Advertisement

Connecting Environmental Stimuli and Crassulacean Acid Metabolism Expression: Phytohormones and Other Signaling Molecules

  • Luciano Freschi
  • Helenice MercierEmail author
Chapter
Part of the Progress in Botany book series (BOTANY, volume 73)

Abstract

Plasticity in Crassulacean acid metabolism (CAM) expression has long been recognized to occur both within and between species, and a range of environmental cues is implicated in both long- and short-term regulation of CAM operation. Important insights into the signal transduction chains between environmental stimuli and CAM expression are now available, and our discussion is focused on these recent findings. The role of plant hormones, nitric oxide, reactive oxygen species, intracellular calcium, protein phosphatases, and kinases in the signaling cascades leading to changes in CAM expression in response to water availability, salinity, light intensity, and photo- and thermoperiod is discussed. Whenever possible, differences and similarities among the signaling elements controlling CAM expression in distinct CAM plant models are highlighted. Conceivably, many other aspects of the signaling processes leading to CAM expression are still to be elucidated; therefore, some potential strategies to improve our knowledge in this field are briefly discussed.

Keywords

Salt Stress Crassulacean Acid Metabolism Crassulacean Acid Metabolism Plant Pineapple Plant Crassulacean Acid Metabolism Species 
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.

References

  1. Barker DH, Marszalek J, Zimpfer JF, Adams WW (2004) Changes in photosynthetic pigment composition and absorbed energy allocation during salt stress and CAM induction in Mesembryanthemum crystallinum. Funct Plant Biol 31:781–787Google Scholar
  2. Behzadipour M, Ratajczak R, Faist K, Pawlitschek P, Trémolières A, Kluge M (1998) Phenotypic adaptation of tonoplast fluidity to growth temperature in the CAM plant Kalanchoë daigremontiana Ham. et Per. is accompanied by changes in the membrane phospholipid and protein composition. J Membr Biol 166:61–70PubMedGoogle Scholar
  3. Black CC, Osmond CB (2003) Crassulacean acid metabolism photosynthesis: ‘working the night shift’. Photosynth Res 76:329–341PubMedGoogle Scholar
  4. Bohnert HJ, Cushman JC (2000) The ice plant cometh: lessons in abiotic stress tolerance. J Plant Growth Regul 19:334–346Google Scholar
  5. Borland AM, Dodd AN (2002) Carbohydrate partitioning in Crassulacean acid metabolism plants: reconciling potential conflicts of interest. Funct Plant Biol 29:707–716Google Scholar
  6. Borland AM, Taybi T (2004) Synchronization of metabolic processes in plants with Crassulacean acid metabolism. J Exp Bot 55:1255–1265PubMedGoogle Scholar
  7. 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 121:889–896PubMedGoogle Scholar
  8. Borland A, Elliott S, Patterson S, Taybi T, Cushman J, Pater B, Barnes J (2006) Are the metabolic components of Crassulacean acid metabolism up-regulated in response to an increase in oxidative burden? J Exp Bot 57:319–328PubMedGoogle Scholar
  9. 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. Funct Plant Biol 29:13–23Google Scholar
  10. Brulfert J, Guerrier D, Queiroz O (1975) Photoperiodism and enzyme rhythms: kinetic characteristics of photoperiodic induction of Crassulacean acid metabolism. Planta 125:33–44Google Scholar
  11. Brulfert J, Guerrier D, Queiroz O (1982) Photoperiodism and Crassulacean acid metabolism. 2. Relations between leaf aging and photoperiod in Crassulacean acid metabolism induction. Planta 154:332–338Google Scholar
