Exploration of Sweet Immunity to Enhance Abiotic Stress Tolerance in Plants: Lessons from CAM

  • Nathalie Ceusters
  • Wim Van den Ende
  • Johan CeustersEmail author
Part of the Progress in Botany book series (BOTANY, volume 78)


The concept of ‘sweet immunity’ or ‘sugar-enhanced defence’ is based on the accumulating evidence that sweet, endogenous saccharides might act as signalling molecules that are activated by exposure to stress and hence initiate signal amplification and lead to more rapid and robust activation of defence, immunity and stress tolerance. Sugars such as glucose, fructose and sucrose have acquired important regulatory functions in evolution and are becoming more and more recognized as signalling molecules in plants controlling gene expression related to plant metabolism, stress resistance and development. This offers opportunities for ‘sweet priming’, defined as a physiological process that prepares plants for a faster and/or stronger defence response to future stress conditions, but does not impose the costs associated with full implementation of an induced defence response. Future possibilities to substitute toxic agrochemicals with biodegradable sugar-(like) compounds in agricultural and horticultural practice requires a thorough understanding of how sugars can play a crucial role in perceiving, anticipating and counteracting abiotic stresses. In this review, the physiological responses of crassulacean acid metabolism (CAM) plants to different conditions of abiotic stress will be discussed with particular attention to sucrose dynamics. CAM plants are ideally suited to different abiotic stress conditions and carbohydrate cycling and availability are of paramount importance for plant growth, photosynthesis and homeostasis. By evaluating the plethora of effects sugars can exert on plant metabolism, growth and development the possibilities for sugars as potential priming agents to enhance abiotic stress tolerance will be explored.


Abiotic Stress Soluble Sugar Circadian Clock Crassulacean Acid Metabolism Crassulacean Acid Metabolism Plant 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Ana Sofia Duque, André Martinho de Almeida, Anabela Bernardes da Silva, Jorge Marques da Silva, Ana Paula Farinha, Dulce Santos, Pedro Fevereiro and Susana de Sousa Araújo (2013) Abiotic stress responses in plants: unraveling the complexity of genes and networks to survive. In: Vahdati K (ed) Abiotic stress - plant responses and applications in agriculture. InTech, Rijeka, Croatia. doi:10.5772/52779Google Scholar
  2. Antony E, Borland AM (2009) The role and regulation of sugar transporters in plants with crassulacean acid metabolism. Prog Bot 70:127–143CrossRefGoogle Scholar
  3. Asada K (1999) The water cycle in chloroplasts: scavenging of active oxygen and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639PubMedCrossRefGoogle Scholar
  4. Behzadipour M, Ratajczak R, Faist K, Pawlitschek P, Tremolieres A, Kluge M (1998) Phenotypic adaptation of tonoplast fluidity to growth temperature in the CAM plant Kalanchoe daigremontiana Ham. et Per. is accompanied by changes in the membrane phospholipid and protein composition. J Membr Biol 166:61–70PubMedCrossRefGoogle Scholar
  5. Birch ANE, Roberson WM, Geoghegan IE, MC-Gavin WJ, Alpheyt JW, Porter EA (1993) DMDP – a plant-derived sugar analogue with systemic activity against plant parasitic nematodes. Nematologica 39:521–535Google Scholar
  6. Bolouri-Moghaddam MR, Van den Ende W (2012) Sugars and plant innate immunity. J Exp Bot 63:3989–3998PubMedCrossRefGoogle Scholar
  7. Bolouri-Moghaddam MR, Van den Ende W (2013a) Sweet immunity in the plant circadian regulatory network. J Exp Bot 64:1439–1449PubMedCrossRefGoogle Scholar
  8. Bolouri-Moghaddam MR, Van den Ende W (2013b) Sugars, the clock and transition to flowering. Frontier Plant Sci 4, 4Google Scholar
