for the tissue invaded by the pathogen. Furthermore, the increase in carbohydrates will generate a metabolic signal that induces the expression of defense-related genes and repression of photosynthesis in addition to signals derived from the pathogen (Roitsch et al., 2003). Herbers et al. (1996b) suggest different mechanisms for the induction of PR-protein genes and the repression of photosynthetic genes by soluble sugars. Hexose as well as sucrose are signal molecules in source-sink regulation (Roitsch 1999).
Above a certain level of glucose and fructose, PR-Q transcript is accumulated, indicating that a defined threshold level of hexose is required for defense gene expression (Herbers et al., 1996a). The disaccharide trehalose is an inducer of wheat defense and resistance against powdery mildew (Tayeh et al., 2014).
Oligogalacturonides (OGs) are oligomers of alpha-1,4-linked galacturonosyl residues released from plant cell walls on partial degradation of homogalacturonan (major component of pectin). OGs are able to elicit defense responses including accumulation of ROS and PR-related proteins protecting plants against pathogen infection (Ferrari et al., 2013). They may also be involved in activation of responses to mechanical wounding.
Plant innate immunity is a complex network including many signaling molecules and various cross-talks.
References:
Bolouri – Moghaddam, M. R. and Van den Ende 2012 Sugars and Plant Innate Immunity. J. Exp. Bot. 63(11): 3989 – 3998
doi.org/10.1093/jxb/ers129
Chen, L-Q. 2014 SWEET Transporters for Phloem Transport and Pathogen Nutrition. New Phytologist. 201: 1150- 1155
doi: 10.1111/nph.12445
Couee, I., Sulmon, C., Gouesbet, G. and Amrani, A. E. 2006 Involvement of Soluble Sugars in Reactive Oxygen Species Balance and Responses to Oxidative Stress in Plants. J. Exp. Bot. 57(3): 449 – 459
doi.org/10.1093/jxb/erj027
Ehness, R., Ecker, M., Godt, D. E. and Roitsch, T. 1997 Glucose and Stress Independently Regulate Source and Sink Metabolism and Defense Mechanisms via Signal Transduction Pathways Involving Protein Phosphorylation. The Plant Cell 9: 1825 – 1841
doi.org/10.1105/tpc.9.10.1825
Essmann, J., Schmitz-Thom, I., Schon, H., Sonnewald, S., Weis, E. and Scharte, J. 2008 RNA Interference-Mediated Repression of Cell Wall Invertase Impairs Defense in Source Leaves of Tobacco [OA]. Plant Physiol. 147: 1288 – 1299
doi/10.1104/pp.108.121418
Ferrari, S., Savatin, D. V., Sicilia, F., Gramegna, G., Cervone, F. and De Lorenzo, G. 2013 Oligogalacturonides: Plant Damage-Associated Molecular Patterns and Regulators of Growth and Development. Front. Plant Sci. 4: 49
doi: 10.3389/fpls.2013.00049
Garcia-Brugger, A., Lamotte, O., Vandelle, E., Bourque, S., Lecourieux, D., Poinssot, B., Wendehenne, D. and Pugin, A. 2006 Early Signaling Events Induced by Elicitors of Plant Diseases. MPMI 19(7): 711 – 724
doi: 10.1094/MPMI-19-0711
Giaquinta, R. T. 1983 Phloem Loading of Sucrose. Ann. Rev. Plant Physiol. 34: 347 – 387
doi.org/10.1146/annurev.pp.34.060183.002023
Herbers, K., Meuwly, P., Frommer, W. B., Metraux, J. P. and Sonnewald, U. 1996a Systemic Acquired Resistance Mediated by the Ectopic Expression of Invertase: Possible Hexose Sensing in the Secretory Pathway. Plant Cell 8(5): 793 – 803
doi: 10.1105/tpc.8.5.793
Herbers, K., Meuwhy, P., Metraux, J-P. and Sonnewald, U. 1996b Salicylic Acid-Independent Induction of Pathogenesis-Related Protein Transcripts by Sugars is Dependent on Leaf Developmental Stage. FEBS Lett. 397(2-3): 239 – 244
doi.org/10.1016/S0014-5793(96)01183-0
Morkunas, I. and Ratajczak, B. L. 2014 The Role of Sugar Signaling in Plant Defense Responses against Fungal Pathogens. Acta Physiol. Plant. 36(7): 1607 – 1619
doi.org/10.1007/s11738-014-1559-z
Roitsch, T., Balibrea, M. E., Hofmann, M., Proels, R. and Sinha, A. K. 2003 Extracellular Invertase: Key Metabolic Enzyme and PR Protein. J. Exp. Bot. 54(382): 513 – 524
doi.org/10.1093/jxb/erg050
Roitsch, T. 1999 Source-Sink Regulation by Sugar and Stress. Curr. Opin. Plant Biol. 2(3): 198 – 206
doi: 10.1016/S1369-5266(99)80036-3
Rolland, F., Baena-Gonzalez, E. and Sheen, J. 2006 Sugar Sensing and Signaling in Plants: Conserved and Novel Mechanisms. Annu. Rev. Plant Biol. 57: 675 – 709
doi.org/10.1146/annurev.arplant.57.032905.105441
Smeekens, S. and Hellmann, H. A. 2014 Sugar Sensing and Signaling in Plants. Front Plant Sci. 5: 113
doi: 10.3389/fpls.2014.00113
Sturm, A. 1999 Invertases Primary Structures, Functions and Roles in Plant Development and Sucrose Partitioning. Plant Physiol. 121: 1 – 7
doi.org/10.1104/pp.121.1.1
Swarbrick, P. J., Schulze-Lefert, P. and Scholes, J. D. 2006 Metabolic Consequences of Susceptibility and Resistance (Race-Specific and Broad-Spectrum) in Barley Leaves Challenged with Powdery Mildew. Plant cell Environ. 29: 1061 – 1076
doi: 10.1111/j.1365-3040.2005.01472.x
Takemoto, D. and Hardham, A. R. 2004 The Cytoskeleton as a Regulator and Target of Biotic Interactions in Plants. Plant Physiol. 136(4): 3864 – 3876
doi/10.1104/pp.104.052159
Tayeh, C., Randoux, B., Vincent, D., Bourdon, N. and Reignault, P. 2014 Exogenous Trehalose Induces Defense in Wheat Before and During a Biotic Stress Caused by Powdery Mildew. APS Publ. 104(3): 293 – 305
doi.org/10.1094/PHYTO-07-13-0191-R
BIOLOGICAL PROCESSES- A NATURE'S GIFT 