  12. Brulfert J, Guclu S, Taybi T, Pierre JN (1993) Enzymatic responses to water stress in detached leaves of the CAM plant Kalanchoë blossfeldiana Poelln. Plant Physiol Biochem 31:491–497Google Scholar
  13. Brulfert J, Ravelomanana D, Guclu S, Kluge M (1996) Ecophysiological studies in Kalanchoë porphyrocalyx (Baker) and K. miniata (Hils et Bojer), two species performing highly flexible CAM. Photosynth Res 49:29–36Google Scholar
  14. Cela J, Arrom L, Munne-Bosch S (2009) Diurnal changes in photosystem II photochemistry, photoprotective compounds and stress-related phytohormones in the CAM plant, Aptenia cordifolia. Plant Sci 177:404–410Google Scholar
  15. Cheng SH, Edwards GE (1991) Influence of long photoperiods on plant development and expression of Crassulacean acid metabolism in Mesembryanthemum crystallinum. Plant Cell Environ 14:271–278Google Scholar
  16. Christopher JT, Holtum JAM (1996) Patterns of carbon partitioning in leaves of Crassulacean acid metabolism species during deacidification. Plant Physiol 112:393–399PubMedGoogle Scholar
  17. Chu C, Dai ZY, Ku MSB, Edwards GE (1990) Induction of Crassulacean acid metabolism in the facultative halophyte Mesembryanthemum crystallinum by abscisic acid. Plant Physiol 93:1253–1260PubMedGoogle Scholar
  18. Cockburn W, Whitelam GC, Broad A, Smith J (1996) The participation of phytochrome in the signal transduction pathway of salt stress responses in Mesembryanthemum crystallinum L. J Exp Bot 47:647–653Google Scholar
  19. Crayn DM, Winter K, Smith JAC (2004) Multiple origins of Crassulacean acid metabolism and the epiphytic habit in the Neotropical family Bromeliaceae. Proc Natl Acad Sci USA 101:3703–3708PubMedGoogle Scholar
  20. Cushman JC (2001) Crassulacean acid metabolism. A plastic photosynthetic adaptation to arid environments. Plant Physiol 127:1439–1448PubMedGoogle Scholar
  21. Cushman JC, Bohnert HJ (1992a) Salt stress alters A/T-rich DNA-binding factor interactions within the phosphoenolpyruvate carboxylase promoter from Mesembryanthemum crystallinum. Plant Mol Biol 20:411–424PubMedGoogle Scholar
  22. Cushman JC, Bohnert HJ (1992b) Salt stress induction of Crassulacean acid metabolism in a facultative CAM plant. Photosynth Res 34:103–103Google Scholar
  23. Cushman JC, Bohnert HJ (1999) Crassulacean acid metabolism: molecular genetics. Annu Rev Plant Physiol Plant Mol Biol 50:305–332PubMedGoogle Scholar
  24. Cushman J, Bohnert HJ (2004) Induction of Crassulacean acid metabolism by salinity – molecular aspects. In: Läuchli A, Lüttge U (eds) Salinity: environment – plants – molecules. Kluwer, Dordrecht, pp 361–393Google Scholar
  25. Cushman JC, Borland AM (2002) Induction of Crassulacean acid metabolism by water limitation. Plant Cell Environ 25:295–310PubMedGoogle Scholar
  26. Cushman JC, Michalowski CB, Bohnert HJ (1990) Developmental control of Crassulacean acid metabolism inducibility by salt stress in the common ice plant. Plant Physiol 94:1137–1142PubMedGoogle Scholar
  27. Dai Z, Ku MSB, Zhang DZ, Edwards GE (1994) Effects of growth regulators on the induction of Crassulacean acid metabolism in the facultative halophyte Mesembryanthemum crystallinum L. Planta 192:287–294Google Scholar
  28. Dyachenko OV, Zakharchenko NS, Shevchuk TV, Bohnert HJ, Cushman JC, Buryanov YI (2006) Effect of hypermethylation of CCWGG sequences in DNA of Mesembryanthemum crystallinum plants on their adaptation to salt stress. Biochemistry 71:461–465PubMedGoogle Scholar
  29. Eastmond PJ, Ross JD (1997) Evidence that the induction of Crassulacean acid metabolism by water stress in Mesembryanthemum crystallinum (L.) involves root signalling. Plant Cell Environ 20:1559–1565Google Scholar