  9. Bolouri-Moghaddam MR, Le Roy K, Xiang L, Rolland F, Van den Ende W (2010) Sugar signaling and antioxidant network connections in plant cells. FEBS J 277:2022–2037PubMedCrossRefGoogle Scholar
  10. Borland AM (1996) A model for the portioning of photosynthetically fixed carbon during the C3-CAM transition in Sedum telephium. New Phytol 134:433–444CrossRefGoogle Scholar
  11. Borland AM, Griffiths H, Broadmeadow MSJ, Fordham MC, Maxwell C (1993) Short-term changes in carbon-isotope discrimination in the C3/CAM intermediate Clusia minor L. growing in Trinidad. Oecologia 95:444–453CrossRefGoogle Scholar
  12. Borland AM, Hartwell J, Jenkins GI, Wilkins MB, Nimmo HG (1999) Metabolite control overrides circadian regulation of phosphoenolpyruvate carboxylase kinase and CO2 fixation in crassulacean acid metabolism. Plant Physiol 121:889–896PubMedPubMedCentralCrossRefGoogle Scholar
  13. Borland AM, Zambrano VAB, Ceusters J, Shorrock K (2011) The photosynthetic plasticity of crassulacean acid metabolism: an evolutionary innovation for sustainable productivity in a changing world. New Phytol 191:619–633PubMedCrossRefGoogle Scholar
  14. Boxall SF, Foster JM, Bohnert HJ, Cushman JC, Nimmo HG, Hartwell J (2005) Conservation and divergence of circadian clock operation in a stress-inducible crassulacean acid metabolism species reveals clock compensation against stress. Plant Physiol 137:969–982PubMedPubMedCentralCrossRefGoogle Scholar
  15. Brandon PC (1967) Temperature features of enzymes affecting crassulacean acid metabolism. Plant Physiol 42:977–984PubMedPubMedCentralCrossRefGoogle Scholar
  16. Broetto F, Lüttge U, Ratajczak R (2002) Influence of light intensity and salt-treatment on mode of photosynthesis and enzymes of the antioxidative response system of Mesembryanthemum crystallinum L. Funct Plant Biol 29:13–23CrossRefGoogle Scholar
  17. Brulfert J, Guerrier D, Queiroz O (1973) Photoperiodism and enzyme activity: balance between inhibition and induction of the crassulacean acid metabolism. Plant Physiol 51:220–222PubMedPubMedCentralCrossRefGoogle Scholar
  18. Brulfert J, Kluge M, Güclü S, Queiroz O (1988) Interaction of photoperiod and drought as CAM inducing factors in Kalanchoë blossfeldiana Poelln., Cv Tom Thumb. J Plant Physiol 133:222–227CrossRefGoogle Scholar
  19. Brutus A, Sicilia F, Macone A, Cervone F, De Lorenzo G (2010) A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. Proc Natl Acad Sci U S A 107:9452–9457PubMedPubMedCentralCrossRefGoogle Scholar
  20. Buchanan-Bollig IC, Kluge M, Müller D (1984) Kinetic changes with temperature of phosphoenolpyruvate carboxylase from a CAM plant. Plant Cell Environ 7:63–70CrossRefGoogle Scholar
  21. Castillo FJ (1996) Antioxidative protection in the inducible CAM plant Sedum album L. following the imposition of severe water stress and recovery. Oecologia 107:469–477CrossRefGoogle Scholar
  22. Ceusters J, Borland AM, Londers E, Verdoodt V, Godts C, De Proft M (2008) Diel shifts in carboxylation pathway and metabolite dynamics in the CAM bromeliad Aechmea ‘Maya’ in response to elevated CO2. Ann Bot 3:389–397CrossRefGoogle Scholar
  23. Ceusters J, Borland AM, De Proft MP (2009a) Drought adaptation in plants with crassulacean acid metabolism involves the flexible use of different storage carbohydrate pools. Plant Signal Behav 4:212–214PubMedPubMedCentralCrossRefGoogle Scholar
  24. Ceusters J, Borland AM, Londers E, Verdoodt V, Godts C, De Proft MP (2009b) Differential usage of storage carbohydrates in the CAM bromeliad Aechmea ‘Maya’ during acclimation to drought and recovery from dehydration. Physiol Plant 135:174–184PubMedCrossRefGoogle Scholar
  25. Ceusters J, Borland AM, Ceusters N, Verdoodt V, Godts C, De Proft P (2010) Seasonal influences on carbohydrate metabolism in the CAM bromeliad Aechmea ‘Maya’: consequences for carbohydrate partitioning and growth. Ann Bot 105:301–309PubMedCrossRefGoogle Scholar
  26. Ceusters J, Borland AM, Godts C, Londers E, Croonenborghs S, Van Goethem D, De Proft MP (2011) Crassulacean acid metabolism under severe light limitation: a matter of plasticity in the shadows? J Exp Bot 62:283–291PubMedCrossRefGoogle Scholar
  27. Ceusters J, Borland AM, Taybi T, Frans M, Godts C, De Proft MP (2014) Light quality modulates metabolic synchronization over the diel phases of crassulacean acid metabolism. J Exp Bot 65:3705–3714PubMedPubMedCentralCrossRefGoogle Scholar
  28. Chen WS, Liu HY, Liu ZH, Yang L, Chen WH (1994) Gibberellin and temperature influence carbohydrate content and flowering in Phalaenopsis. Physiol Plant 90:391–395CrossRefGoogle Scholar
  29. Chen WH, Tseng YC, Liu YC, Chuo CM, Chen PT, Tseng KM, Yeh YC, Ger MJ, Wang HL (2008) Cool-night temperature induces spike emergence and affects photosynthetic efficiency and metabolizable carbohydrate and organic acid pools in Phalaenopsis aphrodite. Plant Cell Rep 27:1667–1675PubMedCrossRefGoogle Scholar
  30. Chiou TJ, Bush DR (1998) Sucrose is a signal molecule in assimilate partitioning. Proc Natl Acad Sci U S A 95:4784–4788PubMedPubMedCentralCrossRefGoogle Scholar
  31. Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–814PubMedCrossRefGoogle Scholar
  32. Ciereszko I, Johansson H, Kleczkowski LA (2004) Interactive effects of phosphate deficiency, sucrose and light/dark conditions on gene expression of UDP-glucose pyrophosphorylase in Arabidopsis. J Plant Physiol 162:343–353CrossRefGoogle Scholar
  33. Clarkson DT, Carvajal M, Henzler T, Waterhouse RN, Smyth AJ, Cooke DT, Steudle E (2000) Root hydraulic conductance: diurnal aquaporin expression and the effects of nutrient stress. J Exp Bot 51:61–70PubMedCrossRefGoogle Scholar
  34. Conrath U (2011) Molecular aspects of defence priming. Trends Plant Sci 16:524–531PubMedCrossRefGoogle Scholar
  35. Couée I, Sulmon C, Gouesbet G, El Amrani A (2006) Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. J Exp Bot 57:449–459PubMedCrossRefGoogle Scholar
  36. Croonenborghs S, Ceusters J, Londers E, De Proft MP (2009) Effects of elevated CO2 on growth and morphological characteristics of ornamental bromeliads. Sci Hortic 121:192–198CrossRefGoogle Scholar
  37. Cushman JC (2001) Crassulacean acid metabolism. A plastic photosynthetic adaptation to arid environments. Plant Physiol 127:1439–1448PubMedPubMedCentralCrossRefGoogle Scholar
  38. Cushman JC, Borland AM (2002) Induction of crassulacean acid metabolism by water limitation. Plant Cell Environ 25:295–310PubMedCrossRefGoogle Scholar
  39. De Bruyne L, Hofte M, De Vleesschauwer D (2014) Connecting growth and defense: the emerging roles of brassinosteroids and gibberellins in plant innate immunity. Mol Plant 7:943–959PubMedCrossRefGoogle Scholar
  40. Debnath M, Pandey M, Bisen PS (2011) An OMICS approach to understand the plant abiotic stress. OMICS 15:739–762PubMedCrossRefGoogle Scholar
  41. Demel RE, Dorrepaal E, Ebskamp MJM, Smeekens S, de Kruijff B (1998) Fructans interact strongly with model membranes. Biochim Biophys Acta 1375:36–42PubMedCrossRefGoogle Scholar
  42. Dicke M, van Loon JJA (2014) Chemical ecology of phytohormones: how plants integrate responses to complex and dynamic environments. J Chem Ecol 40:653–656PubMedCrossRefGoogle Scholar
  43. Dodd AN, Borland AM, Haslam RP, Griffiths H, Maxwell K (2002) Crassulacean acid metabolism: plastic fantastic. J Exp Bot 53:569–580PubMedCrossRefGoogle Scholar
  44. Eveland AL, Jackson DP (2011) Sugars, signalling and plant development. J Exp Bot 63:3367–3377PubMedCrossRefGoogle Scholar
  45. Farrar J, Pollock C, Gallagher J (2000) Sucrose and the integration of metabolism in vascular plants. Plant Sci 154:1–11PubMedCrossRefGoogle Scholar