  30. Edwards GE, Dai Z, Cheng SH, Mu MSB (1996) Factors affecting the induction of Crassulacean acid metabolism in Mesembryanthemum crystallinum. In: Winter K, Smith JAC (eds) Crassulacean acid metabolism: biochemistry, ecophysiology and evolution, vol 114. Springer, Berlin, pp 119–134Google Scholar
  31. Forsthoefel NR, Cushman MAF, Cushman JC (1995a) Posttranscriptional and posttranslational control of enolase expression in the facultative Crassulacean acid metabolism plant Mesembryanthemum crystallinum L. Plant Physiol 108:1185–1195PubMedGoogle Scholar
  32. Forsthoefel NR, Vernon DM, Cushman JC (1995b) A salinity-induced gene from the halophyte M. crystallinum encodes a glycolytic enzyme, cofactor-independent phosphoglyceromutase. Plant Mol Biol 29:213–226PubMedGoogle Scholar
  33. Franco AC, Ball E, Lüttge U (1991) The influence of nitrogen, light and water stress on CO2 exchange and organic acid accumulation in the tropical C3-CAM tree, Clusia minor. J Exp Bot 42:597–603Google Scholar
  34. Freschi L, Rodrigues MA, Domingues DS, Purgatto E, Van Sluys MA, Magalhaes JR, Kaiser WM, Mercier H (2010a) Nitric oxide mediates the hormonal control of Crassulacean acid metabolism expression in young pineapple plants. Plant Physiol 152:1971–1985PubMedGoogle Scholar
  35. Freschi L, Takahashi CA, Cambui CA, Semprebom TR, Cruz AB, Mioto PT, Versieux LD, Calvente A, Latansio-Aidar SR, Aidar MPM, Mercier H (2010b) Specific leaf areas of the tank bromeliad Guzmania monostachia perform distinct functions in response to water shortage. J Plant Physiol 167:526–533PubMedGoogle Scholar
  36. 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 174:453–461Google Scholar
  37. Gehrig HH, Aranda J, Cushman MA, Virgo A, Cushman JC, Hammel BE, Winter K (2003) Cladogram of Panamanian Clusia based on nuclear DNA: implications for the origins of Crassulacean acid metabolism. Plant Biol 5:59–70Google Scholar
  38. Grams TEE, Thiel S (2002) High light-induced switch from C3-photosynthesis to Crassulacean acid metabolism is mediated by UV-A/blue light. J Exp Bot 53:1475–1483PubMedGoogle Scholar
  39. Gregory FG, Spear I, Thimann KV (1954) The interrelation between CO2 metabolism and photoperiodism in Kalanchoë. Plant Physiol 29:220–229PubMedGoogle Scholar
  40. Guralnick LJ, Ting IP (1986) Seasonal response to drought and rewatering in Portulacaria afra (L.) Jacq. Oecologia 70:85–91Google Scholar
  41. Guralnick LJ, Ku MSB, Edwards GE, Strand D, Hockema B, Earnest J (2001) Induction of PEP carboxylase and Crassulacean acid metabolism by gibberellic acid in Mesembryanthemum crystallinum. Plant Cell Physiol 42:236–239PubMedGoogle Scholar
  42. Haag-Kerwer A, Franco AC, Lüttge U (1992) The effect of temperature and light on gas-exchange and acid accumulation in the C3-CAM plant Clusia minor L. J Exp Bot 43:345–352Google Scholar
  43. Halliday KJ, Fankhauser C (2003) Phytochrome-hormonal signalling networks. New Phytol 157:449–463Google Scholar
  44. Hare PD, Cress WA, van Staden J (1997) The involvement of cytokinins in plant responses to environmental stress. J Plant Growth Regul 23:79–103Google Scholar
  45. Herppich W, Herppich M, Vonwillert DJ (1992) The irreversible C3 to CAM shift in well-watered and salt-stressed plants of Mesembryanthemum crystallinum is under strict ontogenic control. Bot Acta 105:34–40Google Scholar
  46. Herrera A (1999) Effects of photoperiod and drought on the induction of Crassulacean acid metabolism and the reproduction of plants of Talinum triangulare. Can J Bot 77:404–409Google Scholar
  47. Herrera A (2009) Crassulacean acid metabolism and fitness under water deficit stress: if not for carbon gain, what is facultative CAM good for? Ann Bot (London) 103:645–653Google Scholar
  48. Herrera A, Ballestrini C, Tezara W (2008) Nocturnal sap flow in the C3-CAM species, Clusia minor. Trees 22:491–497Google Scholar
  49. Herzog B, Hoffmann S, Hartung W, Lüttge U (1999) Comparison of photosynthetic responses of the sympatric tropical C3 species Clusia multiflora H. B. K. and the C3-CAM intermediate species Clusia minor L. to irradiance and drought stress in a phytotron. Plant Biol 1:460–470Google Scholar
  50. Huang NC, Li CH, Lee JY, Yen HE (2010) Cytosine methylation changes in the ice plant Ppc1 promoter during transition from C3 to Crassulacean acid metabolism. Plant Sci 178:41–46Google Scholar
  51. Hurst AC, Grams TEE, Ratajczak R (2004) Effects of salinity, high irradiance, ozone, and ethylene on mode of photosynthesis, oxidative stress and oxidative damage in the C3/CAM intermediate plant Mesembryanthemum crystallinum L. Plant Cell Environ 27:187–197Google Scholar
  52. Ishitani M, Xiong LM, Stevenson B, Zhu JK (1997) Genetic analysis of osmotic and cold stress signal transduction in Arabidopsis: interactions and convergence of abscisic acid-dependent and abscisic acid-independent pathways. Plant Cell 9:1935–1949PubMedGoogle Scholar
  53. Keeley JE, Rundel PW (2003) Evolution of CAM and C4 carbon-concentrating mechanisms. Int J Plant Sci 164:S55–S77Google Scholar
  54. Kliemchen A, Schomburg M, Galla H-J, Lüttge U, Kluge M (1993) Adaptive changes in the fluidity of a tonoplast membrane of a CAM plant. Planta 189:403–409Google Scholar
  55. Kluge M, Wolf H, Fischer A (1991) Crassulacean acid metabolism: temperature effects on the lag-phase in the photosynthetic oxygen evolution occurring at the outset of the light period. Plant Physiol Biochem 29:83–90Google Scholar
  56. Kornas A, Miszalski Z, Surowka E, Fischer-Schliebs E, Lüttge U (2010) Light stress is not effective to enhanced Crassulacean acid metabolism. Z Naturforsch C 65:79–86PubMedGoogle Scholar
  57. Kuznetsov V, Shorina M, Aronova E, Stetsenko L, Rakitin V, Shevyakova N (2007) NaCl- and ethylene-dependent cadaverine accumulation and its possible protective role in the adaptation of the common ice plant to salt stress. Plant Sci 172:363–370Google Scholar
  58. Leung J, Merlot S, Giraudat J (1997) The Arabidopsis ABSCISIC ACID-INSENSITIVE2 (ABI2) and ABI1 genes encode homologous protein phosphatases 2C involved in abscisic acid signal transduction. Plant Cell 9:759–771PubMedGoogle Scholar
  59. Lüttge U (1993) The role of Crassulacean acid metabolism (CAM) in the adaptation of plants to salinity. New Phytol 125:59–71Google Scholar
  60. Lüttge U (2000) Light-stress and Crassulacean acid metabolism. Phyton 40:65–82Google Scholar
  61. Lüttge U (2004a) Ecophysiology of Crassulacean acid metabolism (CAM). Ann Bot (London) 93:629–652Google Scholar
  62. Lüttge U (2004b) Performance of plants with C4-carboxylation modes of photosynthesis under salinity. In: Läuchli A, Lüttge U (eds) Salinity: environment – plants – molecules. Kluwer, Dordrecht, pp 341–360Google Scholar
  63. Lüttge U (2006) Photosynthetic flexibility and ecophysiological plasticity: questions and lessons from Clusia, the only CAM tree, in the neotropics. New Phytol 171:7–25PubMedGoogle Scholar
  64. Lüttge U, Beck F (1992) Endogenous rhythms and chaos in Crassulacean acid metabolism. Planta 188:28–38Google Scholar
  65. Maxwell K (2002) Resistance is useful: diurnal patterns of photosynthesis in C3 and Crassulacean acid metabolism epiphytic bromeliads. Funct Plant Biol 29:679–687Google Scholar
  66. Maxwell C, Griffiths H, Young AJ (1994) Photosynthetic acclimation to light regime and water stress by the C3-CAM epiphyte Guzmania monostachia: gas-exchange characteristics, photochemical efficiency and the xanthophyll cycle. Funct Ecol 8:746–754Google Scholar