  46. Fernandez O, Béthencourt L, Quero A, Sangwan RS, Clément C (2010) Trehalose and plant stress responses: friend or foe? Trends Plant Sci 15:409–417PubMedCrossRefGoogle Scholar
  47. Ferrari S, Savatin DV, Sicilia F, Gramegna G, Cervone F, De Lorenzo G (2013) Oligogalacturonides: plant damage-associated molecular patterns and regulators of growth and development. Front Plant Sci 4:49PubMedPubMedCentralCrossRefGoogle Scholar
  48. Finkelstein RR, Gibson SI (2001) ABA and sugar interactions regulating development: cross-talk or voices in a crowd? Curr Opin Plant Biol 5:26–32CrossRefGoogle Scholar
  49. Frank JH (2005) Phytotelmata. Encyclopedia of Entomology [Internet]. Springer Science + Business Media; 1718–20. Available from:
  50. Friemert V, Kluge M, Smith JAC (1986) Net CO2 output by CAM plants in the light: the roe of leaf conductance. Physiol Plant 68:353–358CrossRefGoogle Scholar
  51. Friemert V, Heininger D, Kluge M, Ziegler H (1988) Temperature effects on malic-acid efflux from the vacuoles and on the carboxylation pathways in crassulacean acid metabolism plants. Planta 174:453–461PubMedCrossRefGoogle Scholar
  52. Gao J, Sun L, Yang X, Liu JX (2013a) Transcriptomic analysis of cadmium stress response in the heavy metal hyperaccumulator Sedum alfredii Hance. PLoS One 8, e64643. doi: 10.1371/journal.pone.0064643 PubMedPubMedCentralCrossRefGoogle Scholar
  53. Gao J, Wang N, Xu S-S, Li Y, Wang Y, Wang G-X (2013b) Exogenous application of trehalose induced H2O2 production and stomatal closure in Vicia faba. Biol Plant 57:380–384CrossRefGoogle Scholar
  54. Geigenberger P, Geiger M, Stitt M (1998) High-temperature perturbation of starch synthesis is attributable to inhibition of ADP-glucose pyrophosphorylase by decreased levels of glycerate-3-phosphate in growing potato tubers. Plant Physiol 117:1307–1316PubMedPubMedCentralCrossRefGoogle Scholar
  55. Gibson SI (2004) Sugar and phytohormone response pathways: navigating a signaling network. J Exp Bot 55:253–264PubMedCrossRefGoogle Scholar
  56. Giron D, Frago E, Glevarec G, Pieterse CMJ, Dicke M (2013) Cytokinins as key regulators in plant-microbe-insect interactions: connecting plant growth and defence. Funct Ecol 27:S599–S609CrossRefGoogle Scholar
  57. Guo WJ, Lee N (2006) Effect of leaf and plant age, and day/night temperature on net CO2 uptake in Phalaenopsis amabilis var. formosa. J Am Soc Hortic Sci 131(3):320–326Google Scholar
  58. Gupta AK, Kaur N (2005) Sugar signaling and gene expression in relation to carbohydrate metabolism under abiotic stresses in plants. J Biosci 30:761–776PubMedCrossRefGoogle Scholar
  59. Haydon MJ, Bell LJ, Webb AAR (2011) Interactions between plant circadian clocks and solute transport. J Exp Bot 62:2333–2348PubMedCrossRefGoogle Scholar
  60. Herbers K, Meuwly P, Frommer W, Métraux JP, Sonnewald U (1996a) Systemic acquired resistance mediated by the ectopic expression of invertase: possible hexose sensing in the secretory pathway. Plant Cell 8:793–803PubMedPubMedCentralCrossRefGoogle Scholar
  61. Herbers K, Meuwly P, Métraux JP, Sonnewald U (1996b) Salicyclic acid independent induction of pathogenesis-related protein transcripts by sugars is dependent on leaf developmental stage. FEBS Lett 397:239–244PubMedCrossRefGoogle Scholar
  62. Holmstrom KO, Mantyla E, Welin B, Mandal A, Palva ET, Tunnela OE, Londesborough J (1996) Drought tolerance in tobacco. Nature 379:683–684CrossRefGoogle Scholar
  63. Horacio P, Martinez-Noel G (2013) Sucrose signalling in plants: a world yet to be explored. Plant Signal Behav 8, e23316CrossRefGoogle Scholar
  64. Islam E, Khan MT, Irem S (2015) Biochemical mechanisms of signalling: perspectives in plants under arsenic stress. Ecotoxicol Environ Saf 114:126–133PubMedCrossRefGoogle Scholar