  67. Maxwell K, Marrison JL, Leech RM, Griffiths H, Horton P (1999) Chloroplast acclimation in leaves of Guzmania monostachia in response to high light. Plant Physiol 121:89–95PubMedGoogle Scholar
  68. McElwain EF, Bohnert HJ, Thomas JC (1992) Light moderates the induction of phosphoenolpyruvate carboxylase by NaCl and abscisic acid in Mesembryanthemum crystallinum. Plant Physiol 99:1261–1264PubMedGoogle Scholar
  69. Merlot S, Gosti F, Guerrier D, Vavasseur A, Giraudat J (2001) The ABI1 and ABI2 protein phosphatases 2C act in a negative feedback regulatory loop of the abscisic acid signalling pathway. Plant J 25:295–303PubMedGoogle Scholar
  70. Meyer K, Leube MP, Grill E (1994) A protein phosphatase 2C involved in ABA signal transduction in Arabidopsis thaliana. Science 264:1452–1455PubMedGoogle Scholar
  71. Miszalski Z, Slesak I, Niewiadomska E, Baczek-Kwinta R, Lüttge U, Ratajczak 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 21:169–179Google Scholar
  72. Miszalski Z, Niewiadomska E, Slesak I, Lüttge U, Kluge M, Ratajczak R (2001) The effect of irradiance on carboxylating/decarboxylating enzymes and fumarase activities in Mesembryanthemum crystallinum L. exposed to salinity stress. Plant Biol 3:17–23Google Scholar
  73. Miyazaki S, Koga R, Bohnert HJ, Fukuhara T (1999) Tissue- and environmental response-specific expression of 10 PP2C transcripts in Mesembryanthemum crystallinum. Mol Gen Genet 261:307–316PubMedGoogle Scholar
  74. Neales TF, Sale PJM, Meyer CP (1980) Carbon dioxide assimilation by pineapple plants, Ananas comosus (L) Merr. 2. Effects of variation of the day/night temperature regime. Aust J Plant Physiol 7:375–385Google Scholar
  75. Nievola CC, Kraus JE, Freschi L, Souza BM, Mercier H (2005) Temperature determines the occurrence of CAM or C3 photosynthesis in pineapple plantlets grown in vitro. In Vitro Cell Dev Biol 41:832–837Google Scholar
  76. Niewiadomska E, Borland AM (2008) Crassulacean acid metabolism: a cause or consequence of oxidative stress in planta? In: Lüttge U, Beyschlag W, Murata J (eds) Progress in botany, vol 69. Springer, Heidelberg, pp 247–266Google Scholar
  77. Niewiadomska E, Miszalski Z, Slesak I, Ratajczak R (1999) Catalase activity during C3-CAM transition in Mesembryanthemum crystallinum L. leaves. Free Radic Res 31:S251–S256PubMedGoogle Scholar
  78. Niewiadomska E, Pater B, Miszalski Z (2002) Does ozone induce a C3-CAM transition in Mesembryanthemum crystallinum leaves? Phyton 42:69–78Google Scholar
  79. Niewiadomska E, Karpinska B, Romanowska E, Slesak I, Karpinski S (2004) A salinity-induced C3-CAM transition increases energy conservation in the halophyte Mesembryanthemum crystallinum L. Plant Cell Physiol 45:789–794PubMedGoogle Scholar
  80. Osmond CB (1978) Crassulacean acid metabolism. Curiosity in context. Annu Rev Plant Physiol 29:379–414Google Scholar
  81. Patel A, Ting IP (1987) Relationship between respiration and CAM-cycling in Peperomia camptotricha. Plant Physiol 84:640–642PubMedGoogle Scholar
  82. Peters W, Beck E, Piepenbrock M, Lenz B, Schmitt JM (1997) Cytokinin as a negative effector of phosphoenolpyruvate carboxylase induction in Mesembryanthemum crystallinum. J Plant Physiol 151:362–367Google Scholar
  83. Piepenbrock M, Schmitt JM (1991) Environmental control of phosphoenolpyruvate carboxylase induction in mature Mesembryanthemum crystallinum L. Plant Physiol 97:998–1003PubMedGoogle Scholar
  84. Piepenbrock M, Vonalbert C, Schmitt JM (1994) Decreasing leaf water content induces Crassulacean acid metabolism in well-irrigated Mesembryanthemum crystallinum. Photosynthetica 30:623–628Google Scholar
  85. Pospisilova J, Synkova H, Rulcova J (2000) Cytokinins and water stress. Biol Plantarum 43:321–328Google Scholar
  86. Pospisilova J, Vagner M, Malbeck J, Travniakova A, Batkova P (2005) Interactions between abscisic acid and cytokinins during water stress and subsequent rehydration. Biol Plantarum 49:533–540Google Scholar
  87. Riera M, Valon C, Fenzi F, Giraudat J, Leung J (2005) The genetics of adaptive responses to drought stress: abscisic acid-dependent and abscisic acid-independent signalling components. Physiol Plantarum 123:111–119Google Scholar
  88. Rodriguez PL, Benning G, Grill E (1998) ABI2, a second protein phosphatase 2C involved in abscisic acid signal transduction in Arabidopsis. FEBS Lett 421:185–190PubMedGoogle Scholar
  89. Ruess BR, Ferrari S, Eller BM (1988) Water economy and photosynthesis of the CAM plant Senecio medley-woodii during increasing drought. Plant Cell Environ 11:583–589Google Scholar
  90. Sato K, Ohsato H, Izumi S, Miyazaki S, Bohnert HJ, Moriyama H, Fukuhara T (2007) Diurnal expression of five protein phosphatase type 2C genes in the common ice plant, Mesembryanthemum crystallinum. Funct Plant Biol 34:581–588Google Scholar
  91. Schmitt JM, Piepenbrock M (1992) Regulation of phosphoenolpyruvate carboxylase and Crassulacean acid metabolism induction in Mesembryanthemum crystallinum L by cytokinin. Modulation of leaf gene expression by roots? Plant Physiol 99:1664–1669PubMedGoogle Scholar
  92. Schmitt J, Fisslthaler B, Sheriff A, Lenz B, Bässler M, Meyer G (1996) Environmental control of CAM induction in Mesembryanthemum crystallinum: a role for cytokinin, abscisic acid and jasmonate? In: Winter K, Smith JAC (eds) Crassulacean acid metabolism: biochemistry, ecophysiology and evolution, vol 114. Springer, Berlin, pp 159–175Google Scholar
  93. Silvera K, Santiago LS, Winter K (2005) Distribution of Crassulacean acid metabolism in orchids of Panama: evidence of selection for weak and strong modes. Funct Plant Biol 32:397–407Google Scholar
  94. Silvera K, Neubig KM, Whitten WM, Williams NH, Winter K, Cushman JC (2010) Evolution along the Crassulacean acid metabolism continuum. Funct Plant Biol 37:995–1010Google Scholar
  95. Sipes DL, Ting IP (1985) Crassulacean acid metabolism and Crassulacean acid metabolism modifications in Peperomia camptotricha. Plant Physiol 77:59–63PubMedGoogle Scholar
  96. Slesak I, Miszalski Z, Karpinska B, Niewiadomska E, Ratajczak R, Karpinski S (2002) Redox control of oxidative stress responses in the C3-CAM intermediate plant Mesembryanthemum crystallinum. Plant Physiol Biochem 40:669–677Google Scholar
  97. Slesak I, Karpinska B, Surowka E, Miszalski Z, Karpinski S (2003) Redox changes in the chloroplast and hydrogen peroxide are essential for regulation of C3-CAM transition and photooxidative stress responses in the facultative CAM plant Mesembryanthemum crystallinum L. Plant Cell Physiol 44:573–581PubMedGoogle Scholar
  98. Slesak I, Libik M, Miszalski Z (2008) The foliar concentration of hydrogen peroxide during salt-induced C3-CAM transition in Mesembryanthemum crystallinum L. Plant Sci 174:221–226Google Scholar
  99. Stetsenko LA, Rakitin VY, Shevyakova NI, Kuznetsov VV (2009) Organ-specific changes in the content of free and conjugated polyamines in Mesembryanthemum crystallinum plants under salinity. Russ J Plant Physiol 56:808–813Google Scholar
  100. Taisma MA, Herrera A (2003) Drought under natural conditions affects leaf properties, induces CAM and promotes reproduction in plants of Talinum triangulare. Interciencia 28:292–297Google Scholar