  65. Jaleel CA, Manivannan P, Lakshmanan GMA, Gomathinayagam M, Panneerselvam R (2008) Alterations in morphological parameters and photosynthetic pigment responses in Catharanthus roseus under soil water deficits. Colloids Surf B Biointerfaces 62:298–303CrossRefGoogle Scholar
  66. Jaleel CA, Manivannan P, Wahid A, Farooq M, Somasundaram R, Panneerselvam R (2009) Drought stress in plants: a review on morphological characteristics and pigments composition. Int J Agric Biol 11:100–105Google Scholar
  67. Jang JC, León P, Zhou L, Sheen J (1997) Hexokinase as a sugar sensor in higher plants. Plant Cell 9:5–19PubMedPubMedCentralCrossRefGoogle Scholar
  68. Johnson R, Ryan CA (1990) Wound-inducible potato inhibitor II genes: enhancement of expression by sucrose. Plant Mol Biol 14:527–536PubMedCrossRefGoogle Scholar
  69. Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329PubMedCrossRefGoogle Scholar
  70. Kano A, Hosotani K, Gomi K et al (2011) d-Psicose induces upregulation of defence-related genes and resistance in rice against bacterial blight. J Plant Physiol 168:1852–1857PubMedCrossRefGoogle Scholar
  71. Kholodova V, Volkov K, Abdeyeva A, Kuznetsov V (2011) Water status in Mesembryanthemum crystallinum under heavy metal stress. Environ Exp Bot 71:382–389Google Scholar
  72. Kliemchen A, Schomburg M, Galla HJ, Lüttge U, Kluge M (1993) Phenotypic changes in the fluidity of the tonoplast membrane of crassulacean acid metabolism plants in response to temperature and salinity stress. Planta 189:403–409PubMedCrossRefGoogle Scholar
  73. Kluge M, Ting IP (1978) Crassulacean acid metabolism. Analysis of an ecological adaptation. Springer, BerlinCrossRefGoogle Scholar
  74. Knaupp M, Mishra K, Nedbal L, Heyer AG (2011) Evidence for a role of raffinose in stabilizing photosystem II during freeze-thaw cycles. Planta 234:477–486PubMedCrossRefGoogle Scholar
  75. Koch KE (1996) Carbohydrate-modulated gene expression in plants. Annu Rev Plant Physiol Plant Mol Biol 47:509–540PubMedCrossRefGoogle Scholar
  76. Koch K (2004) Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr Opin Plant Biol 7:235–246PubMedCrossRefGoogle Scholar
  77. Kunz S, Gardeström P, Pesquet E, Kleczkowski LA (2015) Hexokinase 1 is required for glucose-induced repression of bZIP63, At5g22920, and BT2 in Arabidopsis. Front Plant Sci 6:525PubMedPubMedCentralCrossRefGoogle Scholar
  78. Lastdrager J, Hanson J, Smeekens S (2014) Sugar signals and the control of plant growth and development. J Exp Bot 65:799–807PubMedCrossRefGoogle Scholar
  79. León P, Sheen J (2003) Sugar and hormone connections. Trends Plant Sci 8:110–116PubMedCrossRefGoogle Scholar
  80. Lu C, Qiu N, Lu Q, Wang B, Kuang T (2003) PS II photochemistry, thermal energy dissipation, and the xanthophyll cycle in Kalanchoë daigremontiana exposed to a combination of water stress and high light. Physiol Plant 118:173–182CrossRefGoogle Scholar
  81. Lunn JE, Delorge I, Figueroa CM, Van Dijck P, Stitt M (2014) Trehalose metabolism in plants. Plant J 79:544–567PubMedCrossRefGoogle Scholar
  82. Lüttge U (2000) The tonoplast functioning as the master switch for circadian regulation of crassulacean acid metabolism. Planta 211:761–769PubMedCrossRefGoogle Scholar
  83. Lüttge U (2002) CO2-concentrating: consequences in crassulacean acid metabolism. J Exp Bot 53:2131–2142PubMedCrossRefGoogle Scholar
  84. Lüttge U (2004) Ecophysiology of crassulacean acid metabolism (CAM). Ann Bot 93:629–652PubMedPubMedCentralCrossRefGoogle Scholar
  85. Lüttge U (2006) Photosynthetic flexibility and ecological plasticity: questions and lessons from Clusia, the only CAM tree, in the neotropics. New Phytol 171:7–25PubMedCrossRefGoogle Scholar
  86. Lüttge U (2010) Photorespiration in Phase III of crassulacean acid metabolism: evolutionary and ecophysiological implications. Progr Bot 72:371–384CrossRefGoogle Scholar
  87. Martínez-Noël GMA, Tognetti JA, Salerno GL, Wiemken A, Pontis HG (2009) Protein phosphatase activity and sucrose-mediated induction of fructan synthesis in wheat. Planta 230:1071–1079PubMedCrossRefGoogle Scholar
  88. Matros A, Peshev D, Peukert M, Mock HP, Van den Ende W (2015) Sugars as hydroxyl radical scavengers: proof-of-concept by studying the fate of sucralose in Arabidopsis. Plant J 82:822–839PubMedCrossRefGoogle Scholar
  89. Miszalski Z, Slesak I, Niewiadomska E, Baczek R, Lüttge U, Ratajezak R (1998) Subcellular localization and stress responses of superoxide dismutase isoforms from leaves in the C3-CAM intermediate halophyte Mesembryanthemum crystallinum L. Plant Cell Environ 21:169–179CrossRefGoogle Scholar
  90. Moller IM (2001) Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu Rev Plant Physiol Plant Mol Biol 52:561–591PubMedCrossRefGoogle Scholar
  91. Moore BD, Sheen J (1999) Plant sugar sensing and signaling – a complex reality. Trends Plant Sci 4:250PubMedCrossRefGoogle Scholar
  92. Moore B, Zhou L, Rolland F, Hall Q, Cheng WH, Liu YX, Hwang I, Jones T, Sheen J (2003) Roles of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. Science 300:332–336PubMedCrossRefGoogle Scholar
  93. Moreira Lobo AK, de Oliveira M, Lima Neto MC, Caruso Machado E, Vasconcelos Ribeiro R, Gomes Silveira JA (2015) Exogenous sucrose supply changes sugar metabolism and reduces photosynthesis of sugarcane through the down-regulation of Rubisco abundance and activity. J Plant Physiol 179:113–121CrossRefGoogle Scholar
  94. Moya JL, Ros R, Picazo I (1993) Influence of cadmium and nickel on growth, net photosynthesis and carbohydrate distribution in rice plants. Photosynth Res 36:75–80PubMedCrossRefGoogle Scholar
  95. Nägele T, Weckwerth W (2014) Mathematical modeling reveals that metabolic feedback regulation of SnRK1 and hexokinase is sufficient to control sugar homeostasis from energy depletion to full recovery. Front Plant Sci 5:365PubMedPubMedCentralCrossRefGoogle Scholar
  96. Nie G, Hendrix DL, Webber AN, Kimball BA, Long SP (1995) Increased accumulation of carbohydrates and decreased photo- synthetic gene transcript levels in wheat grown at an elevated CO, concentration in the field. Plant Physiol 108:975–983PubMedPubMedCentralCrossRefGoogle Scholar
  97. Nobel PS (1983) Nutrient levels in Cacti – relation to nocturnal acid accumulation and growth. Am J Bot 70:1244–1253CrossRefGoogle Scholar
  98. Nobel PS, Berry WL (1985) Element responses of agaves. Am J Bot 72:686–694CrossRefGoogle Scholar
  99. Nobel PS, Lüttge U, Heuer S, Ball E (1984) Influence of applied NaCl on crassulacean acid metabolism and ionic levels in a cactus, Cereus validus. Plant Physiol 75:799–803PubMedPubMedCentralCrossRefGoogle Scholar
  100. Ordoñez-Salanueva CA, Seal CE, Pritchard HW, Orozco-Segovia A, Canales-Martinez M, Flores-Ortiz CM (2015) Cardinal temperatures and thermal time in Polaskia Backeb (Cactaceae) species: effect of projected soil temperature increase and nurse interaction on germination timing. J Arid Environ 115:73–80CrossRefGoogle Scholar
  101. Osakabe K, Osakabe Y (2012) Plant light stress. In: Encyclopaedia of life sciences. Wiley, Chichester. doi: 10.1002/9780470015902.a0001319.pub2
  102. Osmond CB (1981) Crassulacean acid metabolism: a curiosity in context. Ann Rev Plant Physiol 29:379–414CrossRefGoogle Scholar
  103. Paparella S, Araújo SS, Rossi G, Wijayasinghe M, Carbonera D, Balestrazzi A (2015) Seed priming: state of the arte and new perspectives. Plant Cell Rep 34:1281–1293PubMedCrossRefGoogle Scholar
  104. Pego JV, Kortstee AJ, Huijser C, Smeekens S (2000) Photosynthesis, sugars and the regulation of gene expression. J Exp Bot 51:407–416PubMedCrossRefGoogle Scholar
  105. Peshev D, Vergauwen R, Moglia A, Hideg E, Van den Ende W (2013) Towards understanding vacuolar antioxidant mechanisms: a role for fructans? J Exp Bot 64:1025–1038PubMedPubMedCentralCrossRefGoogle Scholar