  101. Tanaka Y, Sano T, Tamaoki M, Nakajima N, Kondo N, Hasezawa S (2006) Cytokinin and auxin inhibit abscisic acid-induced stomatal closure by enhancing ethylene production in Arabidopsis. J Exp Bot 57:2259–2266PubMedGoogle Scholar
  102. Taybi T, Cushman JC (1999) Signaling events leading to Crassulacean acid metabolism induction in the common ice plant. Plant Physiol 121:545–555PubMedGoogle Scholar
  103. Taybi T, Cushman JC (2002) Abscisic acid signaling and protein synthesis requirements for phosphoenolpyruvate carboxylase transcript induction in the common ice plant. J Plant Physiol 159:1235–1243Google Scholar
  104. Taybi T, Sotta B, Gehrig H, Guclu S, Kluge M, Brulfert J (1995) Differential effects of abscisic acid on phosphoenolpyruvate carboxylase and CAM operation in Kalanchoë blossfeldiana. Bot Acta 108:240–246Google Scholar
  105. Taybi T, Patil S, Chollet R, Cushman JC (2000) A minimal serine/threonine protein kinase circadianly regulates phosphoenolpyruvate carboxylase activity in Crassulacean acid metabolism-induced leaves of the common ice plant. Plant Physiol 123:1471–1481PubMedGoogle Scholar
  106. Taybi T, Cushman JC, Borland AM (2002) Environmental, hormonal and circadian regulation of Crassulacean acid metabolism expression. Funct Plant Biol 29:669–678Google Scholar
  107. Taybi T, Nimmo HG, Borland AM (2004) Expression of phosphoenolpyruvate carboxylase and phosphoenolpyruvate carboxylase kinase genes. Implications for genotypic cavacity and phenotypic plasticity in the expression of Crassulacean acid metabolism. Plant Physiol 135:587–598PubMedGoogle Scholar
  108. Thomas JC, Bohnert HJ (1993) Salt stress perception and plant growth regulators in the halophyte Mesembryanthemum crystallinum. Plant Physiol 103:1299–1304PubMedGoogle Scholar
  109. Thomas JC, Mcelwain EF, Bohnert HJ (1992) Convergent induction of osmotic stress responses. Abscisic acid, cytokinin, and the effects of NaCl. Plant Physiol 100:416–423PubMedGoogle Scholar
  110. Ting IP (1981) Effects of abscisic acid on CAM in Portulacaria afra. Photosynth Res 2:39–48Google Scholar
  111. Ting IP (1985) Crassulacean acid metabolism. Annu Rev Plant Physiol 36:595–622Google Scholar
  112. Tsiantis MS, Bartholomew DM, Smith JAC (1996) Salt regulation of transcript levels for the c subunit of a leaf vacuolar H+-ATPase in the halophyte Mesembryanthemum crystallinum. Plant J 9:729–736PubMedGoogle Scholar
  113. Winter K (1973) Studies on NaCl-induced Crassulacean acid metabolism in Mesembryanthemum crystallinum. Planta 109:135–145Google Scholar
  114. Winter K, Gademann R (1991) Daily changes in CO2 and water vapor exchange, chlorophyll fluorescence, and leaf water relations in the halophyte Mesembryanthemum crystallinum during the induction of Crassulacean acid metabolism in response to high NaCl salinity. Plant Physiol 95:768–776PubMedGoogle Scholar
  115. Winter K, Holtum JAM (2007) Environment or development? Lifetime net CO2 exchange and control of the expression of Crassulacean acid metabolism in Mesembryanthemum crystallinum. Plant Physiol 143:98–107PubMedGoogle Scholar
  116. Winter K, Ziegler H (1992) Induction of Crassulacean acid metabolism in Mesembryanthemum crystallinum increases reproductive success under conditions of drought and salinity stress. Oecologia 92:475–479Google Scholar
  117. Winter K, Aranda J, Holtum JAM (2005) Carbon isotope composition and water-use efficiency in plants with Crassulacean acid metabolism. Funct Plant Biol 32:381–388Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Department of BotanyInstitute of Biosciences, University of São PauloSão PauloBrazil

Personalised recommendations