  106. Peukert M, Thiel J, Peshev D, Weschke W, Van den Ende W, Mock HP, Matros A (2014) Spatio-temporal dynamics of fructan metabolism in developing barley grains. Plant Cell 26:3728–3744PubMedPubMedCentralCrossRefGoogle Scholar
  107. Pieterse CMJ, Leon-Reyes A, Van der Ent S, Van Wees SCM (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5:308–316PubMedCrossRefGoogle Scholar
  108. Pourtau N, Jennings R, Pelzer E, Pallas J, Wingler A (2006) Effect of sugar-induced senescence on gene expression and implications for the regulation of senescence in Arabidopsis. Planta 224:556–568PubMedCrossRefGoogle Scholar
  109. Quirino BF, Noh YS, Himelblau E, Amasino RM (2000) Molecular aspects of leaf senescence. Trends Plant Sci 5:278–282PubMedCrossRefGoogle Scholar
  110. Ramon M, Rolland F, Sheen J (2008) Sugar sensing and signaling. Arabidopsis Book 6:e0117. doi: 10.1199/tab.0117
  111. Rolland F, Moore B, Sheen J (2002) Sugar sensing and signaling in plants. Plant Cell 14:S185–S205Google Scholar
  112. Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57:675–709Google Scholar
  113. Rosa M, Prado C, Podazza G, Interdonato R, González JA, Hilal M, Prado FE (2009) Soluble sugars – metabolism, sensing and abiotic stress. Plant Signal Behav 4(5):388–393. doi: 10.4161/psb.4.5.8294 PubMedPubMedCentralCrossRefGoogle Scholar
  114. Ruan YL (2014) Sucrose metabolism: gateway to diverse carbon use and sugar signaling. Annu Rev Plant Biol 65:33–67PubMedCrossRefGoogle Scholar
  115. Sairam RK, Tyagi A (2004) Physiology and molecular biology of salinity stress tolerance in plants. Curr Sci 86:407–421Google Scholar
  116. Sairanen I, Novák O, Pencík A, Ikeda Y, Jones B, Sandberg G, Ljung K (2012) Soluble carbohydrates regulate auxin biosynthesis via PIF proteins in Arabidopsis. Plant Cell 24:4907–4916PubMedPubMedCentralCrossRefGoogle Scholar
  117. Sheen J (1994) Feedback control of gene expression. Photosynth Res 39:427–438PubMedCrossRefGoogle Scholar
  118. Sheen J (2014) Master regulators in plant glucose signaling networks. J Plant Biol 57:67–79PubMedPubMedCentralCrossRefGoogle Scholar
  119. Smeekens S, Ma J, Hanson J, Rolland F (2010) Sugar signals and molecular networks controlling plant growth. Curr Opin Plant Biol 13:274–279PubMedCrossRefGoogle Scholar
  120. Smirnoff N (1993) The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol 125:27–58CrossRefGoogle Scholar
  121. Spalding MH, Stumpf DK, Ku MSB, Burris RH, Edwards GE (1979) Crassulacean acid metabolism and diurnal variations of internal CO2 and O2-concentrations in Sedum praealtum DC. Funct Plant Biol 6:557–567Google Scholar
  122. Tarkowski ŁP, Van den Ende W (2015) Cold tolerance triggered by soluble sugars: a multifaceted countermeasure. Front Plant Sci 6:203PubMedPubMedCentralCrossRefGoogle Scholar
  123. Tayeh C, Randoux B, Dorothee V et al (2014) Exogenous trehalose induces defenses in wheat before and during a biotic stress caused by powdery mildew. Phytopathology 104:293–305PubMedCrossRefGoogle Scholar
  124. Tian S, Lu L, Labavitch J, Yang X, He Z, Hu H, Sarangi R, Newvill M, Commisso J, Brown P (2011) Cellular sequestration of cadmium in the hyperaccumulator plant species Sedum alfredii. Plant Physiol 157:1914–1925PubMedPubMedCentralCrossRefGoogle Scholar
  125. Ting IP (1985) Crassulacean acid metabolism. Ann Rev Plant Physiol 36:595–622CrossRefGoogle Scholar
  126. Tognetti JA, Pontis HG, Martínez-Noël GM (2013) Sucrose signaling in plants: a world yet to be explored. Plant Signal Behav 8(3):e23316Google Scholar
  127. Trouvelot S, Héloir MC, Poinssot B, Gauthier A, Paris F, Guillier C, Combier M, Trdá L, Daire X, Adrian M (2014) Carbohydrates in plant immunity and plant protection: roles and potential application as foliar sprays. Front Plant Sci 5:592PubMedPubMedCentralCrossRefGoogle Scholar
  128. Tsai AY-L, Gazzarrini S (2014) Trehalose-6-phosphate and SnRK1 kinases in plant development and signaling: the emerging picture. Front Plant Sci 5:119PubMedPubMedCentralCrossRefGoogle Scholar
  129. Van den Ende W (2013) Multifunctional fructans and raffinose family oligosaccharides. Front Plant Sci 4:247PubMedCrossRefGoogle Scholar
  130. Van den Ende W, El-Esawe SK (2014) Sugar signaling pathways leading to fructan and anthocyanin accumulation: a dual function in abiotic and biotic stress responses? Environ Exp Bot 108:4–13CrossRefGoogle Scholar
  131. Van den Ende W, Valluru R (2009) Sucrose, sucrosyl oligosaccharides, and oxidative stress: scavenging and salvaging? J Exp Bot 60:9–18PubMedCrossRefGoogle Scholar
  132. Wang L, Ruan Y-L (2013) Regulation of cell division and expansion by sugar and auxin signaling. Front Plant Sci 4:163PubMedPubMedCentralGoogle Scholar
  133. Willemoës JG, Beltrano J, Montaldi ER (1988) Diagravitropic growth promoted by high sucrose contents in Paspalum vaginatum, and its reversion by gibberellic acid. Can J Botany 66:2035–2037Google Scholar
  134. Winter K, Smith JAC (1996) Crassulacean acid metabolism: current status and perspectives. In: Winter K, Smith JAC (eds) Crassulacean acid metabolism: biochemistry. Ecophysiology and evolution. Springer, Berlin, pp 230–246CrossRefGoogle Scholar
  135. Winter K, Aranda J, Holtum JAM (2005) Carbon isotope composition and water-use efficiency in plants with crassulacean acid metabolism. Funct Plant Biol 32:381–388CrossRefGoogle Scholar
  136. Wolf S, Marani A, Rudich J (1991) Effect of temperature on carbohydrate-metabolism in potato plants. J Exp Bot 42:619–625CrossRefGoogle Scholar
  137. Yadav S, Irfan M, Ahmad A, Hayat S (2011) Causes of salinity and plant manifestations to salt stress: a review. J Environ Biol 32:667–685PubMedGoogle Scholar
  138. Yadav UP, Ivakov A, Feil R, Duan GY, Walther D, Giavalisco P, Piques M, Carillo P, Hubberten HM, Stitt M, Lunn EJ (2014) The sucrose-trehalose 6-phosphate (Tre6P) nexus: specificity and mechanisms of sucrose signaling by Tre6P. J Exp Bot 65:1051–1068PubMedPubMedCentralCrossRefGoogle Scholar
  139. Yang X, Li T, Yang J, He Z, Lu L, Meng F (2006) Zinc compartmentation in root, transport into xylem, and absorption into leaf cells in the hyperaccumulating species of Sedum alfredii Hance. Planta 224:185–195PubMedCrossRefGoogle Scholar
  140. Yang X, Cushman J, Borland A, Edwards E, Wullschleger S, Tuskan G, Owen N, Griffiths H, Smith J, De Paoli H, Weston D, Cottingham R, Hartwell J, Davis S, Silveria K, Ming R, Schlaugh K, Abraham P, Stewart R, Guo H, Albion R, Ha J, Lim S, Wone B, Yim W, Garcia T, Mayer J, Petereit J, Nair S, Casey E, Hettich R, Ceusters J, Ranjan P, Palla K, Yin H, Reyes-Garcia C, Andrade J, Freschi L, Dever L, Boxall S, Walker J, Davies J, Bupphada P, Kadu N, Winter K, Sage R, Aguilar C, Schmutz J, Jenkins J, Holtum J (2015) A roadmap for research on crassulacean acid metabolism (CAM) to enhance sustainable food and bioenergy production in a hotter drier world. New Phytol 207:491–504PubMedCrossRefGoogle Scholar
  141. Yoon YJ, Mobin M, Hahn EJ, Paek KY (2009) Impact of in vitro CO2 enrichment and sugar deprivation on acclamatory responses of Phalaenopsis plantlets to ex vitro conditions. Environ Exp Bot 65:183–188CrossRefGoogle Scholar
  142. Yu SM (1999) Cellular and genetic responses of plants to sugar starvation. Plant Physiol 121:687–693PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Nathalie Ceusters
    • 1
  • Wim Van den Ende
    • 2
  • Johan Ceusters
    • 1
    Email author
  1. 1.Faculty of Engineering Technology, Department of Microbial and Molecular SystemsBioengineering Technology TC, KU LeuvenGeelBelgium
  2. 2.Faculty of Sciences, Department of BiologyLaboratory of Molecular Plant Biology, KU LeuvenLeuvenBelgium

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